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Microangiographic, histological and radiographic study of the femoral head following experimental hip… Duncan, Clive P. 1972

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MICROANGIOGRAPHY, HISTOLOGICAL AND RADIOGRAPHIC STUDY OF THE FEMORAL HEAD FOLLOWING EXPERIMENTAL HIP DISLOCATION IN RABBITS BY . CLIVE P. DUNCAN  M.B., B.Ch., Honours, National University of Ireland, Dublin, 1968.  A THESIS SUBMITTED IN PARTIAL FULFILMENT OF THE REQUIREMENTS FOR THE DEGREE OF MASTER OF SCIENCE In the Department of SURGERY  We accept t h i s thesis as conforming to the required standard.  THE UNIVERSITY OF BRITISH COLUMBIA September, 1972  In p r e s e n t i n g t h i s  thesis  in p a r t i a l  fulfilment  o f the r e q u i r e m e n t s  an advanced degree at the U n i v e r s i t y o f B r i t i s h Columbia, the L i b r a r y  s h a l l make i t  freely available  I f u r t h e r agree t h a t p e r m i s s i o n  for  1 agree  of  representatives.  this thesis for  written  It  financial  f o r e x t e n s i v e copying o f t h i s  i s u n d e r s t o o d t h a t copying o r gain shall  permission.  Department  of  The U n i v e r s i t y o f B r i t i s h Vancouver 8, Canada  Columbia  that  r e f e r e n c e and s t u d y . thesis  f o r s c h o l a r l y purposes may be g r a n t e d by the Head o f my Department by h i s  for  or  publication  not be a l l o w e d w i t h o u t my  i.  ABSTRACT In 220 rabbits (65 mature and 155 immature) the  effects of d i s l o c a t i o n , persistant d i s l o c a t i o n and reduction at varying i n t e r v a l s (immediately, 12, 24 and 48 hours a f t e r d i s l o c a t i o n ) of the l e f t hip were studied by microangiographic, h i s t o l o g i c a l and radiographic examination. Dislocation of the l e f t hip was ihduced manually under anaesthesia by a doraally applied force with the hip held adducted and i n t e r n a l l y rotated.  Reduction was  effected  by ventral traction with the hip i n the same position. The right hip was untouched and used as a control i n a l l cases. In 135 animals, a tracer dye was infused into the abdominal aorta proximal to i t s b i f u r c a t i o n under standard conditions of temperature and pressure.  This infusion was  done at 10 minutes, and at 1, 3, 5, and 7 days a f t e r dislocation or reduction.  The femoral heads were then processed and  studied under stereomicroscopy.  H i s t o l o g i c a l and radiographic  studies were made i n the remaining 85 animals at intervals between 3 and 10 weeks a f t e r dislocation or reduction. In immature animals, severe dye perfusion deirecit was observed i n a l l cases within 10 minutes of d i s l o c a t i o n . This • was maximal i n the antero-medial h a l f of the femoral head. The defecit was  increased at 24 hours and persisted u n t i l 5  days a f t e r d i s l o c a t i o n . At the seventh day recovery had commenced.  A profound perfusion defectt was also noted within  10 minuted of immediate reduction, however, recovery was observed at 24 hours and was almost complete at 5 - 7 days. The rate of recovery i n those animals In which the d i s l o c a t i o n was reduced at 12, 24 and 48 hours did not d i f f e r from that observed i n unreduced animals.  In adult animals, s i g n i f i c a n t  c i r c u l a t o r y disturbance was infrequently observed a f t e r  ii.  d i s l o c a t i o n and persistant d i s l o c a t i o n . Consequently, the b e n e f i c i a l effects of reduction, i f any, were obscured. The epiphyseo-metaphyseal vascular anastomoses across the  epiphyseal  scar were f i l l e d with dye i n a l l mature rabbits and seemed to act as a route of blood supply and drainage i n adult animals.. Extensive h i s t o l o g i c a l avascular necrosis of the hi^ad was  observed i n the majority of animals, but  femoral  was  s i g n i f i c a n t l y nidre common i n immature rabbits •. Less extensive and less common avascular necrosis was  observed i n immature  animals a f t e r immediate reduction. However, reduction  delayed  to 12 hours or l a t e r was not associated with a lower incidence of bone death. Abnormal r a d i o l o g i c a l findings were common.jaad varied. S p e c i f i c a l t e r a t i o n i n density and outline of the  femoral  head was however infrequently observed, but corelated well with the h i s t o l o g i c a l findings. Decreased bariiodensity was  associated  with inbalanced bone resorption and hyperaemia,and increased radiodensity with bone death and new  bone apposition.  It i s concluded that traumatic d i s l o c a t i o n causes embarassment and sequential changes i n the c i r c u l a t i o n within the femoral head i n rabbits.  The perfusion defecit i s more  severe i n immature animals as the intra-osseous  epiphysea-  metaphyseal vessels minimize this c i r c u l a t o r y distrubance i n adult animals. Early reduction enhances early and complete recovery of blood supply i n immature animals. Varying degrees of avascular necrosis of the femoral head occur i n both adult and immature animals with and without reduction, but i s more common and extensive i n immature animals. Abnormal r a d i o l o g i c a l features within the femoral head are infrequently observed up to ten weeks a f t e r d i s l o c a t i o n but c o r r e l a t e well with h i s t o l o g i c a l findings when present.  the  iii.  INDEX OF CONTENTS Page I. II.  INTRODUCTION AND PURPOSE OF THE STUDY  1  REVIEW OF THE LITERATURE  3  H I T . BONE CIRCULATION  3  Anatomy -- General  4  -- The femoral Head i n Man  13  -- Comparative Anatomy  22  -- Functional Importance i n Man and Animals Physiology-General...  37  -The Femoral Head TRAUMATIC DISLOACTION OF THE HIP Clinical  32  41 43  - 35a Man - C l a s s i f i c a t i o n . . . .  44  Adults  45  Children  47  Avascular Necrosis....... 49 Experimental - In Animals.....  III.  MATERIALS AND METHODS The Experimental Model Investigation - A. Microangiography  54  57 57 .... 58  B. Histology  66  C. Radiography...  68  iv.  Page IV.  71  RESULTS. .  71  A. Microangiography  71  Normal Uninjured Rabbits. Dislocation and reduction, Immature  71  Animals Dislocation and reduction, mature Animals. . , .  79  Reduction at 12 hours, mature 81  and Immature animals  V. VI. VII. VIII.  B. Histology  81  C. Radiology  ...87  General  87  Comparative  89  i  DISCUSSION SUMMARY  92  ,  HI 113  CONCLUSIONS BIBLI0GRAF9Y  1  2  7  V.  INDEX OF FIGURES Page 1. (a). Radiograph. Section of the Adult Human Femoral Head and Neck i n the Frontal Plane  2.  Xb). Diagramatic I l l u s t r a t i o n of the Metaphyseal and Epiphyseal Constituents of the Femoral Head  16  Microarteriogram of the Proximal Human Adult Femur  19  3. (a). Microarteriogram of the Adult Proximal Canine Femur (b) Microangiogram of the Immature Canine Head and Neck of Femur 4.  16  24 •.. 24  Microarteriogram of the Proximal Rabbit Femur  27  High Magnification Microarteriogram of the Proximal Rabbit Femur  27  6.  Microarteriograms of the Rabbit FMmur  28  7.  High Magnification Chinese Ink Microangiogram of the Juxta-articular Vascular system of the Femoral Head i n the Rabbit 30  5.  8. (a). Microangiogram of the Immature Rabbit Femoral Head (b). Microangiogram of the Adult Rabbit Femoral Head  31 31  vi.  Page  9. 10.  11.  12.  13.  14.  15.  16.  1?.  18.  19.  20.  The General Set Up of the Infusion  60  The Bladder Before and After Satisfactory Perfusion with Dye  61  The Posterior Aspect of the Proximal Femora A f t e r Dislocation of the Left Hip and Infusion  62  The F i n a l Preparation Before StereoMicroscopic Analysis  62  High Magnification of the F i n a l Preparations before Stereomicroscopic Analysis  63  Anterior Aspect of the Right and Left Proximal Femora a f t e r Long-term unreduced Dislocation of the Left Hip  67  Antero-posterior x-ray of the Pelvis and Hips within."48 hours of Unreduced d i s l o c a t i o n of the Left Hip  67  Qualitative analysis of Dye Perfusion of the Femoral Head  69  Qualitative analysis of D£e Perfusion of the Femoral Head  69  Qualitative analysis of Dye of the Femoral Head  70  Perfusion  Semiquantitative analysis of Dye Perfusion of the Femoral Head  70  The Results of Unreduced Dislocation in Immature Rabbits at 10 minutes and 24 hours a f t e r Dislocation  73  vii.  Page  21.  22.  23.  24.  25.  26.  27.  28.  29.  The Microangiographic Pattern 7 Days following Unreduced Dislocation in Immature Rabbits  74  The Microangiographic Pattern i n Immature Animals at 10 minutes a f t e r Immediate reduction and 10 minutes a f t e r Unreduced d i s l o c a t i o n  76  The Microangiographic Pattern i n Immature Animals at 24 hours a f t e r Immediate Reduction and 7 days a f t e r Unreduced d i s l o c a t i o n  77  The Microangiographic Pattern i n Immature Animals at 5 days and 7 days following Immediate Reduction  78  The Microangiographic Pattern in Mature Rabbits at 10 minutes and 7 days a f t e r Unreduced Dislocation  80  H i s t o l o g i c a l Section (H.&E.) of the Normal Femoral Head  83  H i s t o l o g i c a l Section of the Left Femoral Head following Prolonged Unreduced Dislocation  83  H i s t o l o g i c a l Section of the Left Femoral Head following Dislocation  85  High Power Photomicrograph from Left Femoral Head  85  Dislocated  viii.  Page 30.  31.  32.  33.  Analysis of the H i s t o l o g i c a l Findings  86  In V i t r o Radiograph of the Right and Left Proximal Femora from an Adult Rabbit Eight Weeks following d i s l o c a t i o n , and Reduction at 24 hours  90  In V.ftro Radiograph of the Proximal Femora from an Adult Rabbit with long-term Unreduced Dislocation of the Left Hip....  91  H i s t o l o g i c a l Sections of the Femoral Head following Infusion  95  ix. TABLES Page 1,  II. III.  C l i n i c o Radiological outcome i n 207 Hips following Traumatic Posterior Dislocation  116  Outline of Experiment I  117  „  Outline of Experiment I I  118  IV.  Outline of Experiment III  119  V.  Outline of Experiment IV.  120  Outline of Long-term Animals f o r H i s t o l o g i c a l Examination  121  Outline of Short-term Animals f o r H i s t o l o g i c a l Examination  122  The Effect of Skeletal Maturity at the Time of Injury on the H i s t o l o g i c a l Outcome, Regardless of Reduction  123  The influence of Reduction on the H i s t o l o g i c a l Outcome, Regardless of Skeletal Maturity  124  The Influence of Early Reduction on the H i s t o l o g i c a l Outcome, regardless of Skeletal Maturity...  125  VI.  VII.  VIII.  IX.  X.  XI.  The Influence of Both Skeletal Maturity and Treatment on the Incidence of Total or Subtotal H i s t o l o g i c a l Avascular Necrosis  ..126  X.  ACKNOWLEDGEMENTS Thie masters dissertation culminates from the efforts of not one i n d i v i d u a l , but of many.  The author wishes to  acknowledge with gratitude the assistance of a l l those who i n various ways contributed to the completion of the study. To. Dr. £>.S. Shitrijtiiy Research Sponsor, who as c r i t i c , mentor and friend gave genorously of his time and patience to provide continued guidance and encouragement at a l l stages of this work. To Dr. F.P. Patterson, Head of the Division of Orthopaedics, who created the i n i t i a l stimulus and kindly arranged what resulted i n a rewarding and enjoyable year. To Mr. George Leung, the s t a f f of the Animal  Research  Lab., and the Medical I l l u s t r a t i o n Department of the University of  B r i t i s h Columbia  for their technical assistance, and  to many colleagues and friends who helped i n various ways.  My grateful thanks to a l l .  F i n a l l y to Margaret, my wife, I owe an immeasurable debt, f o r her understanding and forebearance throughout.  1  INTRODUCTION  Traumatic d i s l o c a t i o n of the hip i n man i s not a rare injury and i t s incidence i s s t e a d i l y r i s i n g with the coincident increase i n the complexity and speed of travel The h i p i s the most stable d i a r t h - r o d i a l j o i n t and traumatic d i s l o c a t i o n must therefore imply severe injury to the surrounding soft tissues. Often this i s accompanied by bone and c a r t i l a g e injury of the femoral head and acetabulum. The hip i s furthermore the largest weight bearing j o i n t i n the body, and a l t e r a t i o n i n the congruity, composition »r function of i t s constituents induced by d i s l o c a t i o n may cause degenerative arthritis. Avascular necrosis of the femoral head, a well recognized complication of traumatic d i s l o c a t i o n , i s a potent cause »f osteo-arthritis.  The vascular anatomy of this region suggests  that damage to the blood vessels surrounding the hip i s a major factor i n the genesis * f the ischaemic necrosis. We are however ignorant of the s e r i a l c i r c u l a t o r y changes which may occur i n the femoral head following dislocation and how they a l t e r with time. C l i n i c a l studies repeatedly stress a number »f salient contributory factors which seem to a f f e c t the outcome. 1. The severity of the injury. and  2. The duration of d i s l o c a t i o n 3. The age »f the patient.  These factors are however commonly i n t e r related i n the Individual patient and so the separate Influence «f each i s uncertain.  2.  PURPOSE OF THE STUDY  1.  To establish the sequential changes i n blood supply of the femoral head following experimental traumatic d i s l o c a t i o n of the hip i n rabbits.  2.  To evaluate the influence of the duration of d i s l o c a t i o n  3.  To evaluate the influence of skeletal maturity.  4.  To evaluate the influence of reduction.  5.  To corelate these changes to the h i s t o l o g i c a l and r a d i o l o g i c a l findings.  It i s hoped this study may add important knowledge to our understanding of the problem i n man.  3,  REVIEW OF THE LITERATURE  BONE CIRCULATION  ANATOMY: General Features The Femoral Head i n Man Comparative Vascular Anatomy of The Femoral Head i n Man and Animals Functional Importance i n Mun and Animals  PHYSIOLOGY: General Features The Femoral Head  4.  ANATOMY  GENERAL FEATURES: The f i r s t suggestion that bone had a blood supply was made i n 1691 by COMPTON HAVERS ? 5  He observed how  large  vessels pierced the shaft of long bones and ramified within in close association with the marrow f a t . ALBINUS^" i n 1756 published what must be the f i r s t account of the blood supply of bone studied by the i n j e c t i o n technique.  He observed blood  vessels within a complex . system of pores i n c o r t i c a l bone. These pores had been described e a r l i e r by HAVERS"*?  and so  are now widely known as Haversian canals. Knowledge was  slow to develop however, p r i n c i p a l l y as  bone, both as a tissue and as an organ, presented almost insurmountable d i f f i c u l t i e s to the investigator. Notwithstanding these d i f f i c u l t i e s the u n t i r i n g i n t e r e s t , industry and consummate s k i l l of the e a r l i e r anatomists and t h e i r ever increasing successors i n widely diverse s c i e n t i f i c  disciplines  has today presented us with an almost unlimited wealth of information and many methods of pursuing further studies of what 121 TRUETA  aptly termed the "Development and Decay of the  Human Frame". The great bulk of our knowledge i s based on examination of  the extra-osseous and intra-osseous nature, course and  behavior of blood vessels. Such Investigation has been considerably enhanced by p r i o r infusion of the vessels with materials which render t h e i r outline more obvious to the human 5 "119 eye or x-ray beam. Many such substances have been used ' ,  among which Neoprene Latex, India Ink, Barium  Sulphate  (Micropaque), Prussian Blue have been the mbst  rewardingi  Introduction of the SPALTEHOLZ technique of allowed  the  investigator to prepare translucent sections of  demineralized bone allowing a remarkably accurate dimensional  113  bone clearance three  analysis of the vascular anatomy, e s p e c i a l l y  with the aid of stereomicroscopy.  F i n a l l y l i g h t and electron  microscopy has proven an important adjunct i n confirming what was  In most instances purely inferred by the l o c a t i o n and  behavior of blood vessels.  In p a r t i c u l a r the "thick - t h i n "  method of preparing adjacent and consecutive sections of bone has been invaluable i n formulating a composite map  of the  morphology and functional implications of bone and i t s blood , 90-125 supply. ' The c l a s s i c a l outline of the blood supply of tubular bone 68 72 was  consecutively described by LANGER  and LEXER  .  findings were »ased on gross d i s s e c t i o n , on i n j e c t i o n  Their techniques  and i n the case of LEXER, on x-ray analysis following blood vessel infusion with a mercury-turpentine emulsion. It Is now accepted  generally  that there are three major vascular systems i n  tubular bone: 1. Nutrient  diaphyseal  2. Epiphyseal and  - metaphyseal  3. Periosteal  THE NUTRIENT DIAPHYSEAL SYSTEM: One or more nutrienr a r t e r i e s enter the diaphysis of a l l long bones i n man  and animals. The number of vessels and  site  of entry vary with the bone and species under consideration.  LAING  described an almost equal incidence of one or two  nutrient vessels entering the proximal two thirds of twenty seven human femora, i n the region of the linea aspera. A l l vessels ultimately derived from the profunda femoris artery. The nutrient artery branches immediately on reaching the marrow cavity.  One superior and one i n f e r i o r branch pass  v e r t i c a l l y up and down the shaft and subdivide into a variable number of medullary branches whose orientation i s again p r i n c i p a l l y v e r t i c a l . ^  Numerous r a d i a l branches  a r i s e from these medullary arteries and pass to the adjacent marrow and cortex. On reaching the bone Bnds there i s at least a functional anastomosis between the diaphyseal and the epiphyseal - metaphyseal systems.  The l e v e l at which these  connections take place i s i n some dispute. BROOKS and HARRISON using micropaque of varying v i s c o s i t y concluded that the nutrient and the metaphyseal systems were largely d i s t i n c t and anastamosed, i f at a l l , at the p r e - c a p i l l a r y l e v e l . However s e l e c t i v e interference with the nutrient vessel i n rab was followed i n time by a restoration of blood supply to the 17' 18 shaft from the metaphyseal system. ' This vouches f o r an effective  c o l l a t e r a l system, but time dependant. 123 ,124  TRUETA and CAVADIAS  following investigation of  nutrient vessel o b l i t e r a t i o n i n rabbits'forelimb concluded that the epiphyseal-metaphyseal system i n adults, and the periosteal and metaphyseal system i n growing rabbits was quite capable of preventing i n f a r c t i o n of marrow and cortex i n the shaft.  SHIM and his associates  confirmed TRUETAS findings. 85  Using an i n d i r e c t method of Sr  clearance by bone, they  found that within f i v e minutes of nutrient diaphyseal vessel obliteration  i n the adult rabbit femur, s t i l l 30% of the blood  supply to the shaft remained. THE EPIPHYSEAL - METAPHYSEAL SYSTEM: A separate system of nutrient vessels enter at each end of a long bone and are responsible for n u t r i t i o n of the growth 122,127 125 plate i n growing bones, , the bony epiphysis , a •v, * 59>71>122 v a r i a b l e amount of the metaphysis , and perhaps the 19 basal layer of the a r t i c u l a r c a r t i l a g e . With few exceptions 1  L  (the ligamentum teres) these vessels stem from the a r t i c u l i vasculosus" described by WILLIAM HUNTER i n  "circulus 58 1743.  The function of the epiphyseal and metaphyseal moeities of this group of vessels d i f f e r .  This i s most evident in the  growing bone when the growth plate separates them. The epiphyseal vessels enter on the epiphyseal side of the growth plate (or epiphyseal scar) and c h a r a c t e r i s t i c a l l y traverse the bone so running at right angles to t h e i r diaphyseal counter parts.  While crossing the epiphysis these vessels branch and  rebranch, but continue  to anastamose profusely. Small vessels  are given o f f i n r a d i a l fashion which course d i r e c t l y towards the a r t i c u l a r c a r t i l a g e , and growth plate, continuing to anastamose and so froming arcades of vessels (similar to those seen i n the mesentery). These branches subsequently form d i s t i n c t juxta a r t i c u l a r and juxta epiphyseal vessels, end - artery i n 15>76>9Jsl25 type.  8.  The metaphyseal vessels enter on the metaphyseal side of the growth plate. They share n u t r i t i o n of the metaphysis with the terminal branches of the nutrient diaphyseal vessels. The contribution made by the metaphyseal vessels alone varies with age, species and the bone i n question. In adult man the proximal femoral neck i s supplied i n toto by perforating metaphyseal 59 71 vessels , but i n the newborn the p r i n c i p a l supply i s diaphyseal 122 TRUETA and AMATO  found that the central t h r e e - f i f t h s of the  upper t i b i a l metaphysis i n rabbits was supplied by nutrient vessels. Only the outer rim was supplied by metaphyseal vessels. Discrete f i n e branches from each source approach the hypertrophic and c a l c i f i e d layers of the growth c a r t i l a g e and -, , i .J , 122*126 there play an important r o l e i n enchondral o s s i f i c a t i o n THE PERIOSTEAL SYSTEM*  1  A double layered system of vessels may be found i n the . ^ 19^20,76,121 . , periosteum . A r i c h network of a r t e r i e s and veins derived from the adjacent the fibrous layer.  soft tissue vasculature, ramifies i n i  Several prominant vascular c i r c l e s can be  seen e n c i r c l i n g the shaft and inter-communicating with their neighbours by v e r t i c a l branches e s p e c i a l l y large at the borders of the shaft. Many small branches derive from this s u p e r f i c i a l system and form a c a p i l l a r y network i n the deeper  osteogenic  layer of the periosteum known as the cambium layer. Small 76 121 22 arteries ' ar c a p i l l a r i e s connect with the l a t t i c e work of vessels within the cortex, and so with the nutrient  diaphyseal  system. There i s no doubt that a large functional anastamosis  9, ,  90.121  exists between the periosteal and nutrient system of vessels, although controversy  continues regarding  vessel type connecting the two,  the  predominant  the r e l a t i v e contribution of  each system, and the predominant d i r e c t i o n of blood flow. VENOUS DRAINAGE OF BONE: A great number of transverse and obliquely orientated venous sinusoids and  larger t r i b u t a r i e s enter into a large  thin walled central venous sinus which courses v e r t i c a l l y through 76;121 the middle of the marrow cavity of the shaft in a l l long bones. These t r i b u t a r i e s deliver the venous side of the microcirculation into this large central c o l l e c t i n g vein.  The venous sinusoids  of the metaphysis course v e r t i c a l l y and p a r a l l e l to the a r t e r i a l branches to the growth plate. The sinusoids  progressively  c o a l i s c e ultimately forming a number of large metaphyseal t r i b u t a r i e s which on joining together would seem to form each . ^ *_ , 76;121 end of the central c o l l e c t i n g sinus. The venous blood may One  leave the bone by a number of routes.  or more large veins may  leave the shaft through emissary  foramina i n the cortex, but as TRUETA'^and MORGAN^ stressed, the diameters of such foramina do not match the potential 121 diameter of the central sinus. described  For this reason TRUETA  the great potential of the intraosseous  metaphyseal  veins to drain into the surrounding soft tissue t r i b u t a r i e s of 115 the limb. This has been confirmed by intraosseous phlebography Small emissary veins are occasionally seen traversing the cortex 19 from the central sinus but the role of the periosteal veins  10.  remains a controversial issue. periosteum  subserves  The degree to which the  the venous drainage of the cortex i s  central to the problem of the d i r e c t i o n of c o r t i c a l blood flow. The p r i n c i p a l epiphyseal venous sinuses traverse and 125 leave the bony epiphysis i n close proximity to the a r t e r i e s .  THE MICROCIRCULATION OF BONE: Morphologically the microcirculation within bone may be considered i n three parts, depending on the location. D i s t i n c t i o n may be found between the vessels i n the cortex, the marrow and the juxta a r t i c u l a r and juxta epiphyseal plate areas. This offers strong evidence i n favour of functional s p e c i a l i z a t i o n . In the cortex the predominant vessel i s a single c a p i l l a r y l i k e structure of unusual length, and approximately 15 microns 61 i n diameter . The c l a s s i c a l description of a v e r t i c a l and transverse complex of a r t e r i e s , veins and c a p i l l a r i e s has now 20 been challenged . The orientation of the c a p i l l a r i e s i s oblique and outwards through the cortex i n a sunray-like pattern radiating from a paint suggested to be the locus of the embryonic X9 22 * 28 primary centre of o s s i f i c a t i o n . '* ' Furthermore the concept of Haversian canals containing multiple vessels, both arteries 20 and veins i s s i m i l a r l y questioned. Within the marrow the pattern i s p r i n c i p a l l y sinusoidal. These sinusoids are modified c a p i l l a r i e s with a single c e l l wall and absent basement membrane. 131 WEISS  has observed  On electrom microscopic  examination  the reticuloendothelial character of the  c e l l s constituting the sinusoidal wall and their phagocytic  1 1 .  9 BLOOM and FAWCETT have described how these  properties.  c e l l s ingest carbon p a r t i c l e s from infused india ink and migrate away from their position on the vessel wall. 83 Whether these vessels are open  or closed to the surrounding  haemopoeitic tissue i s not yet s e t t l e d . Electron microscopic evidence would support the concept of an intact wall with 131*140 „ . . . 2 occasi u l t r a s t r u c t u r a l openings . Erythrocytes have occasionally 83,140 been observed constituting part of the vessel wall. Extravasation however.  of blood was not associated with this  observation  The marrow sinusoids are i n continuity with the 19.  c o r t i c a l c a p i l l a r i e s at the cortex - marrow interface. The sinusoids themselves coalesce to form larger venous sinusoids, sinuses and t r i b u t a r i e s which empty into the large c o l l e c t i n g sinuses withing  the diaphysis, metaphysis, and  epiphysis EPIPHYSEAL PLATE BLOOD SUPPLY The v i a b i l i t y of the growth plate was thought to be . . , 122*127 ^ dependent more on the epiphyseal vessels , but. i t s functional i n t e g r i t y i n contributing longitudinal growth to the metaphysis i s dependant also on an intact metaphyseal blood 122 126 supply.  The q u e s t i o n  7ic as t o whether i t s growth i n width  .89 i s due to i n t e r s t i t i a l or appositional growth i s unsettled  but c e r t a i n l y the outer rim receives i t s n u t r i t i o n from a system of small vessels adjacent to i t s covering peri chondrium^. Branches of the epiphyseal vessels pass through canals i n the lamellated bone approaching the epiphyseal epiphyseal  side of the  growth plate and terminate close to the germinal  12.  layer of c e l l s by breaking up into a spur of vessels withir 127 the c a l c i f i e d matrex . Each spur has been observed to supply the equivalent of four to ten columns of p r o l i f e r a t i n g 127 palisading chondrocytes . These vessels do not penetrate into the d n c a l c i f i e d c a r t i l a g e , but their close proximity to 121 the germinal c e l l s has prompted TRUETA  to postulate an  endothelial o r i g i n f o r the germinal chondrocytes. A very s i m i l a r and r i c h network of vessels constitute the subchondral system i n juxta a r t i c u l a r areas. Precapillary a r t e r i o l e s have been observed to pass through the subchondral bone underlying a r t i c u l a r c a r t i l a g e , but again do not penetrate • •, - 19;121 into the a r t i c u l a r c a r t i l a g e except m disease. J  On the metaphyseal  aide of the growth plate, v e r t i c a l  terminal branches of the perforating metaphyseal and nutrient 127 vessels approach the c a l c i f y i n g layer and hypertrophied layer. 121 TRUETA  described a single discrete loop f o r each column of  degenerating c e l l s .  Furthermore he proposed an open vessel  system at the terminal loop where the erythrocytes were i n direct contact with the c a r t i l a g e and entered the empty lacunae following d i s i n t i g r a t i o n of the chondrocytes. propose a f r e e l y anastomosing  Other investigators  sinusoidal system without the 21  one column, one vessel arrangement.  BROOKS and LANHEN  did  not find an open system at the terminal loop. Their electron always separated red blood c e l l s from the f i n a l transverse microscopic findings suggested that a thin l i n e of 2 endothelim septum of the growth plate.  ANDERSON and PARKER  found be  open and closed systems, but the focmer-in^'the minority.  13.  THE FEMORAL HEAD BLOOD SUPPLY IN MAN: Much data i s now available regarding the extraosseous course and intraosseous behavior of the blood vessels to the , u , ,27j30>3 27i30- 31i49i54,58,59,65 ,68,72 i80.100il20il21jl25i *i lemoral lemoral head. head. 128;129,130,132 ,135 HUNTER described the "circulus a r t i c u l i 58 68 72 vasculosus" i n 1743 and the work of LANGER and LEXER J  f  defined the epiphyseal-metaphyseal  system.  Close analysis of  the intraosseous pattern had to await considerable refinement 5 119 128 of the i n j e c t i o n technique * . TUCKER , TRUETA and 125 59 HARRISON and JUDET and h i s co-workers described the course and contribution of the vessels within the head and neck of the femur, with great uniformity,  In p a r t i c u l a r we  are indebted to the magnificent work of TRUETA and h i s colleagues for the present status of our knowledge. EXTRAflSSEOUS:  The medial circumflex femoral artery i s the  p r i n c i p a l source of blood supply to the femoral head and most commonly derives from the profunda f e m o r i s ? ^ T h e circumflex almost immediately  medial  passes p o s t e r o l a t e r a l ^ between  ileopsoas and pectineus to reach the i n f e r i o r part of the femoral neck.  In this extra-capsular position i t supplies  branches to the lesser trochanter, the suroounding muscles, a common but variable communication to the acetabular branch of the obturator artery and a number of important vessels which pierce the postero l a t e r a l attachment of the capsule and pass up the postero-inferior aspect of the femoral heck as retinacular 54 arteries.  14.  The main circumflex vessel continues up behind the femoral neck supplying further retinacular branches to the posterior neck, but the most important vessels a r i s e within the superior trochanteric notch.  These pierce the capsule and course  medially along the superior aspect of the femoral neck under the r e f l e c t i o n of the synovium and capsule. The l a t e r a l circumflex femoral artery which passes anterior to ileopsoas i s responsible for a variable number of retinacular arteries which pass medially along the anterior aspect 54  of the femoral neck . Within the capsule, a l l the retinacular wessels  partake  in the "circulus vasculosus" and from which two d i s t i n c t systems of vessels are seen to supply the femoral head.  One,  an  i n f e r i o r group, enter the i n f e r i o r neck i n two locations, medial and l a t e r a l , the medial vessels entering quite close to the 59  i n f e r i o r a r t i c u l a r margin.  A superior group s i m i l a r l y supply 59  medial and l a t e r a l perforating metaphyseal vessels  but  two  to six d i s t i n c t arteries continue medially and enter the supero-lateral part of the femoral head and are known as l a t e r a l 125  epiphyseal a r t e r i e s .  The d i s t i n c t i o n between epiphyseal and  metaphyseal vessels i s most clear i n growing bones, when the growth plate c l e a r l y separates them. Before skeletal maturity the supero-lateral epiphyseal vessels enter the femoral head 125  across the superior rim of the growth plate . CROCK believes that the anterior and posterior retinacular arteries are 3 0 31  s i g n i f i c a n t routes of blood supoly to the femoral head.  '  The significance of the ligamentum teres vessels remains a vexing problem to anatomists and orthopaedic surgeons a l i k e .  15.  The bulk of evidence based p r i n c i p a l l y on dissection, h i s t o l o g i c a l and i n j e c t i o n studies, would support their , 54;59;65;125,128;129 132 ;135 patency i n the adult., ' ' ' ' ' a  5  although some investigators claim their contribution to the 65*100 130 121 femoral head diminishes with age . * . ' * TRUETA examined t h i r t y - s i x femoral heads from separate cadavers and found no diminution i n the richness of the intraosseous a r t e r i a l tree 132 with age.  WERTHEIMER  i n a microarteriographic and  h i s t o l o g i c a l study of eighty seven cases found no evidence of v a r i a t i o n i n size of the ligamentum teres vessels with age. His results inferred that i n two thirds of cases the vessels were less than 200 mp  i n diameter and so perhaps incapable of  contributing s i g n i f i c a n t l y to the c i r c u l a t i o n over and above the fovea c e n t r a l i s . Patent vessels were demonstrated  in a l l  cases however. Whatever contribution the ligamentum teres vessels may make to the femoral head v i a b i l i t y , there seems l i t t l e doubt they are important routes of revascularization should the f i T, A • u • • 25;26;99il01 femoral head suffer ischaemic necrosis. INTRAOSSEOUS:  The femoral head i n man  constitutes  approximately two-thirds of a sphere, but bissection i n the fron plane reveals that the growth plate (or epiphyseal scar) l i e s more h o r i z o n t a l l y than a l i n e joing the superior and i n f e r i o r margins (Fig. 1).  Therefore the metaphysis makes up a  considerable proportion of the infero-medial femoral head. In adults the femoral head i s seen to have d i s t i n c t epiphyseal and metaphyseal  systems of vessels with an  intercommunicating  16.  Figure 1: (a) Radiograph. Section of the adult human femoral head and neck i n the frontal plane. (b)Diagrametic i l l u s t r a t i o n of the metaphyseal (M) and epiphyseal (E) constituents of the femoral head. L i n e a joins the superior and i n f e r i o r a r t i c u l a r margins Line 'b' indicates the "epiphyseal scar". 1  1  It*  31,125 system of vessels of varying size and number. THE FEMORAL HEAD EPIPHYSIS:  The organization of blood vessels 125  within the c a p i t a l epiphysis as defined by TRUETA and HARRISON has now  gained universal acceptance.  The l a t e r a l  epiphyseal  a r t e r i e s , derived from the superior retinacular a r t e r i e s , enter the epiphysis between the epiphyseal scar and superior a r t i c u l a r margin.  They then course downwards and medially i n a gentle  curve towards a point half-way between the fovea c e n t r a l i s and i n f e r i o r a r t i c u l a r margin (Fig. 2).  The medial epiphyseal  vessels run l a t e r a l l y i n a horizontal l i n e from their point of entrance at the fovea and r i c h l y anastomose with the l a t e r a l vessels en route.  Numerous branches from these vessels radiate  predominantly and d i r e c t l y towards the a r t i c u l a r surface forming ever increasing but smaller arcades by v i r t u e of t h e i r r i c h anastomoses.  These branches tend to leave the parent stem and  approach the a r t i c u l a r surface at right angles.  In the sub-  chondral area, a r i c h system of subchondral loops i s formed. Some branches pass through the honeycombed subchondral plate of c o r t i c a l bone to reach the basal c a l c i f i e d layer of . , 19 articular cartilage. THE FEMORAL HEAD METAPHYSIS:  This area i s supplied  p r i n c i p a l l y by the medial group of i n f e r i o r perforating metaphyseal a r t e r i e s which enter close to the i n f e r i o r a r t i c u l a r margin and course v e r t i c a l l y into the femoral head. (Fig. 2) The most medial of the superior perforating metaphyseal a r t e r i e s commonly makes an abrupt medial turn on reaching the mid-point of the femoral neck and comrsing into the femoral head shares the supply of the infero medial (or metaphyseal)part with , * • ,59 i n f e r i o r vessels. (Figure 2).  the  18.  The metaphyseal arteries supply the metaphysis by a simple 59 branching system of vessels i n contrast to the vascular 125 arcades seen within the epiphysis. The intraosseous course of the epiphyseal and metaphyseal vessels i s not influenced by the trabecular outline or 59 organization, but seems more influenced by the factors 19 121 governing t h e i r formation  i n utero. '  The morphology of the microvasculature  within the  cancellous spaces depends on the degree of haemopoeisis 121 and this varies with age.  present  In haemopoeitic marrow they form  a p r o l i f i c meshwork of profusely anastamosing wide sinusoids, within f a t t y marrow the more common outline of c a p i l l a r y networks i s reproduced.  19.  Figure2: Microarteriograia of the proximal adult human femur. The l a t e r a l epiphyseal vessels enter the femoral head under the superior a r t i c u l a r margin and traverse the epiphysis a gentle curve towards a point half-way between the fovea c e n t r a l i s and i n f e r i o r a r t i c u l a r margin. Medial epiphyseal vessels are not apparent i n this section. Inferior metaphyseal vessels enter close to the i n f e r i o r a r t i c u l a r margin and share the supply of the femoral head metaphysis with a superior metaphyseal artery which i s seen to turn abruptly medially on approaching the mid-femoral neck.  DEVELOPMENT AND VARIATION WITH AGE: 43 120 , GARDNER and GRAY  and TRUETA  ,  ,^  - ,| -  have described hov; blood  vessel containing tunnels appear within the c a r t i l a g e anlage of the c a p i t a l epiphysis during the ninth week of intra uterine 46 life.  The manner i n which they develop, whether by i n c l u s i o n  or invasion i s not c e r t a i n , but t h e i r function i s n u t r i t i o n a l . : With development these c a r t i l a g e canals become more complex and extensive, and during the t h i r d trimester bear a close resemblance to the epiphyseal system of vessels seen a f t e r b i r t h . Both horizontal superolateral and v e r t i c a l i n f e r i o r patterns appaae, and are destined to become the future l a t e r a l epiphyseal and i n f e r i o r metaphyseal systems respectively. This arrangement has been demonstrated by the i n j e c t i o n technique 19 in a foetus of 22 centimetres crown to rump length, and TRUETA described i t s constancy Following examination of 121 fourteen well=perfused foetuses and s t i l l b o r n children. Each canal contains one afferent and one efferent vessel with 19 ,120 a communicating t u f t of c a p i l l a r i e s .  '  There i s no  anastamosis between the horizontal and v e r t i c a l l y orientated canals. Ligamentum teres vessels have been demonstrated during 43 the t h i r d month of intra-uterine l i f e and s i m i l a r l y observed to increase with age. They did not however extend to any s i g n i f i c a n t depth into the epiphysis. 120 121 TRUETA  described f i v e phases i n the development  of the blood supply to the human femoral head, based on microarteriographic examination of f o r t y s i x cases during the growth period.  1. FOETAL: This he defined as the intrauterine pattern which persisted u n t i l appearance of the secondary centre of o s s i f i c a t i o n within the femoral head at four to s i x fconths following b i r t h .  2.  INFANTILE:  were two f o l d .  From s i x months to four years the changes  During the f i r s t 2 years the ligamentum teres  vessels regressed, and during the second two years, with advancement of the growth plate up the neck of the femur, the i n f e r i o r metaphyseal vessels also began to regress.  3.  INTERMEDIATE:  at approximately four years of age  the growth plate reached i t s d e f i n i t i v e position within the femoral head and offered a staunch b a r r i e r to the i n f e r i o r metaphyseal vessels.  No vessels crossed the growth c a r t i l a g e  and the ligamentum teres vessels did not enter, the epiphysis. Consequently the c a p i t a l epiphyseal v i a b i l i t y was  almost t o t a l l y  dependant on the l a t e r a l epiphyseal vessels.  4. PREADOLESCANT:  The ligamentum teres vessels returned  and anastamosed with the l a t e r a l epiphyseal vessels.  This  medial epiphyseal system however, along the ligamentum teres remained v a r i a b l e and small.  5.  ADOLESCANT:  connections  epiphyseal - metaphyseal  intraosseous  were formed following o b l i t e r a t i o n of the growth  plate, but were v a r i a b l e i n mumber, and at the small a r t e r i a l level.  VENOUS DRAINAGE OF THE FEMORAL HEAD 125 48>55 In v i t r o and i n vivo study has demonstrated that venous drainage p a r a l l e l s a r t e r i a l supply.  The medial and  l a t e r a l epiphyseal veins, and superior and i n f e r i o r metaphyseal veins drain into the obturator,circumflex femoral and g l u t e a l vessels. COMPARATIVE ANATOMY OF THE FEMORAL HEAD BLOOD SUPPLY The basic patterns of the blood supply to long bones i n 121*127 man, are similar i n other mammals.  TRUETA  i n considering  the vascular pattern i n a wide v a r i e t y of species Including man, monkey, pig, dog, cat, rabbit, guinea-pig, hen and the rat concluded that "the basic arrangement of the vasculature of bone i n a l l the animals studied i s so similar to that i n man that many of the small d e t a i l s i n sinusoids and c a p i l l a r i e s found i n the dog and rabbit can not be distinguished from those encountered i n human specimans." 38 FITZGERALD  examined the blood supply to the femoral head  in f o r t y dogs using microarteriography.  He demonstrated both  medial and l a t e r a l epiphyseal vessels and communicating metaphyseal vessels a f t e r o b l i t e r a t i o n of the growth plate. The anatomy therefore c l o s e l y resembled that i n man. HAWK 53 and SHIM confirmed the comparative anatomy i n their preliminary microangiographic  study of the canine femoral head  following traumatic dislocation and epiphyseal separation (Fig. 3) A close s i m i l a r i t y has also been demonstrated i n the pig, 6,97. especially before skeletal maturity.  23.  The vascular anatomy of the femoral head i n the rabbit w i l l be presented i n d e t a i l as i t forms the subject of the experimental model i n this thesis.  The features described  are based on the gross and microscopic anatomy as documented by LEMOINE  70  and by T R U E T A  121  *  127  respectively,  supplemented by p i l o t investigations prior to this study.  24  (b) Figure 3: India ink (a) microarteriogram of adult proximal" canine femur and (b) microangiogram of immature canine head and neck of femur. Note the close s i m i l a r i t y of (a) to the human pattern (Figure 2). The growth plate i n (b) offers an effective b a r r i e r to epiphyseo-metaohyseal connections This b a r r i e r i s not seen i n adult case.  The growing  rabbit i s i d e n t i c a l with man  in posessing  a d i s t i n c t and separate vascular anatomy of the femoral head. A large v e s s e l , a r i s i n g from the deep femoral artery, and equivalent to the medial circumflex femoral artery in descends between the pectineus  man,  and ileo-psoas muscles and  divides into a number of branches on reaching  the i n f e r o - i  medial portion of the femoral neck. Some of these branches r i c h l y anastomose with the adjacent  obturator and g l u t e a l  arteries. Three p r i n c i p a l vessels may  be constantly delineated i n  this region stemming i n whole or part from the medial circumflex artery. 1). An anterior branch which ascends anterior to the femoral neck, close to the outer attachment of the j o i n t capsule.  This vessel supplies a number of twigs  destined to become anterior retinacular a r t e r i e s and partake i n the c i r c u l u s vasculosus. 2) .A posterior branch commonly a r i s i n g from a coalescance of medial circumflex, obturator  and  gluteal vessels, which accompanies the external rotators of the hip to the posterior trochanteric notch.  This vessel plays a large role with other  vessels i n the region, and with the nutrient  diaphyseal  artery i n supplying the greater trochanter, the base of the femoral neck, and the upper diaphysis.(Fig. 4) 3) .The most important branch, a small vessel which passes under the femoral neck and almost immediately pierces the capsule postero-inferior to the neck. It d i r e c t l y ascends the neck under a d i s t i n c t mound of synovial  and fibrous tissue.  This postero-inferior artery  supplies branches to the c i r c u l u s vasculosus, further branches to the proximal metaphysis, and  finally  as the main continuation plunges deeply into the c a p i t a l epiphysis at the junction of the growth plate and femoral neck. (Figures 4 & 5). This artery therefore constitutes a true nutrient vessel to the epiphysis and corresponds to the l a t e r a l epiphyseal  vessels in man.  It i s the p r i n c i p a l route  of blood supply to the femoral head in the rabbit. The metaphysis, unlike that i n man,  receives a sizeable  contribution from the terminal radicles of the nutrient artery to the shaft, subsidized to a varying extent by perforating metaphyseal a r t e r i e s from the c i r c u l u s vasculosus. (Fig. 6)  Within the epiphysis the postero-inferior artery divides repeatedly.  epiphyseal  The branches r i c h l y anastomose  and pass forwards in fan-shaped fashion roughly p a r a l l e l to the growth plate, forming a gentle arc convex medially. Four main branches of the o r i g i n a l postero-inferior artery terminate within the anterior epiphysis. Short branches of these vessels, d i f f i c u l t to v i s u a l i z e , feed into the rich sinusoidal network of the concellous  spaces. Long r a d i a l branches run towards  and perpendicular  to the a r t i c u l a r surface and  in a brush-border l i k e complex of subchondral  terminate terminal  a r t e r i o l e s and c a p i l l a r i e s . The efferent end of this subchondral system coalesce with the venous sinusoids of the  27  Figure 4: Microarteriogram of the proximal rabbit femur. Note the large posterior branch of the medial circumflex artery aoproaching the nosterior trochanteric notch. The posteroi n f e r i o r nutirent vessel to the c a p i t a l er>inhysis ascends the postero-inferior aspect of the femoral neck.  Figure 5: Higher magnification of the posterior aspect of the rabbit femoral head and neck seen in Figure 4. The posteroinf e r i o r artery to the c a p i t a l epiphysis i s seen in more d e t a i l .  28.  (a)  (b)  Figure 6: Microarteriograms of the rabbit femur. Note the entrance of the diaphyseal nutrient artery into the proximal asre t h i r d of the femur and i t s ramifications within the shaft. The vessels surrounding the upper femur i n (b) are i l l u s t r a t e d in higher magnification i n Figures 4 and 5. Note the terminal radicles of the nutirent artery^ entering the femoral neck i n (a). The dark blue stained vessels i n (a) are c o l l e c t i n g venous sinuses.  cancellous spaces (Fig. 7) and share with them the large f r i a b l e venous sinuses of the epiphysis.  The  epiphyseal  veins retrace i n a transverse fashion the route taken by the afferent vessels and egress as one to three large veins at the postero-inferior os. A juxta epiphyseal system of vessels i d e n t i c a l with those in man,  pass through the canals of the epiphyseal bone plate  to supply the epiphyseal side of the growth c a r t i l a g e . On the metaphyseal side the process of endochondral o s s i f i c a t i o n i s c a r r i e d on by terminal radicles of the nutrient diaphyseal artery and more peripherally, the perforating metaphyseal arteries. The importance of the ligamentum teres vessels i n rabbits i s uncertain.  The results of s e l e c t i v e interference with  these vessels, which w i l l be presented  l a t e r , suggest they are  a s i g n i f i c a n t route of blood supply to the femoral head i n very young rabbits only. Maturity and closure of the growth plate allows free epiphyseo-metaphyseal vascular communication. (Figure 8). This i s most obvious on the efferent side where with age the venous sinus connections  may  reach enormous proportions.  The diaphysis i s supplied by one or more nutrient vessels originating from the equivalent of the l a t e r a l circumflex artery in man.  These nutrient a r t e r i e s enter the medial margin of the  shaft i n i t s upper one third and divide into superior and i n f e r i o r branches on reaching the marrow cavity.(Figure 6). Thereafter they behave as i n man  and other animals.  30.  Figure 7 High magnification Chinese ink microangiogram of the juxta a r t i c u l a r vascular system of the rabbit femoral head. Coalescence with the sinusoidal networks wdfh the subjacent cancellous spaces i s seen i n the lower part of the i l l u s t r a t  31.  (b) Figure 8: Chinese ink microangiogram of (a) immature and (b) adult rabbit femoral heads. The dye has advertantly crossed the c a p i l l a r y bed and so f i l l e d both the afferent and efferent microvasculature, therefore the larger intraosseous vessels are obscured. Note the e f f e c t i v e b a r r i e r to epiphyseo-metaphyseal anastomoses by the growth plate i n (a)  32The blood supply to the femoral head therefore compares well i n man and rabbit.  Both are dependant on an epiphyseal  system of vessels especially before skeletal maturity. These vessels d i f f e r p r i n c i p a l l y i n the intra-capsular course they take to enter the femoral head.  In both the growth c a r t i l a g e  offers a staunch b a r r i e r to epiphyseo-inetaphyseal vascular connections. With maturity this b a r r i e r disappears (Figure 8) In man the ligamentum teres vessels regress i n early childhood and return i n preadolescance to play a v a r i a b l e role i n supplying blood to the c a p i t a l epiphysis. Although t h e i r importance i n maintaining v i a b i l i t y of the human femoral head following injury i s uncertain, they are an important avenue of revascularization i n man as has been demonstrated 99 25 26 by SEVITT, and by CATTO .' In the rabbit also i t would seem (from evidence to be presented l a t e r ) the ligamentum teres vessels diminish i n importance i n late immaturity, and contribute less than 207= of the blood flow to the femoral 104 head i n adulthood . demonstrated  Their role i n revascularization has been  i n very young rabbits by LEMOINE ? 7  but not studied  in adult animals. FUNCTIONAL IMPORTANCE OF THE EIPIPHYSEAL VESSELS IN MAN Non-inflammatory or aseptic necrosis of the femoral head following fractures, of the femoral neck i s the most common, and indeed important example of the funcional importance of 3 85 these vessels i n man. AXHAUSEN and PHEMISTER separately described the true ischaemic nature of this complication, and i t i s generally believed that damage to the superior  27  retinacular vessels i s the p r i n c i p a l factor i n i t s genesis.  33. TRUETA  121  examined the uninjured femoral heads of  f i f t e e n cadavers with t e c h n i c a l l y acceptable microarteriographic r e s u l t s .  The l a t e r a l epiphyseal vessels supplied  approximately four f i f t h s of the epiphysis i n seven specimens, two thirds i n a further seven and a l i t t l e over h a l f i n one. 100 SEVTTT investigated the r e l a t i v e contribution of the various possible routes of blood supply to the femoral head in f i f t y seven cadavera, using microarteriography. Before i n j e c t i o n he s e l e c t i v e l y obliterated a l l but one avenue of blood supply i n each case.  He found that i n s i x specimens  with the superior retinaculum alone i n t a c t , a l l or nearly a l l of the head was injected. In eight cases with the i n f e r i o r retinaculum alone i n t a c t , only one showed f i l l i n g of more than one t h i r d of the femoral head.  It would seem therefore,  we have abundant cTJinical and experimental evidence to support the importance of the intracapsular or retinacular vessels. Interference with the extracapsular epiphyseal vessels diminishes i n effect the further away from the j o i n t this injury 59 i s caused.  JUDET and h i s coworkers  i n a microarteriographic  study using cadaver. , f a i l e d to prevent f i l l i n g of the retinacular vessels by l i g a t i o n of the medial and  lateral  circumflex a r t e r i e s at their o r i g i n alone. This i s not surprising Ihiview of the r i c h a r t e r i a l anastomoses between the medial circumflex, obturator and gluteal vessels demonstrated on gross 54 80 dissection by HOWE. MUSSBICHLER demonstrated s i g n i f i c a n t connections between the i n f e r i o r gluteal and posterior capsular a r t e r i e s i n f i v e of fourteen normal volunteers who underwent s e l e c t i v e internal i l i a c arteriography. In two of these the posterior capsular artery seemed to a r i s e s o l e l y  from the i n f e r i o r g l u t e a l .  Complete capsulectomy however  consistantly prevented retinacular f i l i n g i n JUDETS study 80 and i n nine cases followed by MTJSSBICHLER  59  who demonstrated  preoperative arrest of c i r c u l a t i o n i n the posterior capsular vessel following fracture of the femoral neck, seven developed avascular necrosis of the femoral head. FUNCTIONAL IMPORTANCE OF THE EPIPHYSEAL VESSELS IN RABBITS The importance of the epiphyseal  system of vessels i n  maintaining v i a b i l i t y of the femoral head i n animals i s now well established.  Interference with these vessels may be  achieved  by a number of methods including subcapital , , 10,47,64,92 osteotomy or experimental epiphyseal separation 64•75•92 by i n c i s i o n , stripping or l i g a t i o n of the femoral neck ' * 93 94:95 : ' ' , or by s e l e c t i v e vascular damage such as interference . _ - _ , 64,70,92;116;141 with the ligamentum teres vessels , or the nutrient vessel to the epiphysis, that i s the posterot  1  i n f e r i o r artery. Generally speaking, damage to the retinacular vessels, with or without ligamentum teres i n j u r y , i s followed by epiphyseal bone death i n young animals.  The growth plate renders the  blood supply to the epiphysis more precarious and e f f e c t i v e l y hinders revascularization from the femoral neck In adult animals the intraosseous  '  '  epiphyseo-metaphyseal  anastomoses may o f f e r an alternate route of blood supply and 93 drainage  but this has been i n s u f f i c i e n t l y studied.  Selective interference with the ligamentum teres vessels has  met with variable r e s u l t s .  In rabbits the changes  35.  induced were inversely proportional to the age of the animal^'^ adults.  and epiphyseal bone death was  STEWART * 1  not found i n  f a i l e d to produce s i g n i f i c a n t  6  and  consistant avascular necrosis i n six-week old rabbits and 141 ZEMANSKY and LIPMANN  produced necrosis by ligamentura  teres l i g a t i o n i n rabbits less than seven weeks old only. The data dealing reported changes following ligamentum teres damage i s however d i f f i c u l t to interpret as a s a t i s f a c t o r y l i g a t i o n or d i v i s i o n must involve an arthrotomy and at least transient subluxation or luxation.  The  earlier  reports do not indicate that "sham" proceedures were c a r r i e d out on the control side.  The bone death may  therefore have  resulted from the capsulotomy, transient subluxation luxation, or the ligamentum teres damage per se. 104 SHIM  or  quantitated the contribution of the ligamentum  teres vessels to epiphyseal blood flow as 177= i n adult rabbits. 70 LEMOINE  s e l e c t i v e l y divided the postero«inferior artery  to the c a p i t a l epiphysis, within the joint capsule.  Each one  of sixteen young rabbits developed some changes detectable on radiographic, h i s t o l o g i c a l or macroscopic examination. Microarteriography  revealed an avascular femoral head during  the first,week revascularization through the ligamentum teres and metaphyseal a r t e r i e s during the second week, hyperv a s c u l a r i t y during the t h i r d and gradual return to normal thereafter. It i s interesting to note that interference with the stem vessels outside the joint capsule was l a r g e l y 70 j92 without e f f e c t on epiphyseal v i a b i l i t y . This i s iinn 59. keeping with the work of JUDET and h i s associates i n man.  Interference with the epiphyseal blood supply  may  be induced also by experimental microembolization using 134 carbon or sodium morrhuatc p a r t i c l e s . The lesions are not s p e c i f i c for the epiphysis however and have been produced 112 i n the diaphysis and metaphysis with equal ease using carbon 63 and septic emboli .  This i s s i m i l a r to the non-specific  lesions following suggested micro-embolization  in  man,  as seen i n Caissons disease. Epiphyseal  ischaemia may  be produced i n dogs and  pigs  by prolonged forced hip j o i n t splintage i n an unphysiological 24 97 112 133 position. It has been suggested that prolonged increase i n the i n t r a a r t i c u l a r pressure i s the mechanism 137 97 responsible .  SALTER  has however interpreted the changes  as due to i n t r a epiphyseal  interference with perfusion,  induced by d i s t o r t i o n of the soft and maleable cartilagenous femoral head i n young animals .  The same e f f e c t may however  be produced by d i r e c t l y increasing the i n t r a a r t i c u l a r v i a an indwelling catheter. epiphyseal perfusion may 50 mmHg suggest a  i n the youn pig^  pressure  S i g n i f i c a n t interference with  be incurred by pressures and  75mraHg i n puppies^?  as low as This would  tamponade effect on the retinacular vessels, perhaps  leading to venous gangrene of the femoral head.  37.  PHYSIOLOGY  GENERA, FEATURES 35 DRINKER, DRINKER and LUND  pioneered the t r u l y objective  study of bone blood c i r c u l a t i o n with their perfusion studies in dogs and other animals.  The principles underlying such  investigation and the sum of knowledge so f a r gained were comprehensibly  reviewed by SHIM?  He c l a s s i f i e d the  5  possible methods of investigation as follows: I  QUANTITATIVE STUDIES. A. Direct Methods. 1. Cannulation - c o l l e c t i o n measurement 2. Application of electromechanical flow meters B. Indirect Methods. 1. Blood tissue exchange mechanism a. Fick p r i n i c p l e b. Radioisotope clearance 2. Indicator-dilution p r i n c i p l e . r, , .,131. 5 1  a. Radioisotope (Cr b. Dye  , I  )  (Evans blue)  3. venous^ occlusion Plethysmography II  Qualitative Studies A. Flow Pattern 1. V i t a l  microscopy  2. Bone venography  i  38.  Selective a r t e r i a l i s o l a t i o n to determine r e l a t i v e importance of a r t e r i e s . 1. Destruction  or occlusion of certain vessels  a. Study of devitalized area b. Effect on fracture healing or bone growth. c. Effect on r e l a t i v e isotope uptake 2. Injection of indicators into an artery to observe the area i t sustains. Bone hemodynamics 1. Direct methods (cannulatinn) a. Assessment of r e l a t i v e flow volume change b. Study of arteriovenous blood  constituents.  2. Indirect Methods. a. Intramedullary blood pressure b. Intra osseous thermometry c. Oxygen tension of bone d. Radiosotope uptake or clearance from bone . A l t e r a t i o n of hemodynamics to stimulate  growth,  fracture repair and bone v i t a l i t y . 1. Sympathectomy 2. Arteriovenous f i s t u l a 3. Periosteal stripping 4.  Fracture  5. Ligation of a major vein 6. Application of low pressure tournequets 7. Artery or muscle transplantation  to bone.  TO  COPP and SHIM^ described an i n d i r e c t method of assessing bone blood flow using the clearance by bone of a c i r c u l a t i n g bone-seeking  radioisotope.  SHIM applied this  method extensively to the quantitation of bone blood flow and i t s c o n t r o l l i n g factors i n a n i m a l s ^ ' , and PATTERSON '^ 07  08  and with COPP  described the rate of blood flow i n canine  and rabbit bones as approximately 10 ml/min/lOOgms fresh 85 weight.  Corrected f o r the extraction r a t i o of Sr  , and  the r e l a t i v e percentage of t o t a l body weight contributed by the endoskeleton they estimated that t o t a l skeletal flow accounted f o r 7% of the resting cardiac output In these animals. SHIM and h i s associates applied the same technique to the lower limb of a 24 year old male about to undergo a high 109 thigh amputation  f o r l o c a l i z e d malignant bone disease.  Bone blood flow was  estimated at 2.5 ml/min/100gms wet bone  in this patient an4 t o t a l skeletal flow at 6.37c of the resting cardiac output.  This compared well with skeletal blood flow i n  dogs and rabbits. DRINKER et a l also suggested that blood c i r c u l a t i o n i n bone was controlled by hormonal, metabolic and neuronal 34 *35 factors. ' today?  5  There i s ample evidence to support this hypothesis  It has been demonstrated that stimulation of the  s c i a t i c nerve i n adult rabbits reduces bone blood flow i n the hind limb.  This was measured d i r e c t l y using the nutrient  vessel cannulation technique* -and by monitoring i n t r a 52 medullary pressure. Furthermore section of 139 the s c i a t i c nerve This increase was maximal i n the foot bones. YU demonstrated 106 increased the rate of bone blood flow by 5 to 457« with 14 days. 10  40  that experimental haemorrhagic shock caused a f a l l i n bone blood flowj and i t s relationship with systemic blood pressure suggested a vasomotor tone increase i n intraosseous peripheral vascular system.  Dibenzylihe abolished this  vasoconstriction suggesting that the vasomotor effects of  shock on bone blood flow were largely mediated  through  an alpha receptor system. The effects of norepinephrine, epinephrine, actylcholine, 103x104 and p i t r e s s i n have been quantitated i n experimental animals. Microgram doses of epinephrine reduced the rate of bone 52 51 139 blood flow by 25 to 75%. HAWK and SHIM, HAWK, and YU have perfected the use of intramedullary pressure monitoring as a tool i n studying d i r e c t l y the quantitative and q u a l i t a t i v e aspects of blood flow.  Their work further confirmed  hormonal effects of blood flow.  the  Adrenaline and noradrenaline  caused a profound f a l l i n intramedullary pressure associated with a decrease i n bone blood flow.  The s i t e of action whether  extra- or intraosseous was not c l e a r , but the pressure effects in bone were independant of the systemic effects of the hormones. There i s evidence to suggest that metabolic factors are the 110 most important o v e r a l l c o n t r o l l i n g mechanisms.  Systemic  hypoxia induced by rebreathing has been demonstrated to increase bone blood flow i n the rabbit and l o c a l increase i n p'CO^  , acid metabolites and reduced pH exerted a similar e f f e c t ,  t y p i f i e d by the prolonged hyperaemia following temporary femoral artery occlusion.  More important, this hyperaemia was not  abolished by nerve stimulation or vasopressor hormones.  41.  Obviously therefore metabolic factors may ovar ride other c o n t r o l l i n g niechaniems. THE FEMORAL HEAD: The physiology  of blood c i r c u l a t i o n within the ends  of long bones i s not well understood.  The many channels  taken by the epiphyseo-metaphyseal vessels, and the further v a r i a t i o n which must be incurred by s k e l e t a l maturity and o b l i t e r a t i o n of the growth plate personifies the d i f f i c u l t i e s which bone as an organ i n general presents to the investigator. MATUMOTO and MIZUN^ using the clearance 3  rate of a  radiopaque dye d i r e c t l y injected into bone, estimated the rate of blood flow i n the femoral head of a normal adult man to vary 3 to 7 ml/min/cu. cm. of bone SHIM and his a s s o c i a t e s ^ 85 c i r c u l a t i n g Sr discovered  7  using the bone clearance of  a s i g n i f i c a n t difference i n the  regional flow rates i n the femur of 50 adult rabbits.  Bone  blood flow within the femoral head was 18.5 ml/min/100 gms. fresh weight.  This contrasted with 7.5 ml/min/100 gms. fresh  weight i n the shaft.  Using a s i m i l a r technique the same workers  investigated the regional cotribution of the nutrient artery to 108 the femur i n adult rabbits.  Obliteration of the diaphyseal  nutrient artery caused a reduction of 3 7%  i n the flow rate  within the upper femoral epiphysis and metaphysis.  It was  concluded that under normal conditions the epiphyseo-metaphyseal vessels are responsible for 637„ of the bone blood flow within this  region.  42.  MILES  measured the intramedullary pressure i n the  femoral head of over 30 patients following i n t r a and extracapsular fractures, following reduction of traumatic d i s l o c a t i o n and i n some normals.  The pressure varied and  sometimes rose to 50 ml. saline.  He stressed the normal  f l u c t u a t i o n with a r t e r i a l pulse pressure and rate, and suggested  that loss of this conducted  pulse wave following  trauma was i n d i c a t i v e of an ischaemic femoral head. 114 STEIN  and h i s co-workers demonstrated a s i g n i f i c a n t  difference between the mean diaphyseal and epiphyseal i n t r a medullary pressures i n dogs (50:12 min Hg). There was a s i m i l a r but greater discrepancy i n pulse pressure (8.1 min Hg). 19 The significance of these observations i s not clear. has suggested  BROOKS  that the c i r c u l u s vasculosus serves a purpose  in lowering the blood pressure within the epiphyseal a r t e r i e s before they enter the bone. metaphyseo-epiphyseal,  He fuuthermore interpreted the  and epiphyseo-joint space pressure  differences as an indication of u n i d i r e c t i o n a l flow of nutrients from metaphysis to epiphysis and epiphysis to j o i n t space.  This, i f correct, would support h i s  contention that growth-plate v i a b i l i t y i s dependant on the metaphysis,  and a r t i c u l a r c a r t i l a g e v i a b i l t y dependant  on the epiphysis, both somewhat controversial and unorthodox views.  43.  REVIEW OF THE LITERATURE  TRAUMATIC DISLOCATION OF THE HIP  CLINICAL: Classification Adults Children  Avascular Necrosis  EXPERIMENTAL  ' 44.  TRAUMATIC DISLOCATION OF THE The  serious  implications  weight-bearing j o i n t in man editorial?  "Of  HIP of this injury to the p r i n c i p a l  were well emphasized in a recent  the known causes of u n i l a t e r a l o s t e o a r t h r i t i s  Of the hip, traumatic dislocation of the hip j o i n t , by involving c h a r a c t e r i s t i c a l l y the young working male, can repsonsible for not only great pain and economic loss as well".  The  be  d i s a b i l i t y , but grave  overall incidence i s unknown,  but would obviously depend on the l i f e s t y l e of the population under consideration,  as i t i s c h a r a c t e r i s t i c a l l y associated  with high impact injury.  BRAv^  described the incidence  as 57o of a l l j o i n t i n j u r i e s , but did not c l a r i f y his source. Although the incidence of hip dislocation has with the speed and complexity of transport,  s t e a d i l y risen  i t remains an  uncommon injury, e s p e c i a l l y i n childhood, and  statisically  s i g n i f i c a n t appraisal of the o v e r a l l outcome and contributory and  factors has had  long-term study.  documented and  i t s salient  to await co-operative, combined  A number of such reports have now  been  these w i l l be reviewed.  CLASSIFICATION: The  femoral head may  displace over the l i p of  the  acetabulum or through i t s f l o o r , into the pelvis.  The l a t t e r  i s described as a central fracture dislocation and  considered  as a separate, or predominantly acetabular inury, by most authors.  One  series of 193 dislocations included  an  117  incidence of 147 central fracture dislocations. 0  This review  w i l l not deal with the outcome of central displacement.  45,  The dislocated hip i s generally c l a s s i f i e d by type and group.  The type may indicate the route taken by the luxating  33 femoral head, or more commonly describe  the position of the  displaced head at the time of diagnosis, and so posterior, anterior, obtarator and  perineal.  Anterior dislocation  accounts for 10 to 127, of such i n j u r i e s ^ obturator  and  perineal types are rare.  while the  The grouping i s based  on the presence and degree of bone damage around the hip, and the number of groups used varies from author to author. 16  BRAv, reporting on 523 dislocations, used three groups: Group 1: simple d i s l o c a t i o n Group 11: d i s l o c a t i o n with associated fracture of the acetabular rim. Group 111: Dislocation with associated fracture through the acetabulum or femoral head.  ADULT: Over one thousand cases have been reported by seven authors . ...  *  16,57,67,77,81,117,118  -I  within the l a s t twenty years,  , and more  than h a l f of these were suitable for close analysis and follow up.  Furthermore MORTON reviewed 825 cases from the l i t e r a t u r e 7  with p a r t i c u l a r stress on the The  complications.  injury i s most common during  decade and in the population  the third and fourth  at large males are affected three ,  117,118  times more commonly than females .  „ ,  Although varying  from series  s e r i e s , the l e f t and right hips are equally affected o v e r a l l . C h a r a c t e r i s t i c a l l y the d i s l o c a t i o n i s suffered in a motor vehicle accident  ) and associated with bone 117,118  damage to the femoral head or acetabulum (707o  ).  .  46. 1 THOMPSON and EPSTEIN suitable f o r follow-up.  reported 204 cases.  116 were  On c l i n i c a l and r a d i o l o g i c a l  evidence, the outcome was c l o s e l y related to the severity of the injury as judged by the degree of bone damage. (Table 1). Of 78 patients with a f a i r or poor r e s u l t , only 10 had suffered a simple dislocation.  An i n s u f f i c i e n t number underwent  delayed reduction to draw any conclusions related to the duration of dislocation. The adult age and length of time before unprotected weight bearing did not influence  the results.  STEWART and MILFORf) reported 193 cases, 123 of which 17  were available f o r follow-up.  The c l i n i c o - r a d i o l o g i c a l  outcome was again c l o s e l y related to the severity of injury (Table 1). None of t h e i r cases reduced a f t e r 24 hours had a  s a t i s f a c t o r y r e s u l t , but a l l of these patients had associated  bone damage.  The age did not a f f e c t the outcome.  MORTON reported 62 cases. In 48 followed up, the 7  influence  of bone damage was similar to e a r l i e r  Excellent  results were gained only i n those reduced i n less than  twelve hours.  reports.  The duration on non-weight bearing did not seem  to a f f e c t the outcome. BRAV  reported 523 dislocations.  was possible  i n 264.  c l o s e l y correlated.  Satisfactory  analysis  The severity of injury and outcome again Delay i n reduction past 12 hours was  associated with more than a two-fold increase i n unsatisfactory end  results. He reported an 66 anterior dislocations, 157» of  which were ultimately  unsatisfactory.  47. COMPLICATIONS IN ADULTS'. Recurrent d i s l o c a t i o n : Myositis o s s i f i c a n s : S c i a t i c nerve palsy:  TRAUMATIC ARTHRITIS: unsatisfactory  12 to 167«, most common and severe following associated bone damage.  This i s the most common cause of functional  recovery.  As e a r l i e r reviewed,  i t i s c l o s e l y related to the severity of injury and the duration of dislocation, Avascular necrosis of the femoral head i s a common accompaniment and i t i s frequently d i f f i c u l t to d i f f e r e n t i a t e the two. This may account f o r the exceptionally  low incidence of avascular necrosis  following  traumatic h i p dislocation recently reported 57 67 by HUNTER and LAMPKE at 27o and 7% respectively.  AVASCULAR NECROSIS: For l a t e r  discussion.  CHILDREN: Traumatic dislocation i s d i s t i n c t l y less common i n childhood. and  84).  The male preponderence i s again 3:1 (combined 78 Anterior  dislocation occurrs i n 7 to 167, of casest^'^  while central dislocation i s uncommon or unreported. recorded complications are associated fractures,  The  epiphyseal  separation, premature closure of the growth plate, recurrent d i s l o c a t i o n , coxa magna, traumatic a r t h r i t i s and avascular necrosis.  Permanent s c i a t i c palsy has not been reported.  48.  The f i r s t large-scale review was documented by MORTON. He reported 136 cases following extensive review of the l i t e r a t u r e , and addition of 7 new cases.  The mechanism and  severity of the injury, and duration of dislocation had been poorly recorded i n the l i t e r a t u r e and conclusions were consequently d i f f i c u l t  to make.  '  GLASS and POWELL^ reported on 108 cases following s i m i l a r l i t e r a t u r e review and addition of 47 new cases. Only 257. of their cases had been associated with a possible high impact injury. injury  They stressed the t r i v i a l nature of the  frequently seen i n childhood.  They could find no  corelation between the severity of injury, and the type  ^  and incidence of complications. 40 FUNK  reported 40 new cases, and was the f i r s t to subgroup  this injury and i t s outcome on the basis of age.  He stressed  the close relationship between age above 5 years, and the severity of injury.  He concluded that this relationship was  based on the ease with which the hip may be dislocated i n very young children.  Duration of displacement considerably  influenced the ultimate r a d i o l o g i c a l outcome, but age had a similar influence even i f the dislocation was reduced with 24 hours. 84 The PENSYLVANIA ORTHOPAEDIC SOCIETY  presented the most  comprehensive and recent report availabe, with 165 patients, including 51 personal cases.  They found a clear connection  between severity of injury and ultimate c l i n i c o - r a d i o l o g i c a l outcome. Severe injury as judged by the mechanism or circumstances of the accident and x-ray findings, was associated  49.  with a 3 fold increase i n c l i n i c o - r a d i o l o g i c a l d i s s a t i s f a c t i o n ; In t h e i r personal series 187, had accompanying bone damage around the hip.  Seven of these cases were followed to  maturity and 6 of them classed as unsatisfactory r e s u l t s .  40 As i n FUNK's series limit.  f i v e years seemed the c r i t i c a l  age  907, of these cases reduced within 24 hours gained  excellent or good r e s u l t . delayed reduction;  an  This f e l l to 447, following  The authors stressed however that severe  i n j o r y commonly influenced the duration of d i s l o c a t i o n by hindering diagnosis, or of necessity delaying prompt treatment of the d i s l o c a t i o n . The period of non-weight bearing did not c l e a r l y influena the outcome.  AVASCULAR NECROSIS OF THE FEMORAL HEAD FOLLOWING TRAUMATIC DISLOCATION OF THE  HIP  It i s generally believed that death i n whole or part of the femoral head following traumatic in man,  d i s l o c a t i o n of the hip  i s incurred by interference with the blood  supply.  i t was  f i r s t s and almost simultaneously described as a 8 36 complication of d i s l o c a t i o n by BERGMANN, DYES, and 116 STEWART  on the basis of i t s c l i n i c a l and  radiological  s i m i l a r i t y to avascular necrosis following intracapsular 85 fracture of the femoral neck documented e a r l i e r by PEMISTER 3 and AXHAUSEN . 69 LAUFER  reported the macroscopic and h i s t o l o g i c a l picture  in a case of late segmental collapse of the femoral head following traumatic  posterior d i s l o c a t i o n . The  features  described and i l l u s t r a t e d are indistinguishable from those constantly found i n vascular necrosis following femoral neck  25526>85,86j87;98,99,101 fracture.  . _ . , Indeed they are s i m i l a r l y t  comparable with the h i s t o l o g i c a l features of bone, necrosis within the t i b i a commonly associated with occlusive 102 peripheral vascular disease. The location and type of vessel damage or occlusion i s not certain and i t may understandably vary. Our knowledge . , . , _• i , 120>125 of the p a r t i c u l a r vascular anatomy of the femoral head and the functional importance of the epiphyseal vessels, as presented e a r l i e r ; would support extraosseous blood vessel damage as a reasonable supposition. The work of JUDET on 59 70 92 cadavers and LEMOINE and ROKANNEN on rabbits indicates that such vessel injury close to the femoral head obviates c o l l a t e r a l anastomatic compensation and causes  significant  embarassment of blood supply to the femoral head. Venous tamponade would seem u n l i k e l y as the capsular damage caused by d i s l o c a t i o n would be expected to decompress i n t r a - a r t i c u l a r pressure.  Intraosseous and extraosseous  vascular occlusion i s a further possible cause or contributory factor.  The features of avascular necrosis following  trauma are not d i s t i n c t from those associated with Caissons Ai • u , 62>135 disease, i n man, or microembolization i n animals. 69 6  LAUFER  0  described a case of delayed segmental collapse  of the femoral head i n a 13 year-old boy following blunt traama to the hip without fracture or dislocation.  This case could  be c i t e d to support a theory forwarded by STEWART and MILFOR^  17  that avascular necrosis following traumatic d i s l o c a t i o n may result from i n t r a c e l l u l a r damage incidental to the force and counterforce imposed at the time of injury, I t could, of course,  be more e a s i l y explained by assuming the tamponade effect of post-traumatic effusion which would i n t e r f e r e with the superior retinacular route of blood supply and drainage upon which the c a p i t a l epiphysis i s almost  totally  dependant i n pre-adolescance.  INCIDENCE AND ADULTS:  CONTRIBUTORY FACTORS: 77  MORTON  reviewed 645 cases from the l i t e r a t u r e and  found an incidence of 147.. In 48 new cases he estimated that avascular necrosis was c e r t a i n i n 177o and probable in 307 . o  The overall incidence i s otherwise reported at 2 and 2 6 ^ .  Close analysis of the c l i n i c a l material repeatedly  stresses two salient contributory factors: 1. Duration of dislocation. A l l authors have implicated delay i n reduction as a factor contributing to the .16 incidence of avascular necrosis.  In p a r t i c u l a r BRAV s  figures suggest that delay beyond 12 hours i s associated with more than a three-fold increase i n the l i k l i h o o d of bone death within the femoral head, regardless of the severity of the i n i t i a l  injury.  2. Severity of injury. Avascular necrosis following simple d i s l o c a t i o n alone i n adults f a l l s to 107o** 11%}^ and 8  ( i f reduced with 12 hours). Assoicated bone damage increased the overall incidence to 357o and i f severe, such as fracture through the femoral head or acetabulum, 1 6  to 70% i n BRAV's series.  Age and duration before unprotected weight bearing does not apparently influence the Incidence of avascular necrosis, although  early weight bearing may a f f e c t the degree  of associated bone c o l l a p s e d Repeated attempts at closed reduction or open reduction does o f f e r a poorer  prognosis,  but obviously b y a mulTtifactorials influence. ' ^  Lu'tl-  -  BRAV^ reported 66 cases of anterior dislocation of which avascular necrosis was 97» .  CHILDREN: Ischaemic necrosis of the femoral head occurs i n 44:78 84 10%, of children a f t e r traumatic hip dislocation  ' *  As i n adults the incidence i s considerably influenced by the duration of displacement injury.  and severity of the i n i t i a l  The PENNSYLVANIA ORTHOPAEDIC SOCIETY c l o s e l y 84  analysed 20 cases of resulting avascular necrosis. 18 - had reduction delayed beyond 24 hours 14 - had suffered severe h i p truama 1 - had a recurrent d i s l o c a t i o n 78 MORTON  found 12 cases reported i n the l i t e r a t u r e . The  duration of d i s l o c a t i o n was reported i n 5 only, and 4 of these were reduced l a t e r 7 days from the time of injury. He furthermore  found 7 cases with assoicated bone damage. 88  Three of these developed avascular necrosis. PIGOTT  reported  9 cases of traumatic .dislocation i n which one, a nine year old  g i r l , developed Ischaemic necrosis. She had f a l l e n from  a height of f o r t y feet.  53.  Avascular necrosis i s rare as a complication i n 1  children less than f i v e years of age, but  so too. i s severe  injury as the cause of d i s l o c a t i o n i n this age group.  Overall therefore, avascular necrosis of the head may  femoral  be expected to follow i n up to 307,, of adults, and  i 0 % of Children a f t e r a traumatic nip d i s l o c a t i o n .  The  mechanism and Severity of the injury, and duration before reduction considerably influence the outcome i n this regard. It i s well to remember however that severe injury i s a common cause and accompaniment of delayed treatment.  The influence  of s k e l e t a l maturity i s obviously personified by the greater liklehood of severe injury and associated fractures about the hip in adults. Considering simple dislocation alone i n adults the incidence of ischaemic that seen i n children.  femoral head necrosis approaches  This i 8 s u r p r i s i n g , as the more  precarious blood supply to the c a p i t a l epiphysis before 120 skeletal maturity in c h i l d r e n .  would lead one to expect a higher incidence  The influence of age in childhood i s probably  a result of the ease with which the hip may be dislocated , , ,.40 below f i v e years of age. It i s c l e a r therefore that the factors of age i f a c h i l d , skeletal maturity, severity of injury and duration of dislocation are largely inseparable and cannot be i n d i v i d u a l l y assessed on the basis of our c l i n i c a l information alone.  54.  EXPERIMENTAL DISLOCATION OF THE HIP IN ANIMALS:  As presented e a r l i e r , the functional importance of the epiphyseal vessels i n maintaing v i a b i l i t y of the femoral head i n animals i s now well proven. Avascular necrosis may be consistently produced by gross i n t r a - or extraosseous damage to this system, or s e l e c t i v e Interference with the nutrient vessels to the epiphysis.  The growth plate may increase  the r i s k and extent of ischaemic bone damage i n growing animals and c e r t a i n l y hinders revascularization a f t e r the fact of epiphyseal death has occurred. In contrast the series of events following d i s l o c a t i o n has received scant attention.  No doubt many of th e a r l i e r  reports dealing with s e l e c t i v e damage to the ligamentum teres vessels Infers at least transient subluxation or luxation. 70 LEMOINE  ligated the ligamentum teres i n 5 immature  and 2 mature rabbits. Four of the growing rabbits developed r a d i o l o g i c a l features of avascular necrosis associated i n 3 with hypervascularity detected by microarteriography. author stressed however that each case underwent  The  postero-  l a t e r a l arthrotomy and d i s l o c a t i o n of the h i p during the proceedure.  He made no conclusions.  ROKANNEN*^ also recognized  this problem and investigated  the effects of ligamentum teres l i g a t i o n and transient dislocation i n 2 2 rabbits (age not stated). He found h i s t o l o g i c a l evidence of limited avascular necrosis i n 4 animals.  MULLER  studied the effects of traumatic luxation of  the hip i n animals of various ages and was the f i r s t to describe the h i s t o l o g i c a l features following this injury.  He described  fibrous replacement of the marrow and scattered bone necrosis within the femoral head i n adult animals, . BERGMANN  produced closed d i s l o c a t i o n i n 2 adolescant  rabbits and noted limited subchondral bone necrosis i n one animal s a c r i f i c e d at 8 weeks. BOH& conducted a radiographicj H i s t o l o g i c a l and 1  microarteriographic  study of the femoral head following  manual posterior d i s l o c a t i o n of the hip i n 20 newborn rabbits* while investigating the dysplastic features of congenital d i s l o c a t i o n of the hip. extreme.  Ischaemic necrosis,was constant and  The c a p i t a l epiphysis was rendered almost t o t a l l y  avascular and revascularization occurred  from the trochanteric  epiphysis and through the growth plate during the second week of displacement. pattern returned reported  The h i s t o l o g i c a l picture and vascular to normal during the fourth week.  He l a t e r  the same series of events using t e t r a c y c l i n e 12  fluorescance as a measure of blood supply to the femoral head. SMITH  11  investigated the gross alterations following  operative luxation of the hip i n pups. Considerable coxa vara was  produced, but no histology undertaken.  was  not carried out on the control side  Sham arthrotomy  ROKANNEN induced sustained d i s l o c a t i o n i n 22 i-abbits 2  (age not stated) following arthrotomy  The animals were  s a c r i f i c e d at varying intervals up to nine months following Injury.  Segmental necrosis of the femoral head was noted i n  h a l f the cases, and occurred  as a l a t e feature  only.  56.  Overall therefore the reported consequences  of open  of closed dislocation of the hip i n animals varies with the investigator, and method of study and the age of the animal. A controlled study of the time sequenced  events following  d i s l o c a t i o n has not been undertaken; nor an attempt to assess the influence of skeletal maturity, duration of displacement and reduction.  57.  MATERIALS AND METHODS  The EXPERIMENTAL MODEL: The comparative anatomy of the blood supply of the femoral head in man and the rabbit has been reviewed. The hip j o i n t of the rabbit i s a suitable model for studying the events following traumatic  dislocation.  ANIMALS: A t o t a l of 220 New Zealand white (female) rabbits, 65 mature (averaging 3.98 Kgm)  and 155 immature (averaging 2.22 Kgm)  were used.  ANAESTHESIA: Intravenous nembutal 30mg. per kilogramMaintenance doses were not required.  DISLOCATION: The l e f t hip was manually dislocated i n a l l cases by d o r s a l l y applied force along the l i n e of the femur with the hip held adducted, i n t e r n a l l y rotated and i n s l i g h t extension. was  The route and ultimate position of displacement  poster-superior.  Successful d i s l o c a t i o n declared i t s e l f by  an audible and palpable c l i c k , postero-superior s h i f t of the greater trochanter, and leg - length  discrepancy.  REDUCTION: I f planned, manual reduction was undertaken at the same, or a different s i t t i n g  (under anaesthesia). Reduction was  achieved by ventral traction along the l i n e of the femur with the hip held i n the same position as for dislocation.  The pelvis was s t a b i l i z e d with the l e f t hand and the femoral head guided into the acetabulum with the l e f t index finger. Palpable excursion of the femoral head into the acetabulum, and disappearance of the leg length discrepancy s i g n i f i e d reduction. Fluoroscopic examination waa •'carried out within 10 minutes i n a l l cases. The aminal was discarded from the study ii a second attempt at reduction was needed.  A l l animals were returned to their cages following anaesthesia and allowed unrestricted a c t i v i t y and standard diet f o r the length of their s u r v i v a l .  CONTROL: The right hip was untouched  i n a l l cases and used  as a control.  INVESTIGATION:  The changes within the femoral head following  d i s l o c a t i o n , and reduction were assessed by three methods. A.  Microangiography  B. Histology C.  A.  Radiography.  MICROANGIOGRAPHY Under nembutal anaesthesia, and following a mid-line  abdominal i n c i s i o n , the abdominal aorta and i n f e r i o r vena cava  (I.V.C.) were exposed.  The aorta was ligated just d i s t a l  to the renal vessels a f t e r i n j e c t i o n of Heparin  (1000 U per  kilogram) and cannulated with a f8 polyethylene catheter. The  I.V.C. was allowed to bleed f r e e l y into the peritoneal cavity a f t e r proximal l i g a t i o n  (Figure 9).  Two solutions were infused sequentially at constant temperature  (42 degrees C) and pressure (80 mm Hg).  1. Physiological saline (+ Heparin lOOOU/litre) u n t i l the return through the I.V.C. was l a r g e l y c l e a r of blood. 2. Tracer Dye: 250 ml 207= Mannitol 250 ml commercial Chinese ink 500 ml water with 40 gms Gelatin. The dye infusion was continued u n t i l the surrounding skin, serosa and organs indicated a s a t i s f a c t o r y perfusion, This averaged s i x minutes.  (Figure 10).  The animal was s a c r i f i c e d with an overdose of numbutal, into the proximal I.V.C. during the saline infusion. The hind limbs were moved through a physiological range of movement during infusion. The vessels were decannulated and tied.  The animal was  stored overnight i n a fridge to form a g e l of the Chinese inkg e l a t i n dye, and the following day the hind limbs were c a r e f u l l y removed a f t e r proximal vessel l i g a t i o n . The macroscopic features i n terms of the j o i n t position, bone damage and deformity, and gross perfusion quantity and i t s extent were rioted at this time  (Figure 11). The proximal h a l f of each  femur with attached soft tissues was stored i n 107= formalin.  60.  (b) Figure 9: The ganeral set up of the infusion. Under nembutal anaesthesia two solutions (1. Saline & 2. The tracer dye) were sequentially infused into the abdominal aorta proximal to i t s bifucation under standard conditions of temperature and pressure.  61,  Figure 10: The bladder (a) before and infusion with dye.  (b) after  satisfactory  62.  Figure 11. Posterior aspect of the proximal femora a f t e r dislocation of the l e f t hip (to the l e f t of the i l l u s t r a t i o n ) and infusion. Note the frayed ligamentum teres, and absence of dye perfusion in the soft tissues of the postero-inferior femoral neck and c a p i t a l epiphysis on the l e f t side.  Figure 12: The f i n a l preparation before steromicroscopic analysis from one immature rabbit a f t e r dislocation of the l e f t hip and infusion. The l e f t c a p i t a l epiphysis i s Almost devoid of dye perfusion (to the right of the illustration).  63.  (b) Figure 13: Closeup of the mid-sections of the (a) right and (b) l e f t femoral heads presented in Figure 12 There i s a profound perfusion d e f i c i t within the dislocated l e f t c a p i t a l epiphysis. The l e f t metaphysis has perfused well, but the growth plate offers an e f f e c t i v e b a r r i e r to perfusion of the epiphysis from this source.  §4: This caused an i r r e v e r i s b l e gel of: the dye, and fixed the tissues."  Seven days l a t e r the soft  tissues were c a r e f u l l y  removed and the proximal 1/3 of each femur d e c a l c i f i e d i n * R.D.O. for four days, with constant agitation and at room temperature.  The bone segments were then divided  i n the  f r o n t a l plane into 1 to 2 mm. sections, bleached in Hydrogen Peroxide, dehydrated i n 70 to 1007c alcohol and cleared by the 113  SpalteBolz technique. The  f i n a l sections were each analysed by steromicroscopy  always i n r e l a t i o n to the control side.  At that time a  composite map could be made of the location, extent, and quantity of dye perfusion,  and i t s source. This f i n a l stage  undertaken on average, 4 weeks a f t e r sacrifice{Figures  was  12 & 13).  EXPERIMENT I 10  rabbits, 5 mature, 5 immature.  Aim:  (Table II)  to establish i f infusion proximal to the a o r t i c  b i f u r c a t i o n before dislocation would result i n q u a n t i t a t i v l y and  q u a l i t a t i v l y eomparable perfusion  and  l e f t femoral heads.  of dye i n the right  EXPERIMENT I I : 95  immature rabbits  (Table III)  Aims:l)to establish what changes would be apparent at 10 minutes a f t e r dislocation,.  *MAYNARD DIAGNOSTIC, Ontario.  Constituents not  revealed.  65; 2. to establish what changes would be apparent at 10 minutes a f t e r immediate reduction. 3.  to study the sequential changes i n dye perfusion of the  femoral head at 1, 2, 3, 5 and 7 days a f t e r dislocation, 4. to evaluate how the changes following  d i s l o c a t i o n could  be altered by immediate reduction, reduction at 24, and at 48 hours, as evidenced by the microangiographic  picture  at 1,3,5, and 7 days a f t e r reduction.  EXPERIMENT I I I : 20 mature rabbits  (Table IV)  Aims: 1. to establish what changes could be observed 10 minutes a f t e r d i s l o c a t i o n of the mature femoral head. 2. to establish what changes would be apparent at 7 days a f t e r dislocation. 3. to evaluate how the changes 7 days following  dislocation  could be altered by immediate reduction, and reduction at 24 hours.  EXPERIMENT IV: 10 rabbits, 5 mature, 5 immature (Table V) Aim:  to extablish  i f reduction at 12 hours offered any  improvement over reduction delayed to 24 or 48 hours, i n terms of the microangiographic picture 7 days a f t e r reduction.  The early changes following  unreduced d i s l o c a t i o n , and  immediate reduction were studied by manipulation of the hip a f t e r mid-line abdominal i n c i s i o n and atraumatic exposure of the aorta and i n f e r i o r vena cava was carried out.  66, Thereafter, heparitiizatidn, cannulation and infusion could be achieved with an average delay of 10 minutes.  B. HISTOLOGY: Each animal was s a c r i f i c e d by intracardiac i n j e c t i o n of 10% KC1.  The hind-limbs were c a r e f u l l y detached, note being  made of the macroscopic features (Figure 44).After i n v i t r o x-ray, the proximal \ of each femur was removed and bissected in the f r o n t a l plane.  The specimens were fixed i n a mixture of  100 parts 96% alcohol, 40 parts formalin, and 7 parts g l a c i a l 94:95 acetic acid f o r 4 hours,  d e c a l c i f i e d i n RDO* f o r 12 hours,  and processed f o r haemotoxylin and eosin staining.  Two  5 u ^representative sections were taken from each h a l f of each femoral head.  One anterior, one posterior and two mid-sections  were thus examined from each side. Two major groups of animals underwent h i s t o l o g i c a l examination: 1. 60 long-term survival rabbits.  (Table VI). The  mismatched numbers of animals i n each  sub-group  were incurred p r i n c i p a l l y by deaths and complications. 2. 25 rabbits (Table VII) This group represents 5 sub-groups of 5 animals each, chosen randomly from a larger number survived f o r 3 to 4 weeks.  * MAYNARD DIAGNOSTIC, Ontario:  Constituents not revealed.  67.  F i g u r e 14:  A n c e r i o r aspect  of the r i g h t and  left  femora a f t e r long-term unreduced d i s l o c a t i o n hip.  Note the extreme coxa vora and  the abundant chondro-osseous t i s s u e of the l e s s e r  t r o c h a n t e r and  ant$.version formation  i n f e r i o r femoral  F i g u r e 15: A n t e r o - p o s t e r i o r x-ray  proximal  of the  Note  i n the  also  region  neck.  o f the p e l v i s and  w i t h i n 48 hours of unreduced d i s l o c a t i o n  left  of the l e f t  hips hip.  68.  C.  RADIOGRAPHIC: A l l animals intended f o r survival past 7 days were  x-rayed with 48 hours of the l a s t manipulation to the hip. (Figure 15).  A l l animals that underwent reduction, and  intended for survival past 7 days, were fluoroscoped 7 days a f t e r reduction to rule out delayed spontaneous radislocation. Thereafter repeat x-ray examination was  planned at four  week intervals in a l l cases. It soon became obvious that the flexion-adduction contracture of the hip present at 4 weeks rendered comparable positioning of the right and l e f t hips d i f f i c u l t , and possibly harmful to the reactive soft tissue and new blood vessel formation around the l e f t hip.  In vivo x-raying was  consequently abandoned as an investigative proceedure, and continued at 4 week intervals only in reduced animals to outrule redislocation. posterior radiograph was  At such intervals an anterotaken with both hips lying i n  the p r e f e r e n t i a l position of rest. The upper femora were x-rayed i n v i t r o a f t e r s a c r i f i c e and removal of the hind limbs, i n a l l cases before bissection and processing f o r histology.  69.  (a)  (b)  (c)  Figure 16: (a) Superioriaspect of the l e f t femoral head and neck. (b) Sectioned i n the f r o n t a l plane. Sections numbered 1 to 4, posterior to anterior. (c) Anterior aspect of the separated segments  Figure 17: (a). Anterior aspect of the separated segments of the femoral head and neck sectioned i n the frontal plane. The s o l i d dark f i l l i n g indicates perfusion with dye. (b) . Transfer of information regarding the location and extent of perfusion to a map, using the superior aspect of the femoral head. (c) . The f i n a l diagramatic map. There i s dye onjy within the postero l a t e r a l part of the femoral head.  70.  12  Figure 18: Inclusion of (b) the anterior view of the posterior segment (No. 1) augments the information offered i n Figure 17 (c) and Figure 18(a).  • •O M  (b)  (c)  Figure 19: Semiquantitative analysis. (a) perfusion equal, greater or s l i g h t l y less than control (b) perfusion considerably less than control (c) no perfusion (d) to the l e f t , the anterior view of the posterior segment, and to the r i g h t , the superior view of the femoral head and neck. IThere i s equal, greater or s l i g h t l y less perfusion than control p o s t e r o - l a t e r a l l y . There i s no perfusion antero-medially. The intermediate area i s considerably underperfused.  71.  RESULTS  A.  MICROANGIOGRAPHIC FINDINGS:  Steireomicroscopic examination of the perfused  sections  allowed a semiquantitative analysis of the l o c a t i o n , extent, and degree and source of vascular f i l l i n g within the head.  A composite map  femoral  could be made i n each case, and  information w i l l be presented 16i 17, 18 and  19.  EXPERIMENT I:  (Table II)  Infusion of dye proximal  the  as i l l u s t r a t e d i n Figures  to the a o r t i c b i f u r c a t i o n in  uninjured mature and immature animals consistantly yielded comparable perfusion of the femoral head on right and l e f t sides.  A s l i g h t quantitative difference was  observed between the i n d i v i d u a l sections. discrepancy  on occasion  This was  a uniform  i n a l l cases and p r i n c i p a l l y due to s l i g h t  differences i n section thickness.  The femoral heads when  assessed as a whole were quantitatively equal. Segmental defects i n perfusion were not observed,  EXPERIMENT I I : (Table III) 1.  In 30 immature rabbits the l e f t hip was dislocated  and l e f t unreduced.  Groups of 5 animals each were infused  and s a c r i f i c e d at 10 minutes and at 1,2,3,5 and dislocation.  7 days a f t e r  75 Figure 20 i l l u s t r a t e s the microangiographic findings at  10 minutes.  Disturbance of perfusion was  s i g n i f i c a n t in a l l cases.  present and .  The perfusion defecit varied,  with a gradual t r a n s i t i o n from reduced to absent dye i n the antero-medial part of the femoral head;  The extraosseous  vessels were obscured by dye which had leaked from damaged vessels belbw and behind the femoral head. At 24 hours a f t e r d i s l o c a t i o n , a greater c i r c u l a t o r y disturbance was observed  (Figure 20). Constant f i l l i n g  was  seen p o s t e r o - l a t e r a l l y , but the antero-medial % to 2/3 of the femoral head was  empty i n a l l cases.  Blood vessels were seen  connecting the epiphysis with the posterior trochanteric notch i n 4 cases, and with the greater trochanter i n 3 cases, such vessels are respectively uncommon, and rare in normal immature rabbits.  The extraosseous, postero-inferior vessels  to and from the epiphysis did not  fill.  The microangiographic piture at 2 and 3 days following d i s l o c a t i o n did not s i g n i f i c a n t l y d i f f e r from that seen at 24 hours, but a fine network of extraosseous vessels was  seen  developing on the postero i n f e r i o r femoral neck by the third day. Intraepiphyseal revascularization seemed to have commenced possibly on the f i f t h and c e r t a i n l y on the seventh day  (Figure 21).  The extraosseous meshwork of vessels noted  four days e a r l i e r had enlarged and was using the posteroinf e r i o r nutrient foramen of the epiphysis i n 4 cases. Perforation of  the growth plate, and epiphyseo-metaphyseal  anastomoses  73.  Figure 20: The results of unreduced dislocation In immature rabbits (a) at 10 minutes and (b) at 24".hours a f t e r dislocation.  Figure 21: The microangiographic pattern 7 days unreduced dislocation i n immature  rabbits.  following  75.  were noted in one case each at 5 and 7 days a f t e r dislocation.  2.  In 25 immature rabbits the l e f t hip was dislocated and  immediately reduced.  Groups of 5 animals each were infused  and s a c r i f i c e d at 10 minutes, and at 1,3,5  and 7 days a f t e r  reduction (Table I I I ) . A profound perfusion defedit was observed i n a l l cases within 10 minutes of reduction and this contrasted markedly with the picttire at 10 minutes following unreduced  dislocation  (Figure 22). Unlike these unreduced however, the c i r c u l a t o r y disturbance did not increase within 24 hours, but rather compared well with the microangiographic picture seen at 7 days following unreduced dislocation  (Figure 23).  Early  reduction seemed to enhance early recovery, and this was almost complete at 5 and 7 days a f t e r reduction (Figure 24). A notable feature i n those animals reduced early, was early use of the postero-inferior nutrient os to the epiphysis, as a route of blood supply. t h i r d day.  This was observed on the  Furthermore, f i l l i n g of the epiphyseal end of the  p r i n c i p a l epiphyseal vessels was observed i n three cases on the seventh day, although they did not bbviously connect with the main capsular vessels.  3.  The remaining subgroups  at 24  i n this experiment were reduced  and at 48 hours, so accounting f o r 40 immature animals  (Table I I I ) . In terms of the rate and extent of recovery  .<-y  of dye perfusion to the femoral head, those reduced at 24 hours did not d i f f e r from those reduced l a t e r . More important,  76.  Figure 22: The microangiographic pattern i n immature animals (a) at 10 minutes a f t e r immediate reduction and (b) 10 minutes a f t e r unreduced d i s l o c a t i o n .  79 s  (a) (b)  Figure 23: Microangiographic pattern in immature animals (a) 24 hours a f t e r immediate reduction and (b) 7 days a f t e r unreduced dislocation.  78\  (a)  (b)  Figure 24- Microangiographic pattern in immature animals (a) at 5 days and (b) 7 days following immediate reduction.  79-,  neither subgroup was seen to be s i g n i f i c a n t l y d i s t i n c t from those l e f t unreduced.  Furthermore, recovery seemed to  date not from the time of d i s l o c a t i o n , but rather the time of the l a s t injury to the j o i n t , that i s , reduction.  EXPERIMENT I I I : 1. In 10 mature rabbits the l e f t hip was dislocated and unreduced.  Groups of 5 animals each were infused and  s a c r i f i c e d at 10 minutes and 7 days (Table IV). At  10 minutes a f t e r dislocation c i r c u l a t o r y disturbance  was observed i n 4 out of 5 cases but in one only was  this  disturbance more than s l i g h t . At  7 days a l l animals but one had perfusion equal or  greater than control.  One had a segmental absence of vessel  f i l l i n g postero-medially (Figure 25). 2.  In 10 rabbits the l e f t hip was dislocated.  immediately and 5 at 24 hours.  5 were reduced  A l l were s a c r i f i c e d 7 days  a f t e r reduction (Table IV). Based on the microangiographic findings, these reduced subgroups could not be told apart, nor indeed did they s i g n i f i c a n t l y d i f f e r from those l e f t  unreduced.  The intraosseous epiphyseo-metaphyseal  anastomoses  across the epiphyseal scar f i l l e d i n a l l cases,,and seemed responsible as an avenue of blood supply and drainage i n adult animals.  (b)  Figure 25: Microangiographic pattern i n mature rabbits (a) at ±0 minutes and (b) 7 days after unreduced dislocation.  81.  EXPERIMENT IV: In 5 mature and 5 immature rabbits the l e f t h i p was dislocated and reduced at 12 hours.  A l l were s a c r i f i c e d  7 days l a t e r (Table V) 1.  Mature: As expected from Experiment I I I (results of which  were not available at the time), reduction at 12 hours resulted i n microangiographic findings indistinguishable from those adult animals unreduced, or reduced late. 2.  Immature:  The findings i n this subgoup s i m i l a r l y did  not d i f f e r from those i n animals unreduced, or reduced l a t e , i n Experiment I I .  HISTOLOGICAL FINDINGS:  H i s t o l o g i c a l investigation was intended p r i n c i p a l l y to augment analysis of the microangiographic findings. The aim in each case was therefore to establish the fact and extent of bone necrosis i f present, and to assess the degree, and e f f i c a c y of revascularization, reganeration and repair. Changes within the c a r t i l a g e of the a r t i c u l a r surface and growth plate were not c l o s e l y analysed, and no account of such alterations w i l l appear i n the text. The hall-marks of v i a b i l i t y were evident i n a l l control sections.  Marrow, although varying i n c e l l content and  haemopoeitic a c t i v i t y , nevertheless retained i t s highly  82  organized character throughout.  The trabecular stained  uniformly, and eonsiderable lengths of their cancellous surfaces were seen to be covered by a layer of endosteal cells  (Figure 26). Osteocyte morphology varied with the distance of the  c e l l from the nearest cancellous surface or Haversian system. In s u p e r f i c i a l situations the osteocyte nuclei appeared large, avoid and had a d i s t i n c t chromatin network.  More  deeply, the n u c l e i became smaller, spindle shaped, darker staining, and l o s t the fine chromatin meshwork.  Red blood  c e l l s were consistantly seen within the juxta a r t i c u l a r and juxta epiphyseal system of vessels.  Bone death was always obvious  Empty lacunae were  seen over extensive areas, alone, or i n conjunction with lacunae containing the remains of osteocytes such as poorly stained debris, f a i n t l y outlined anuclear c e l l s , or pyknatic n u c l e i .  Such bone always contrasted markedly with  the control side, and was accompanied by circumstantial evidence of death,  ranging from t o t a l and wide-spread  marrow i n f a r c t i o n with scattered debris and ghost c e l l s , to granulation tissue replacement bone apposition (Figure 27).  of marrow with hyperactive new Between these two extremes a  wide range of f i b r o c e l l u a r i t y of the marrow and endosteal a c t i v i t y was  observed.  New bone was e a s i l y recognized.  Always i t was marked  off from the dead bone by a d i s t i n c t cement l i n e which  83..  F i g u r e 26: H i s t o l o g i c a l femoral head. and  section  (H & E) o f the normal  The marrow p r e s e n t s an o r g a n i z e d appearance  i s haemopoeitically active.  The lacunae c o n t a i n s v i a b l e  o s t e o c y t e s . fin e n d o s t e a l l a y e r o f o s t e o b l a s t s c o v e r s the c e n t e r  trabeculum.  F i g u r e 27: H i s t o l o g i c a l s e c t i o n o f the l e f t  femoral head  f o l l o w i n g prolonged unreduced d i s l o c a t i o n .  There a r e s c a t t e r e d  areas of empty lacunae, and lacunae c o n t a i n i n g p o o r l y staining debris. has  spread  There i s h y p e r a c t i v e new bone f o r m a t i o n which  t o and p a r t l y r e p l a c e d the marrow c a v i t y .  84.  sheared  e a s i l y during processing.  It was common therefore  to find new bone partly or completely  separated  underlying dead trabeculae and appearing within the cancellous spaces.  from the  as a halo of bone  The deeper layers of new bone  were usually basophilic and woven i n type, and the s u p e r f i c i a l layers lamellated.  The osteocytes were more  numerous and c l o s e l y packed than i n the older bone and had large ovoid n u c l e i and well outlined chromatin. Endosteal a c t i v i t y was however variable. areas were c l e a r l y delineated from surrounding v i r t u e of t h e i r fibrous content.  Some cancellous dead bone by  These spaces contained  c l o s e l y packed fibrous tissue, of poor c e l l u l a r i t y , intimately associated with the dead trabeculae, but without an intervening layer of endosteal osteoblasts (Figure 28). Suprisingly, avascularity was not a feature i n these cases  (Figure 29)  and the reason f o r this apparent dormancy was not clear. More commonly however whole areas of dead trabeculae were outlined by many layers of osteoblasts rapidly laying down reactive Hone (Figure 2 7).  This new bone increased at the  expense of the cancellous spaces, and seemed to increase the t o t a l bone mass.  This phenomenon was commonly observed to  spread to the cancellous spaces per se, where large groups of osteoblasts were found i n mosaic form, laying down bone de novo (Figure 27).  \ 85.  Figure 28: H i s t o l o g i c a l section, of the l e f t femoral head following dislocation. The marrow i s replaced by grannulation tissue throughout. The trabeculae contain empty lacunae and basophilic? new bone apposition i s seen to the l e f t of the section. The new bone i s separated from the underlying dead trabeculae by a d i s t i n c t cement l i n e . There i s no endosteal a c t i v i t y to the right of the section.  Figure 29: High power photomicrograph from dislocated l e f t femoral head. The lacunae are empty and the marrow replaced by fibrous tissue. Despite the close proximity of the blood vessles, there i s no endosteal layer of c e l l s or osteoblastic activity  86.  A  E  B  F  Figure 30: Analysis of the H i s t o l o g i c a l Findings. A. Superior aspect of the l e f t femoral head and neck B. The sampling locations f o r h i s t o l o g i c a l sections C. Light-microscopic analysis, The s o l i d shading, as an example, respresents avascular necrosis. D. E and F: I l l u s t r a t i o n of how the h i s t o l o g i c a l features may be transferred to a composite map of the femoral head, and so i n d i c a t e the location and extent of avascular necrosis.  87.  As i l l u s t r a t e d in Figure 30, a composite map of the location and extent of h i s t o l o g i c a l v i a b i l i t y , death, revascularization and repair could be made i n each case, based on the s e r i a l sections of the femoral head. Total or sub-total necrosis was the most common finding overall  (70%). Complete v i a b i l i t y or minimal bone death  (limited to one or two medial trabeculae) occurred i n 24% of a l l cases examined. It therefore seemed the h i s t o l o g i c a l features almost obeyed an " a l l or none" law.  The findings  w i l l consequently be presented i n terms of these two extremes. The overall effects of skeletal maturity, reduction and early reduction are outlined i n Tables VIII,IX and X. The influence of skeletal maturity on the individual results of unreduced  dislocation and of early and delayed redaction  i s of necessity based on smaller groups of animals which rendee the conclusions less s i g n i f i c a n t .  This data i s  presented i n Table XI. A s t a t i s t i c a l analysis of the h i s t o l o g i c a l findings w i l l appear i n the Discussion of this study  C.  RADIOLOGICAL FINDINGS: This report i s based on i n vivo x-ray examination of the  separated hind limbs of 6 6 long-term survival animals, a f t e r sacrifice  (Table VI)  for assessment.  The plates from 55 cases were suitable  88.  Abnormal r a d i o l o g i c a l features were frequent and many, but highly v a r i a b l e , even within any one subgroup. The salient features w i l l be summarized. Increased radiolucency of the femoral neck was common observation.  the most  This finding rendered accurate  assessment of the injured femoral head radiodensity difficult  and frequently ersoneoas. For this reason the  right and l e f t femoral heads were compared only a f t e r blacking out the remainder of the upper femora with dark paper. In the majority of animals the right and l e f t femoral heads were indistinguishable i n terms of the radiodensity alone.  Absolute increase i n density (Figure 31), was  most common in those reduced  (9 of 39 cases) and absolute  decrease (Figure 32) i n those unreduced  (6 of 16 cases).  The femoral neck appeared osteopaenic i n the majority of injured hips.  Occasionally this radiolucency presented a  motheaten c y s t i c appearance with surrounding s c l e r o s i s . Coxa vara was  evident i n more than 50% of the immature animals  regardless of reduction, but was most severe i n those unreduced  and in this subgroup commonly associated with  deformity of the femoral head per se. Deformity of the femoral head was not observed i n those reduced and coxa vara in these animals was accounted for by shortening and widening of the femoral neck, and in some subcapital erosion of the infero-medial part of the femoral neck.  89.  The appearance of the growth plate varied from widening, which was rare, to premature closure which was most common and advanced i n those unreduced. Generally speaking the reduced subgroups could not be told apart on the x-ray findings, and those unreduced were d i s t i n c t only by v i r t u e of the degree to which they demonstrated the various abnormal r a d i o l o g i c a l features.  COMPARATIVE HISTOLOGY AND RADIOLOGY: The findings may be simply stated.  Increased  radiolucency was always associated with h i s t o l o g i c a l evidence of unbalanced resorption of bone within the epiphysis. This was most common i n those unreduced, and frequently associated with epiphyseal hyperaemia. Increased  radiodensity  was always associated with avascular necrosis and new bone apposition to the dead trabeculae.  However, radiodensity  judged comparable with the control side was compatable with both l i v i n g bone, formation.  and necrotic bone with new bone  90.  mm F i g u r e 31:  In v i t r o radiograph  proximal femora from an a d u l t d i s l o c a t i o n , and increase right  reduction  of the r i g h t and  at 24 hours.  i n r a d i o d e n s i t y of the  of the i l l u s t r a t i o n ) .  left  r a b b i t e i g h t weeks f o l l o w i n g left  Note the  femoral head  absolute (to  the  91.  Figure 32: In v i t r o radiograph of the proximal femora from an adult rabbit with long term unreduced dislocation of the l e f t hip. Note the diminished radiodensity of the femoral head and superior femoral neck, and associated coxa vara, of the l e f t hip. (t'o "tH'e right of the i l l u s t r a t i o n ) .  BISCUSSION Death of the femoral head, iri whole or part, may  be  expected to ensue i n 10% of children and up to 307« of adults following traumatic dislocation of the hip. The age in childhood, skeletal maturity, severity of the injury, and duration of dislcoation considerably influence the incidence of avascular necrosis but the individual contribution of these factors to the outcome i s d i f f i c u l t to assess as they are c l o s e l y inter-related. The cause of avascular necrosis of the femoral head a f t e r d i s l o c a t i o n i s not known, but we have good reason to believe that damage to the intracapsular or immediately extracapsular course of the epiphyseal vessels i s a major factor in i t s genesis.  The series of events that occur  following displacement, and how  they affect the c i r c u l a t i o n  within the femoral head i s s i m i l a r l y unknown. Our current concepts in this regard are based largely on indirect evidence from c l i n i c a l , pathological, r a d i o l o g i c a l and experimental 100 data.  SEVITT  investigated one case of posterior dislocation  of the hip in an eighteen year old male, by graphy.  microarterio-  The femoral head had been reduced soon a f t e r injury,  but the patient l a t e r succumbed to associated i n j u r i e s . Diaphyseal-metaphyseal  connections were demonstrated within  the base of the femoral neck, but the femoral head was  <93. largely avascular, and the retinacular vessels f a i l e d to fill.  This i s the only report of i t s type in the l i t e r a t u r e . Experimental dislocation of the hip in animals s i m i l a r l y  causes avascular necrosis of the femoral head. The incidence and extent i s however highly variable between 11  individual investigators.  BOHR  using  microarteriography,  documented the weekly series of events following manual dislocation of the hip in newborn rabbits, but wa  are  aware that femoral head v i a b i l i t y i s p a r t i c u l a r l y dependant on the ligamentum teres vessels at this in rabbits.  The affects of this injury on adult  age and  growing animals have not been s u f f i c i e n t l y compared in any single study.  The influence of reduction has  not  been investigated. The rabbit i s a suitable experimental model. Anatomical dissection, microarteriography  and the results  of s e l e c t i v e interference with the postero-inferior nutrient vessels of the c a p i t a l epiphysis has proven the functional s i m i l a r i t y between these vessels and superior retinacular system in man.  the  The individual role  of the ligamentum teres vessels i s uncertain in each species. These vessels are perhaps most important as a route of revascularization should  the femoral head suffer necrosis.  Species differences i n this regard would be minimized by d i s l o c a t i o n which of i t s nature implies ligamentum teres  rupture.  $4.  The value of microangiography in terms of i t s functional relationship to the actual perfusion by blood of the femoral head, i s d i f f i c u l t to assess.  The dye used was  designed during extensive p i l o t studies to f i l l both the afferent and efferent vessels, and so cross the c a p i l l a r y bed.  For this reason the larger intraosseous vessels  were usually obscured and perfusion assessed on the location and extent of microvascular f i l l i n g .  The v i s c o c i t y of the  dye compared with whole rabbit blood at body temperature was 1.6.  The aggregate size of the carbon p a r t i c l e s as measured  in v i t r o did not exceed 4 microns, and on repeated examination  of bone sections prepared for routine histology  and by the Spalteholz technique, extravasation of dye from the vessels was not observed  (Figures 7 and 33).  The y i e l d  of t e c h n i c a l l y acceptable results within the control hips was high.  Furthermore the pattern of segmental c i r c u l a t o r y  disturbance, as i l l u s t r a t e d , was usually consistant, and reflected a gradual t r a n s i t i o n from case to case. reasons  I believe that the microangiographic  For these  pattern  observed bore a close relationship to the patency of the microvasculature, and so the perfusion by blood of the femoral head, at the time of infusion. The severity of the injury was  standardized by one  operator using one technique throughout.  This has  limitations  which are r e a l i z e d , but offers considerably more control over the trauma than seen i n the comparable c l i n i c a l s i t u a t i o n i n man where the mechanism and severity of the injury cannot be considered a l i k e in any two cases.  95.  (b) Figure 35.: H i s t o l o g i c a l sections of the femoral head following infusion. The dye i s c l e a r l y outlined and well contained within (a) the marrow sinusoids and (b) the capillaries.  96.  The animals were grouped and subgrouped and  a c c o r d i n g to S k e l e t a l m a t u r i t y  On the b a s i s of the d u r a t i o n of d i s l o c a t i o n  the time of r e d u c t i o n .  I t h e r e f o r e b e l i e v e that  and v a l u a b l e c o n c l u s i o n s may  valid  be drawn w i t h regard to the  i n d i v i d u a l i n f l u e n c e of these f a c t o r s on the outcome. Reduction was i t was  u s u a l l y c l i n i c a l l y obvious. N e v e r t h e l e s s  c o n f i r m e d i n a l l cases by f l u o r o s c o p i c  of the h i p w i t h i n ten minutes.  examination  Repeat f l u o r o s c o p y a t  seven  days and monthly x - r a y s s e r v e d as f u r t h e r c o n f i r m a t i o n i n those animals s u r v i v e d past seven days.  Clinical  examination  ( l e g - l e n g t h ) ' under a n a e s t h e s i a a t the time of i n f u s i o n the p o s i t i o n of the femoral head a f t e r c a r e f u l was  used  animal  to r u l e out spontaneous was  and  dissection  r e d i s l o c a t i o n . w h e n the  s a c r i f i c e d w i t h i n seven days. D a i l y  fluroscopic  examination would have been ""ideal, and c l o s e to the c o u n c i l of p e r f e c t i o n .  The need f o r a g e n e r a l a n a e s t h e t i c i n each  case and at each examination however rendered t h i s impractical  an  goal.  In t h i s study, d i s l o c a t i o n caused a p e r f u s i o n d e f e c i t w i t h i n ten minutes The d i s t u r b a n c e was  segmental  significant  i n immature animals.  i n type and seemed c o n s t a n t  i n c h a r a c t e r i n s o f a r as the a n t e r o - m e d i a l part of the femoral head c o n s i s t a n t l y s u f f e r e d d i m i n u t i o n i n v a s c u l a r  97  filling  (Figure 20(a) ).  Judging by the findings, i n  animals s a c r i f i c e d after ten minutes, the c i r c u l a t o r y  "  • .'-  disturbance worsened within twenty-four hours and thereafter remained constant i n degree and extent u n t i l f i v e to seven days a f t e r injury, when recovery commenced. (Figure 20(b) & 21) 11,12,70 Such recovery has been observed to occur i n rabbits ' ' and other animals, but usually within the second week a f t e r 15 138 injury .' These investigators had however Induced massive epiphyseal necrosis by s e l e c t i v e or gross interference 95 with the epiphyseal-metaphyseal  vessels. ROSINGH  has  observed revascularization to occur with the infarcted rabbit c a p i t a l epiphysis three days following injury.  In  this study the principal extraosseous epiphyseal vessels f a i l e d to f i l l up to and including seven days from dislocation. Epiphyseal vascular connections with the greater trochanter and posterior trochanteric notch were observed to enlarge and maintain perfusion of a limited part of the posterol a t e r a l epiphysis throughout.  Effective recovery was  coincident with appearance of a rich extraosseous network of vessels at the postero-inferior aspect of the femoral neck.  This meshwork was  f i r s t noticed on the t h i r d day  a f t e r injury, and seemed to use the postero-inferior nutrient foramen of the femoral head as a route of supply and drainage at the seventh day.  Intraosseous  metaphyseal connections were developed  epiphyseo-  in one animal each at  f i v e and seven days by perforation of the growth plate.  98,  This phenomenon was  a constant  feature in a l l of BOHR's 11, 12 immature rabbits, during the second week.  In mature animals d i s l o c a t i o n again caused interference with perfusion within ten minutes (Figure 25(a) This was  ).  judged s i g n i f i c a n t in one animal anly. S i m i l a r l y ,  seven days a f t e r injury only one animal demonstrated a s i g n i f i c a n t c i r c u l a t o r y disturbance within the femoral head (Figure 25(b)  ).  F i l l i n g of the intraosseous epiphyseo-  metaphyseal anastomoses across the epiphyseal scar noted in a l l mature animals at both periods.  was  The major  extraosseous epiphyseal vessels as i n growing animals, f a i l e d to f i l l at ten minutes and seven days. Immediate reduction i n growing rabbits was  associated with  a most profound perfusion defecit at ten minutes (Figure  22)  indicating greater injury than that induced by d i s l o c a t i o n alone. However judging by the microangiographic at 1, 3, 5 and 7 days, early reduction had enhanced early and complete recovery was  findings  obviously  (Figure 24), Again i t  noted that recovery paralleled use of the  postero-  i n f e r i o r route of supply to the femoral head, and i n some cases use of the major postero-inferior retinacular vessels. These vessels did not obviously connect with the capsular stem vessels however and presumably f i l l e d by a more circuitous route, either v i a the "circulus a r t i c u l i vasculosus" or in a retrograde fashion from the metaphysis.  99.  Recovery of the femoral head perfusion in immature animals reduced at 12, 24 and 48 hours proceeded at a rate comparable to that observed in unreduced animals.  The events  within the extraosseous system of vessels were also similar. It i s interesting to note that revascularization seemed to date from the last manipulation of the hip.  As an example,  the microangiographic picture i n those animals reduced at 48 hours did not compare well t i l l  7 days a f t e r  reduction, with those animals unreduced though i n the former the infusion was 9 days a f t e r the i n i t i a l  f o r 7 days, even  in effect conducted  injury.  In adult animals the reduced and unreduced  subgroups  were indistinguishable on the basis of the microangiographic picture at seven days alone.  Dislocation per se infrequently  caused a s i g n i f i c a n t perfusion defecit and so the b e n e f i c i a l affects of reduction, i f any, were obscured.  Perfusion defecit was  therefore most obvious i n  immature animals, increased with time and recovered with p a r a l l e l recovery of an extraosseous route of blood supply. Reduction was of benefit to immature animals only and altered the expected s e r i a l events following dislocation only i f achieved in less than twelve hours. was equally b e n e f i c i a l , to intraosseous and  Early reduction immediately  extraosseous c i r c u l a t i o n a l i k e and recovery i n these locations was  coincident.  100  The p r i n c i p a l retinacular vessels recovered only i n some of those immature animals reduced early and did not obviously connect with the capsular vessels.  These findings  would suggest that damage to the postero-inferior branch of the medial circumflex femoral artery before or during i t s passage through the hip joint capsule was to a large part responsible for the c i r c u l a t o r y disturbance by d i s l o c a t i o n .  This was confirmed  at gross dissection  by the frequent finding of a torn or avulsed j o i n t capsule, presumably suffered during excursion of the femoral head and neck.  inferior  postero-superior Early reduction  offset whatever detrimental effects continued caused.  induced  displacement  It i s well to remember that a l l rabbits reduced  late were allowed unlimited a c t i v i t y u n t i l the time of reduction.  It i s reasonable  to presume such a c t i v i t y added  i n s u l t to injury. The intraosseous epiphyseo-metaphyseal anastomoses minimized the effects of dislocation i n adult animals and recovery was not dependant on a p a r a l l e l return of an extraosseous  route of blood supply to the femoral spiphysis.  The influence of early reduction, i f any, was therefore masked. The h i s t o l o g i c a l c h a r a c t e r i s t i c s of revascularization and repair following avascular necrosis of the femoral head or other osseous tissue has been well and repeatedly , .... 3,13,23,25,26,56,85,98,99,101 3,13,23 10,11 described i n man and animals 12,15,47,94,95,122,138  Granulation tissue origionating  101.  p r i n c i p a l l y from the metaphysis and fovea c e n t r a l i s ( i f the ligamentum teres i s intact) invades the infarcted cancellous of new  spaces and  i s followed by an advancing wave  bone which i s l a i d down upon the non-viable  trabeculae.  Transformation of the c e l l u l a r elements of the  invading vascular connective tissue, to osteoblasts, i s responsible for this new  This process was 85 86 87 termed ''creeping s u b s t i t u t i o n " by PHEMISTER ' ' although 10 l a t e r BABECHKO and HARRIS  bone.  were to describe i t as  "creeping  apposition" and so stress the i n i t i a l tendency towards bone formation, rather than coexisting regeneration resorption.  The delay in man  between invasion and  and cellular  transformation i s variable and depends on the age, s i t e . •• 86,87 and functional use of the part. In the rabbit this duration i s less variable. Complete r e o s s i f i c a t i o n of the infarcted c a p i t a l epiphysis has been demonstrated by six weeks i n immature rabbits following experimental epiphyseal 47 separation, and by eight weeks in adult rabbits a f t e r 10 subcapital osteotomy.  Reossification in the rabbit i s  therefore dependant on the rate of revascularization and the speed and extent of revascularization depends on hindrences" met a hindrence  en route.  the  The growth plate can offer such  and has, been demonstrated to act as a staunch  b a r r i e r to vascular invasion from the metaphysis in . , 10,47. experimental animals.  102.  ROSINGH and h i s associates  have described  in the vascularization and repair of the c a p i t a l epiphysis in the rabbit.  four phases  avascular  The f i r s t phase i s  characterized by tissue decay, the second by  granulation  tissue invasion, the third by c e l l u l a r d i f f e r e n t i a t i o n within the new  connective tissue and new  bone apposition,  and the fourth or reparative phase, by gradual return of the marrow elements to normal.  These authors had  noticed  revascularization within three days of ingury i n some cases. A s i m i l a r series of events was  observed by BRASHEAR*  following experimental i n f a r c t i o n of the lower femoral  95 epiphysis in the rat.  In ROSINGHS study  dead  trabeculae  were noted to remain within the apposed new bone covering  for the length of the experiment, which was  21  weeks. It was  not therefore elected to repeat these  studies and evaluate the h i s t o l o g i c a l series of events following d i s l o c a t i o n in this study.  It was  presumed  that repair would follow revascularization, and  that  the  e a r l i e r microangiographic study would o f f e r s u f f i c i e n t information  regarding  vessel invasion.  the rate and extent of blood  It was  further presumed that  avascular  bone i f observed up to 10 weeks following injury would have dated from the time of d i s l o c a t i o n or  reduction.  Separate analysis of animals s a c r i f i c e d at four and at eight weeks a f t e r d i s l o c a t i o n did not reveal any evidence of continued bone damage.  103  In this study t o t a l or subtotal avascular necrosis occurred In 51% of adult and 847= of growing animals. . " _ Absent or minimal necrosis occurred i n 3 7% of mature and 147, of immature animals  (Table VIII)  are s t a t i s t i c a l l y s i g n i f i c a n t  These differences  (Total or subtotal: p value  less than 0.05. Minimal of absent: p value equals 0.05) The h i s t o l o g i c a l and microangiographic findings were therefore complimentary  and favored the adult animal.  However the overall incidence of 317> extensive necrosis i n mature animals was unexpected, and surprising in view of the microangiographic findings at 10 minutes and 7 days a f t e r dislocation  (Figure 25). There are perhaps two explanations.  One, as suggested by STEWART and MILFORD*  that i n t r a  c e l l u l a r damage caused by the force and counterforce of the injury largely governed vascular injury and repair.  the outcome regardless of the This would not explain the  small, but s i g n i f i c a n t difference between ad'ilt and growing animals.  The l i t e r a t u r e i n general and this study cannot  support or refute this hypothesis  A l t e r n a t i v e l y the  adult femoral heads may have suffered periods of prolonged hypoxia not stressed by the outline of the study. As 136 suggested by W00DH0USE and demonstrated by ROSINGH and 94 JAMES  using Fuelgen-DNA microdensitometry, osteocytes  suffer irreparable c e l l u l a r damage a f t e r six hours of anoxia. Perfusion of the femoral head was demonstrated to considerably deteriorate within 24 hours of dislocation in immature animals.  (Figure 20).  104.  T h i s was  not i n v e s t i g a t e d  minute and  i n a d u l t r a b b i t s as the  7 day p e r f u s i o n p a t t e r n and c o n s t a n t  metaphyseal  anastomotic  filling  suggested  e a r l y complete  and  i n view of the h i s t o l o g i c a l  particularly  seems l i k e l y after of  that 50%  epiphyseo-  limited  embarassment and  10  circulatory  r e c o v e r y . In r e t r o s p e c t , findings, i t  of a d u l t animals s u f f e r e d  deterioration  ten minutes, and a prolonged p e r i o d of anoxia or h y p o x i a  the femoral head; Reduction o v e r a l l , and p a r t i c u l a r l y  i n immature animals seemed to b e n e f i t outcome b e n e f i c i a l l y  (Tables IX,X  the h i s t o l o g i c a l  & XI)  number of animals i n these subgroups  immediate r e d u c t i o n  However, the  i s not s u f f i c i e n t to  support t h i s  observation s t a t i s t i c a l l y .  histological  and m i c r o a n g i o g r a p h i c f i n d i n g s a r e not  c o n t r a d i c t o r y i n t h i s regard. even e a r l y , was In growing  N e v e r t h e l e s s the  In a d u l t animals r e d u c t i o n ,  not demonstrated  to i n f l u e n c e the outcome.  animals a l t h o u g h e a r l y r e d u c t i o n enhanced  and complete  r e c o v e r y , profound c i r c u l a t o r y  was  demonstrated  two  o f the f o u r animals i n f u s e d a t 24 hours  recovery  w i t h i n 10 minutes  early  embarassment  (Figure 22) and o n l y  ( F i g u r e 23). In both mature and  demonstrated  immature animals  t h e r e f o r e a prolonged p e r i o d of hypoxia w i t h i n the femoral head d u r i n g the f i r s t this  study.  24 h o u r s , cannot be o u t r u l e d  by  105.  More important,  the h i s t o l o g i c a l findings s e r i o u s l y  challenge the influence of continued dislocation and delayed reduction on the incidence of avascular necrosis. Although i n many instances i n man the severity of the injury 16 and the duration of d i s l o c a t i o n are i n t e r - r e l a t e d , BRAV s figures s i g n i f y c l e a r l y that delay i n reduction past 12 hours i s associated with a 3-fold increase i n the incidence of avascular necrosis regardless of the presence and degree of bone damage.  How may these figures be interpreted?  BRAV graded avascular necrosis according to the r a d i o l o g i c a l features.  Slight to moderate a l t e r a t i o n i n radiodensity  only, without accompanying deformity of the femoral head 14 was present i n 45% of h i s cases.  BOYD  and GLASS and  POWELL^ have stressed the d i f f i c u l t y and u n r e l i a b i l i t y of d i f f e r e n t i a t i n g between degenerative  arthritis and  avascular necrosis of the femoral head a f t e r trauma to the h i p , i n the absence of f l a t t e i n g or collapse of the weightbearing area. •  1  Only 55% of BRAV's cases demonstrated  6  this sign. Does r a d i o l o g i c a l examination y i e l d an accurate index of the incidence of avascular necrosis of the femoral 13 56 head a f t e r injury? BOHR and HULTH have demonstrated that dead trabeculae retain normal mineralization up to f i v e 26 years following injury.  CATTO  described 12 cases of late  segmental collapse following femoral neck fracture, i n which the r a d i o l o g i c a l features were normal u n t i l the onset of deformity.  This was despite the fact that t o t a l or  106  subtotal necrosis of the femoral head was demonstrated on subsequent h i s t o l o g i c a l examination.  i t would seem  therefore that dead bOrie per se has a normal  radiological  appearance; and that the consequences, rather than the fact of avascular necrosis are responsible for the indices on which we make a r a d i o l o g i c a l  diagnosis.  Revascularization and new bone apposition with increase in trabecular width and t o t a l bone content of the femoral head has been demonstrated to cause increased in man  13,56  ,  3  ,  and animals  10,95  .  radiodensity  Furthermore, collapse  occurs within a segment of the femoral head which has f a i l e d ,  .  26,101.  to revascularize  _  .  ,  These signs are respectively a  consequence of adequate and inadequate repair and do not necessarily relate to the actual incidence of avascular 96  necrosis.  SEVITT  examined 25 femoral heads removed from  cadavera up to 10 years following femoral neck fracture. He found h i s t o l o g i c a l evidence of s i g n i f i c a n t bone death in 847o, and of t o t a l or subtotal necrosis in 647,. His 4 23  figures contrast markedly with the 15 to 457'  '  37  '  39  '  42  '  45  incidence of avascular necrosis which has been documented on the basis of c l i n i c o - r a d i o l o g i c a l c r i t e r i a e alone. It seems therefore that not a l l cases go on to develop the r a d i o l o g i c a l l y obvious signs of successful or hindered repair on which the diagnosis i s dependant.  On this basis  16  BRAV's  figures may be interpreted i n a new l i g h t . Acceptir  that f l a t t e i n g or collapse of the femoral head i s the most  107  r e l i a b l e r a d i o l o g i c a l index of past ischaemic necrosis, i t would seem that delay i n reduction  past 12 hours i s  associated  in the occurrence of  with a three-fold increase  frustrated revascularization and repair, but that we not know the incidence  of avascular necrosis  In this study early reduction was  per_ee.  observed to enhance  early revascularization in immature rabbits. 16 support the neo  do  interpretation of BRAV's  This would  figures as  discussed above. Why  then did h i s t o l o g i c a l examination not reveal a  highec incidence  of poorly vascularized  segments within  femoral head in rabbits unreduced or reduced late?  the  The  Important s i z e , - difference between the femoral heads of 41 man  and  the rabbit must be considred in this regard. GALLIE  suggested there was  a physiological l i m i t to which bone  as a tissue could be expected to revascularize a f t e r ischaemic necrosis.  He stated that the femoral head in  small experimental animals probably f e l l well within  this  l i m i t . Consequently factors hindering or exhausting repair in man would not be as e a s i l y demonstrated in animals. 14 BOYD  also drew on this hypothesis of the  "physiological  l i m i t " to explain the phenomenon of delayed segmental collapse in man. necrosis  If we  i s influenced  therefore accept that repair and by the duration  of d i s l o c a t i o n , then  the results of this study support the concept that reduction w i l l reduce the incidence collapse.  not  early  of late segmental  108  In this study, extensive avascular necrosis was c l e a r l y more common i n growing animals, c h i e f l y on account of the growth-plate which prohibited early intraosseous c o l l a t e r a l compensation a f t e r damage to the extraosseous epiphyseal vessels.  In man, the more precarious blood  supply of the femoral head before skeletal maturity i s 120 well established.  I t i s c l e a r that the severity of the  injury which Is usually greater i n adults i s responsible for the higher incidence of avascular necrosis a f t e r skeletal maturity.  But i n considering simple dislocation  alone, the incidence i n adults approaches, but i s not l e s s , than that seen i n childhood. The reason for this discrepancy between what i s expected and what i s observed i s not c l e a r , but the concept of the "physiological l i m i t " of 41 14 bone repair as forwarded by GALLIE be c i t e d i n explanation.  and BOYD  could well  This study and our current  knowledge of the peculiar vascular anatomy of the femoral head would suggest that children s u f f e r a higher incidence of ischaemic necrosis than adults following an injury of s i m i l a r severity.  However £'s .the affif^acy bff 'h±Qlogical  repair i s inversely related to the age of the organism, the c h i l d i s less apt to develop.the features of frustrated revascularization on which our c l i n i c o r a d i o l o g i c a l diagnosis of avascular necrosis must rest.  109  Absolute  a l t e r a t i o n i n the radiodensity of the  injured femoral head was  absent or uncertain i n the  majority of animals x-rayed by the i n v i t r o technique between  f i v e and ten weeks a f t e r injury.  When  present however the radiographic abnormality c l o s e l y correlated with the h i s t o l o g i c a l findings. readiodensity was  Increased  always associated with bone 'death,  new bone apposition, and increased bone mass within the 13 ,51 femoral head.  This has been previously reported in man' '  and experimental  animals*^  In p a r t i c u l a r BOHR^, on  examination of 20 human femoral heads removed 5 days to 5 years a f t e r femoral neck fracture found that radios c l e r o s i s d i r e c t l y and consistantly related to increased trabecular width due to new bone apposition. Densitometry revealed comparable mineralization between dead and l i v i n g 56 bone. HULTH s i m i l a r l y concluded with x-ray d i f f r a c t i o n 9'. that dead bone retained i t s normal mineralization. ROSINGH objectively estimated  the bone-marrow r a t i o in 30 young  rabbits, including 15 cantrols, a f t e r inducing necrosis.  epiphyseal  Increase i n this r a t i o was noted 3 weeks a f t e r  avascular necrosis and coincided with new bone formation and increased radiodensity.  The r a t i o returned to normal  from 6 weeks onwards with concurrent radiodensity.  reduction in  110.  When present therefore, increased radiodensity of the femoral head always s i g n i f i e d avascular necrosis. In the majority of cases however, the avascular  femoral  head had an appearance comparable with the control side and so radiographic examination at 5 to 10 weeks did not prove a r e l i a b l e index of the incidence of necrosis.  ischaemic  SUMMARY  A microangiographic, h i s t o l o g i c a l and radiographic investigation  of the femoral head following  dislocation of the h i p i n 220 rabbits Dislocation  experimental  i s reported.  of the l e f t hip was induced manually  under anaesthesia by a dorsally applied hip held adducted i n t e r n a l l y rotated Reduction was effected by ventral  force with the  and s l i g h t l y extended  traction with the  hip held i n the same position. The animals were grouped according to skeletal maturity, and subgrouped on the basis of the duration of d i s l o c a t i o n and time of reduction.  The l e f t hip was  manipulated by one operator using one technique throughout The  right hip was untouched and used as a control The affects of d i s l o c a t i o n , persistant  and  reduction at varying intervals  dislocation,  (immediately, 12,24  and 48 hours a f t e r dislocation) were studied by microangiography at 10 minutes, 1 , 3 , 5  and 7 days after  injury, and by h i s t o l o g i c a l and radiographic examination up to 10 weeks a f t e r dislocation. The 1.  purpose of the study was:  To establish the segmental changes i n blood supply of the femoral head following  experimental traumatic  dislocation of the h i p i n rabbits.  112  2. To evaluate the influence of the duration of dislocation. 3. To evaluate the influence of skeletal maturity. 4. To evaluate the influence of reduction 5. To analyze what relationship the early changes in blood supply of the femoral head may bear to the l a t e r h i s t o l o g i c a l and radiographic findings.  113.  CONCLUSIONS  Traumatic dislocation of the hip causes c i r c u l a t o r y embarassment rabbits.  i n the femoral head i n mature and immature  Damage to the extraosseous epiphyseal-  metaphyseal vessels of blood supply and drainage i s a major causative factor.  The perfusion defecit i s most severe i n immature animals, and i s maximal i n the antero-medial portion of the femoral head which i s devoid of perfusion or considerably underperfused within ten minutes of dislocation.  Disturbance of c i r c l u a t i o n i n immature animals worsens with continued dislocation to reach a maximum within 24 hours.  Recovery does not commence u n t i l 7 days  a f t e r dislocation.  Recovery of perfusion within the femoral head of immature animals with unreduced dislocation i s coincident with development of an extraosseous network of epiphyseal blood supply and drainage on the postero-inferior  femoral neck.  114  Reduction i s per se injurious to the blood supply of the femoral head, but i f early, enhances early and complete recovery of blood supply.  Reduction delayed to 12 hours or longer a f t e r d i s l o c a t i o n does not benefit the rate arid extent of return of perfusion of the femoral head.  In mature animals, the intraosseous epiphyseemetaphyseal anastomoses across the obliterated growth plate are seen to minimize the perfusion defecit induced by dislocation and enhance early and complete recovery of blood supply of the femoral head. Consequently  the possible benefits of reduction are  obscured.  H i s t o l o g i c a l l y demonstrable avascular necrosis of the femoral head occurrs i n the majority of animals regardless of skeletal maturity or reduction. It i s more common and more extensive i n immature animals.  Early recovery of blood supply does not consistantly minimize or prevent h i s t o l o g i c a l avascular necrosis of the femoral head.  115.  Abnormal r a d i o l o g i c a l features within the femoral head are infrequently observed up to ten weeks a f t e r d i s l o c a t i o n , but correlate well with the h i s t o l o g i c a l findings when present.  Absence of abnormal r a d i o l o g i c a l features within the femoral head does not outrule avasaular necros  TABLE I CLINICO-RADIOLOGICAL OUTCOME IN 207 HIPS FOLLOWING TRAUMATIC POSTERIOR DISLOCATION  AUTHOR Thompson & ^ Epstein  Stewart & Milford  GRADE  OUTCOME  117  Excellent or Good  1 66%  II 33%  III 10%  Fair or Poor  33%  66%  90%  Excellent or Good  66%  44%  22%  Fair or Poor  33%  56%  78%  * Amended Grading (by the author) I: simple dislocation II: dislocation & associated acetabular rim fracture. One or more large fragments. Ill: dislocation & greater associated bone damage  TABLE II  EXPERIMENT I  Normal Rabbits MATURE -  5 animals  IMMATURE - 5 animals  113  TABLE III  EXPERIMENT II  Subgroup  Number  5 animals sacrificed  Dislocated alone  20  1,3,5 & 7 days  Reduced - immediate  20  1,3,5 & 7 days  Reduced -@ 24 hours  20  1,3,5 & 7 days  Reduced - @ 48 hours  20  1,3,5 & 7 days  Dislocated alone  5  @ 10 mins  Reduced - immediate  5  @ 10 mins  Dislocated alone  5  @ 2 days  119  TABLE IV  EXPERIMENT 111  Subgroup  Number  Sacrificed  Dislocated alone  5  @ 10 mins  Dislocated alone  5  @ 7 days  Reduced - immediate  5  @ 7 days  Reduced - @ 24 hours  5  @ 7 days  120  TABLE V  EXPERIMENT IV Subgroup  Number  Sacrificed  MATURE: Reduced @ 12 hrs  5  @ 7 days  IMMATURE: Reduced @ 12 hrs  5  @ 7 days  121  TABLE VI LONQ TERM ANIMALS FOR HISTOLOGICAL EXAMINATION  IMMATURE - 35 animals Dislocated Reduced - immediate Reduced - @ 24 hours Reduced - @ 48 hours  Number  Average Duration  9 9 7 10  7 weeks 6 6 5  8 8 4 5  10 weeks 9 8 8  MATURE - 25 animals Dislocated Reduced - immediate Reduced - @ 24 hours Reduced - @ 48 hours  122  TABLE VII  SHORTTERM ANIMALS FOR HISTOLOGICAL EXAMINATION  IMMATURE - 15 animals Dislocated Reduced - immediate Reduced - delayed  Number  Average Duration  5 5 5  4 weeks 4 4  5 5  3 weeks 3  MATURE - 10: animals. Dislocated Reduced - immediate  123  TABLE VIII  THE EFFECT OF SKELETAL MATURITY AT THE TIME OF INJURY, ON THE HISTOLOGICAL OUTCOME, REGARDLESS OF REDUCTION  MATURE:  35 Rabbits  Total or subtotal necrosis Minimal or absent necrosis  - 18 animals (51%) - 13 animals (37%)  IMMATURE: 50 Rabbits Total or subtotal necrosis Minimal or absent necrosis  - 42 animals (84%) - 7 animals (14%)  124  TABLE IX  THE INFLUENCE OF REDUCTION, ON THE HISTOLOGICAL OUTCOME, REGARDLESS OF SKELETAL MATURITY  Unreduced: 27 Rabbits Total or subtotal necrosis  - 21 animals (78%)  Reduced, earl/ or delayed: 58 Rabbits Total or subtotal necrosis - 39 animals (67%)  125  TABLE X  THE INFLUENCE OF EARLY REDUCTION, ON THE HISTOLOGICAL OUTCOME, REGARDLESS OF SKELETAL MATURITY  Immediate Reduction: 27 Rabbits Total or subtotal necrosis  16 animals (59%)  Delayed Reduction: 31 Rabbits Total or subtotal necrosis  23 animals (74%)  Unreduced dislocation: 27 Rabbits Total or subtotal necrosis  21 animals (78%)  126  TABLE XI  THE INFLUENCE OF BOTH SKELETAL MATURING & TREATMENT ON THE INCIDENCE OF TOTAL OR SUB-TOTAL HISTOLOGICAL AVASCULAR NECROSIS  IMMATURE: 50 Rabbits Unreduced Dislocation: 14 animals Total or Subtotal necrosis Earl/ reduction: 14 animals Total or Subtotal necrosis Delayed reduction: 22 animals Total or Subtotal necrosis MATURE: 35 Rabbits Unreduced dislocation: 13 animals Total or subtotal necrosis Early reduction: 13 animals Total or subtotal necrosis Delayed reduction: 9 animals Total or subtotal necrosis  13 animals (94%) 10 animals (71%) 19 animals (86%)  8 animals (61.5%) 6 animals (46%) 4 animals (44%)  127. 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