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The relationship of prenatal maternal depression or anxiety to maternal caregiving behavior and infant… Warnock, Fay F; Craig, Kenneth D; Bakeman, Roger; Castral, Thaila; Mirlashari, Jila Sep 7, 2016

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RESEARCH ARTICLE Open AccessThe relationship of prenatal maternaldepression or anxiety to maternalcaregiving behavior and infant behaviorself-regulation during infant heel lance: anethological time-based study of behaviorFay F. Warnock1,2*, Kenneth D. Craig3, Roger Bakeman4, Thaila Castral5 and Jila Mirlashari6AbstractBackground: Sensitive and responsive maternal caregiving behavior strengthens infant self-regulatory capacities (HL),but this regulatory role may be diminished in some mothers with second-trimester prenatal exposure to depressionand/ or anxiety (MDA). This study examined maternal and infant behavior during infant heel lance (HL) when mothershad or did not have MDA. Ethological methods and micro-analytic approaches capable of distinguishing andcomparing time-based patterning in maternal and infant behavior were used to clarify biological mechanisms, such asMDA, that may underlie observed behavior. Aims were to examine group differences in caregiving behavior betweenmothers with and without MDA 5 min Pre-HL and 5 min Post-H, and relationships between MDA, maternal caregivingbehavior and infant pain behavior self-regulation, concurrently.Methods: At second trimester, mothers were assessed for symptoms of mild-severe depression or anxiety. Motherswhose scores exceeded predetermined cut-off scores on one or more of the mental health measures were allocated tothe MDA-exposure group, those below to the non-MDA-exposure group. Reliable observers, blinded to MDA statusand study phases, coded video records of the caregiving behavior of each study mother for the full duration of the5 min Pre-HL and 5 min Post-HL study phases. Group differences and associations between mean measures ofmaternal mental health scores, time-based measures of maternal behavior, and time-based measures of infant painbehavior regulation (previously coded) were concurrently analyzed using comparative and correlational statistics.Results: MDA-exposed mothers spent significantly more time not embracing, engaging or responding to infant cuesthan maternal controls Pre-HL and Post-HL. MDA was associated with atypical maternal caregiving behavior, which inturn was related to atypical infant pain behavior self-regulation during and after the HL.Conclusion: Our findings have implication for practice. We recommend inclusion of mothers with MDA and theirinfants in interventions that strengthen the early mother-infant interaction and mother’s regulatory caregiving role.MDA and maternal caregiving behavior must be considered in future infant pain studies to examine if they confoundeffectiveness of mother driven caregiving interventions for neonatal pain. We highlight the importance of examiningmaternal mental health throughout the perinatal and postnatal trajectory, and particularly the newborn period.(Continued on next page)* Correspondence: fay.warnock@nursing.ubc.ca1Developmental Neurosciences, Child and Family Research Institute, L408,4480 Oak Street, Vancouver, BC, Canada2University of British Columbia (BC), School of Nursing, Vancouver, BC,CanadaFull list of author information is available at the end of the article© 2016 The Author(s). Open Access This article is distributed under the terms of the Creative Commons Attribution 4.0International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, andreproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link tothe Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver(http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated.Warnock et al. BMC Pregnancy and Childbirth  (2016) 16:264 DOI 10.1186/s12884-016-1050-5(Continued from previous page)Keywords: Prenatal depression, Prenatal anxiety, Maternal caregiving behavior, Infant pain, Infant pain behavior,Perinatal maternal mental health, EthologyAbbreviations: MDA, Second-trimester prenatal maternal exposure to depression and/ or anxiety; HL, Infant heel lancepain procedure; Prop-T, The proportion of time that an individual or group spends in a particular behavior during anobservation session(s); NAS, Neonatal abstinence syndrome; SSRIs, Selective Serotonin Re-uptake Inhibitorantidepressant medication; HPA, Hypothalamic–pituitary-adrenal axisBackgroundSensitive and responsive caregiving actions and interac-tions (typically provided by the mother) play a crucial rolein protecting, buffering and strengthening infant ability toself-regulate to everyday stressors [1]. This is important be-cause, throughout the perinatal period, the self-regulatorycapacities of the human infant continue to develop withrapid changes also occurring in brain structure andfunction. It is also during the neonatal period whenmost infants are exposed to painful clinical proceduressuch as heel lance (HL) for necessary blood screeningand monitoring. Established evidence suggests that earlyexposure to everyday stressors including routine HL canovertax and disrupt the still immature newborn’s ability toself-regulate subsystems (autonomic, motor, state, atten-tion, behavioral organization) [2], and confer damage tothe structure and function of the developing pain system[3, 4]. This is particularly so if the infant is born at-risk(born with prenatal exposures, ill, developmentallycompromised and/ or premature), and if the pain goesuntreated [3, 4].Currently, there are no analgesics that can be safely ad-ministered to infants to relieve procedural pain [5]. Thereis, however, substantial evidence that non-pharmacologicalpain treatments can effectively alleviate procedural pain innewborns based on a reduction in mean measures of painbehavior (primarily changes in facial movement), heart rate,and/or salivary cortisol levels [6, 7]. Examples include theuse of oral sucrose as well as mother driven caregivinginterventions (eg., kangaroo mother care, breastfeeding,facilitated tucking) [6, 7].Growth in the number of maternal caregiving interven-tions for neonatal pain and their uptake into the clinicalsetting provides confidence in their reported effectiveness[6]. While in most of these interventions, the infant’smother is acknowledged to play a fundamental role inregulating the infant and that the mother drives/functionsas the “intervention”, there is limited reporting of thematernal sample beyond demographics (eg., age, socio-economic status). Under-reporting precludes understand-ing as to whether the interventions are representative ofthe diverse population of mothers and infants for whichthey are intended. Furthermore, lack in examining maternalfactors prevents early recognition/detection of perinatalfactors and mechanisms that could hamper a mother’sability to regulate her infant, or that may function to con-found effectiveness of the interventions. Findings of a re-cent narrative systematic review of 12 kangaroo maternalcare intervention studies for neonatal pain [8], for ex-ample, show that none of the 12 studies provided informa-tion as to whether mothers with prenatal depressionand/or anxiety were included in the sample. As well,none explicitly examined prenatal maternal depressionand/or anxiety or maternal caregiving behavior as distinctstudy variables [8]. The consideration of these kinds ofmaternal factors in neonatal pain studies including motherdriven interventions for neonatal pain is essential for thefollowing reasons.Depression and/or anxiety during pregnancy are consid-ered some of the most serious and concerning issues con-fronting pregnant women and perinatal health practitioners[9]. Both often co-exist and confer increased risk foradverse maternal, pregnancy and infant outcomes [10].Historically, the emphasis on prenatal assessment/screening, epidemiology, and research has focused ondepression [10]. For example, prenatal depression has beenshown to increase the risk for preterm birth, low birthweight, and intrauterine growth restriction [9, 11]. Recentfindings, however, indicate that prenatal anxiety and stressare also associated with adverse maternal and infant out-comes and that anxiety related to the current pregnancy(pregnancy anxiety) may be especially potent [9]. Althoughexact mechanisms underlying pregnancy anxiety remainunclear, it is thought that potent infant effects may be dueto complex interactions between maternal vulnerabilitiesthat predate the pregnancy (eg., insecure attachment, lackof psychosocial resources) and anxieties a mother mayhave concerning certain aspects of the pregnancy [9].These interactions are thought to increase levels of ma-ternal anxiety that, in turn, influence the maternal-fetal-placental stress and hormonal systems in a mannerthat may contribute to functional changes in fetalhypothalamic–pituitary-adrenal (HPA) axis and to in-creased risk for adverse fetal neurodevelopment andpremature birth [9].Systematic review studies estimate that major depres-sion, during pregnancy, affects up to 12.7 % of pregnantwomen [12] and that the prevalence rates (95 % CI) ofWarnock et al. BMC Pregnancy and Childbirth  (2016) 16:264 Page 2 of 12depression for the 1st, 2nd, and 3rd trimesters of preg-nancy are 7.4 % (2.2, 12.6), 12.8 % (10.7, 14.8), and 12.0 %(7.4, 16.7), respectively [13]. The preceding findings con-tribute to increased understanding of the prevalence ofdepression and anxiety during the trimesters of pregnancy.More recently, interest has shifted to also examining howthe course of depression and anxiety throughout and ateach trimester may adversely impact maternal, fetal andinfant outcomes. Findings of a recent systematic review,for example, suggest that depression occurring during midto late pregnancy may have the greatest adverse effects onfetal growth and development, while anxiety associatedwith preterm birth may contribute to changes in fetalHPA axis [14].Studies that have linked maternal psychopathology withmaternal caregiving have mostly involved mothers withpostnatal depression. Findings show that some of thesemothers exhibit a range of inconsistent or atypical care-giving behaviors such as being less or overly responsiveto their infant cues, intrusive, or they withdraw frominteracting with their infants [15]. Currently, it has beensuggested that maternal caregiving behavior (eg., sensitivity)is a likely mechanism that links prenatal maternal de-pression [16] and /or anxiety [17] to infant and childbio-behavioral outcomes (e.g., difficult emotion regula-tion, altered cortisol patterns).The previous findings highlight the concerning impli-cations of 2nd-trimester exposure to maternal depres-sion and/or anxiety (hereafter referred to as MDA) onmaternal and infant outcomes as well as pointing to thepotential mediating effect of maternal caregiving behav-ior. As it pertains to maternal caregiving interventionsfor neonatal pain, improved reporting and targetedrecruitment of mothers with MDA and their infantsinto the study will help ensure the interventions arerepresentative. However, more research is needed toclarify the significance of MDA during the neonatalperiod and if it underlies atypical maternal caregivingbehavior as well as neonatal pain outcomes duringroutine pain procedures.To our knowledge, there have only been two independentstudies that have examined some of the linkages betweenMDA, and/or postnatal maternal caregiving behavior and/or newborn pain outcomes in full-term infants [18, 19].Both were conducted by some of the authors of the currentstudy (FW, KC, and RB). The first study [18] compared theproportion of time that mothers in three study groups [twogroups of mothers with MDA (medicated with SelectiveSerotonin Re-uptake Inhibitor antidepressants (SSRIs) andnot), and a control group] spent exhibiting atypical caregiv-ing behavior as they held their infants while the infant hada routine HL. The findings showed that during the HL,both groups of mothers with MDA were more likely tobe less responsive to their infant’s pain cry and to engagetheir infant less, compared to maternal controls. Thesecond study [19] quantified the temporal profile of thebehavioral responses of infants with and without 2nd-trimester MDA exposure during the sub-phases of theactual HL procedure (HL, post-HL). In that study, theHL was performed with the infant laying on a cot. Find-ings showed no group differences in the magnitude ofinitial behavioral reactions to the actual HL, but duringthe post-HL sub-phase, MDA-exposed infants spentmore time crying in a weak/exhausted manner and inexhibiting strained and erratic limb movement and im-mobility. The findings indicated that infant prenatal ex-posure to MDA might have contributed to delayedrecovery and diminished capacities for self-regulationof noxious distress in those infants.Taken together, findings from the two studies [18, 19]indicate that MDA may underlie the observed atypicalexpression of maternal caregiving behavior and infantpain behavior. They further suggest that MDA and mater-nal caregiving behavior are significant factors to considerin neonatal pain studies and maternal caregiving interven-tions for neonatal pain. However, the first study [18] waslimited in that findings were based on the brief event ofinfant HL (eg., 2 min). Hence, it is unclear whethermothers with MDA would exhibit similar patterns of be-havior for longer periods of the HL session. The secondstudy [19] examined linkages between MDA and infantpain behavior self-regulation, but not maternal caregivingbehavior. To further clarify the significance and potentialunderlying impacts of MDA, it is necessary to examinethe relationships of MDA to maternal caregiving behaviorand infant behavior self-regulation concurrently and toexamine maternal caregiving behavior over longer dura-tions during HL.This study addresses gaps and builds on findings ofthe two preceding studies [18, 19]. The study is part of alarge project on MDA and its potential underlying effectson the caregiving behavior of mothers and newborn painbehavior self-regulation from which findings of infant painself-regulation behavior reported by Warnock et al. [19]originate.The first aim was to examine association and groupdifferences in caregiving behavior between mothers withand without MDA before and following infant HL. Todo this behavioral data were generated from the pre-recorded videotapes of the caregiving behavior of 24mothers that had been collected but never coded or an-alyzed in the Warnock et al. [19] study. On the basis offindings of the first study [18], we hypothesized thatMDA (as measured by maternal mental health scorestaken at 2nd trimester) would be associated with maternalatypical caregiving behavior during a 5 min observationsession before the infant was placed in a cot to have theHL (Pre-HL phase), and during a 5 min observationWarnock et al. BMC Pregnancy and Childbirth  (2016) 16:264 Page 3 of 12session after the infant had the HL and was reunited withtheir mother (Post-HL phase). We also hypothesized thatduring each of these two study phases, that the proportionof time that mothers spend exhibiting atypical behaviorwould differ between MDA-exposed mothers and mater-nal controls.The second aim was to examine associations betweenmaternal MDA-exposure, time-based measures of mater-nal caregiving behavior and the three atypical patterns ofinfant pain behavior self-regulation previously reported(crying in a weak/exhausted manner, strained and erraticlimb movement and immobility) [19], concurrently. Datawere time-based measures of maternal caregiving behaviorgenerated from the 24 maternal pre-recorded videotapesas well as time-based measures of the three atypical pat-terns of infant pain behavior self-regulation. The infantmeasures were drawn from the pool of pre-calculatedtime-based measures of the 21 infants who had partici-pated in the Warnock et al. [19] study. From the totalsamples of 24 mothers and 21 babies, there was a matchedsubsample of 16 maternal-infant dyads with completetime-based behavioral data to undertake the second studyaim. Extending prior research [18, 19], we hypothesizedthat in this matched subsample of 21 mothers and theirinfants, maternal atypical caregiving behavior duringthe 5 min Pre-HL phase would be associated with thethree atypical patterns of infant pain behavior self-regulation during the sub-phases of the actual infantHL (HL, post-HL).MethodsStudy designThis was an ethological micro-analytic descriptive com-parative study that made use of systematic observationmethods and time-based analytic approaches. We chosethese methods and approaches because unlike conven-tional approaches, they are capable of generating precisemeasures of the proportion of time (Prop-T) that an in-dividual or group spends in a particular behavior duringan observation session(s), and that can be compared[20]. Furthermore, they have a unique ability in distin-guishing patterning in behavior from the co-occurringrunning streams of behavior as the normally unfold, andin explicating biological mechanisms, such as MDA, thatmay underlie observed behavior [20].Main outcomes of the current study were Prop-T timescores of maternal caregiving behavior and infant painbehavior self-regulation for the 5 min Pre-HL, 2 min in-fant HL (including post-HL sub-phase), and 5 min Post-HL study phases. Prop-T scores were calculated by div-iding the full duration of time a mother or infant spentin a particular behavior by the entire duration of the re-spective study phase. MDA was operationally defined asmild to severe symptoms of prenatal depression and/oranxiety based on mean scores of prenatal mental healthmeasures that mothers completed at the 2nd trimester.Descriptions of maternal recruitment and data collectionprocedures that we provide below are summarized fromWarnock et al. [19]. This is because mothers of thecurrent study were mothers of some of the infants fromthe Warnock et al. [19] study and because measures ofMDA were collected from mothers prenatally. A furtherreason is that measures of maternal caregiving and in-fant pain behavior self-regulation were collected at thesame time.ParticipantsAs reported by Warnock et al. [19], mothers were re-cruited during the 2nd trimester of pregnancy (first visit)and then again on the day of their infant’s scheduled HL,which occurred about 36 h after infant birth (secondvisit). The 2nd trimester was chosen because of the in-creased prevalence and impacts of depression and anx-iety compared to the 1st and 3rd trimesters, as notedearlier. Four mothers with MDA, who volunteered theirparticipation were referred to the study by their primarycare physicians who had diagnosed them as depressedand/or anxious. The remaining mothers were those whoresponded to advertisements of the study posted in healthclinics, prenatal classes or newspapers. To be included,women had to be proficient in the English language, haveno birth complications, no bipolar disorder or Axis II dis-orders, and their infants had to be >37 weeks gestationalage with a birth weight of > 2500 g. Excluded were infantswith congenital heart disease, central nervous system mal-formations and neonatal abstinence syndrome (NAS). Ofthe 36 mothers who initially volunteered, all met studyinclusion criteria and all completed a mental health as-sessment at 2nd trimester of pregnancy. There were nomissing data on any of the mental health measures thatmothers completed.Twelve of the 36 mothers were not included in thecurrent analysis because of loss to follow-up duringpregnancy (n = 1) or because of insufficient data on ma-ternal caregiving behavior (n = 11). Of the remaining 24mothers, six had reported taking drugs during pregnancy(SSRIs (n = 3), crack cocaine (n = 2) or SSRI + crack co-caine (n = 1). Those six mothers were not excluded fromthe current analysis in recognition that in our region,5 % of pregnant women are prescribed SSRIs antidepres-sant medications [21] and 3.5 % report taking crack co-caine during pregnancy [22]. A further reason was thatnone of the infants had NAS based on pre-study screen-ing by a neonatologist. However, because little has beenpublished on the effects of prenatal drug use on maternalcaregiving behavior during neonatal pain, “prenatal mater-nal drug use” (SSRIs and/ or crack cocaine) was enteredas a covariate in the analysis as appropriate.Warnock et al. BMC Pregnancy and Childbirth  (2016) 16:264 Page 4 of 12The final sample, therefore, consisted of 24 mothers.On the basis of a-priori sample size calculations of theprevious study that involved infants of study mothers[19] (for Type 1 error rate of 0.05, a power of .80 and ef-fect size of .30, ((G-Power 3.1)), a total sample of 24mothers was needed to examine change and group differ-ences in Prop-T scores of maternal behavior before andfollowing infant HL. Based on Stevens [23], the samplesize for each of the simple regressions involving one pre-dictor variable required 15 subjects. The larger study fromwhich this study and the Warnock et al. [19] study ori-ginate, received ethical approved from the University ofBritish Columbia Research Ethics Board and by the Chil-dren’s and Women’s Health Centre Research ReviewCommittee. All mothers gave written informed consentfor both themselves and their infants.ProceduresPrenatal maternal mental health assessmentAs reported by Warnock et al. [19], the prenatal assess-ment that the 24 study mothers completed at 2nd trimes-ter and that took place during the first visit, included thewell validated 10 item patient-rated Edinburgh PostnatalDepression Scale (EPDS), the well validated clinician-rated21-item Hamilton Depression Scale (HAM-D) and the14-item Hamilton Anxiety Scale (HAM-A). The threetools were administered to the mothers by a researchassistant who was knowledgeable and trained in the tools,but not blinded to study aims. Mothers were assigned tothe MDA-exposed group or the non-MDA-exposed group(control) on the basis of meeting predetermined cut-offscores on one or more of the mental health measuresand that were capable of detecting symptoms of depres-sion and/or anxiety or not. The cut-off scores were:HAM-D > 8 [24, 25], HAM-A > 8 [26], EPDS > 11 [27]. Allthree tools including same cut-off scores have been usedin prior neonatal pain studies that involved mothers withMDA (medicated with SSRIs and not) [18, 19, 28–30].Data collection: maternal and infant behaviorAs per Warnock et al. [19], mothers and infants wereassessed during the second visit in a quiet and heat reg-ulated room in the hospital. Mothers were debriefedabout the study procedures and advised that they couldwithdraw their participation at any time, or for any rea-son and to care for their infants as they normallywould. Research staff did not interfere with the carethat a mother chose to provide her infant during theHL procedure or with the routine hospital protocol forneonatal HL, which was performed with the infant lay-ing on a cot. All HLs were performed by experiencedlab technicians on infants who were awake and who didnot have any HL in past 12 h. Also, data were based ona single HL.Data collection commenced with mothers seated andholding their infants on their laps. One camera was posi-tioned to capture full body views of the mother and theinfant and to videotape continuously the behavioral re-sponses a mother made to her infant for 5 min beforethe infant’s HL (Pre-HL). Upon arrival of the lab techni-cian, the infant who was clothed in a vest and diaperwas gently placed supine onto a cot by the infant’smother or by the research assistant if the mother re-quested. A second camera captured body movements ofthe infant continuously for the duration of HL with cryingsimultaneously audio-recorded. All mothers remained inthe room, and none chose to touch their infant. After theHL, the infant was reunited with their mother, and mater-nal behavioral responses to the infant were videotapedcontinuously for 5 min (Post-HL). The research assistantdepressed a foot peddle to mark the beginning and end ofeach study phase and a running time was encoded on thestudy videotapes to enable second-by-second coding ofmaternal and infant behavior.Maternal behavioral measures and coding proceduresIn the current study, the pre-recorded videotaped cases ofthe 24 study mothers were each coded using the reliablyestablished Maternal Behavior Coding System (MBCS)[18]. The MBCS is an ethologically based micro-analyticbehavioral research coding tool that had been previouslydeveloped inductively for use with mothers with andwithout MDA during an infant pain event [18]. In across-validated sample, the MBCS distinguished typicalfrom atypical caregiving behavior between two groupsof mothers with MDA (medicated and not) and a controlgroup of mothers [18]. The tool consists of main categor-ies and subcategories of maternal caregiving behavior thatare structured into two main domains typical caregivingbehavior and atypical caregiving behavior. We chose theMBCS because it enables trained coders to continuouslycode behavioral items second-by-second as the coders ob-serve them to occur on pre-recorded videotapes fromwhich precise Prop-T scores of behavior can be generatedand compared (see Warnock et al. [18] for a copy of theMBCS for that study).In this study, we drew on the coding procedures fromthe Warnock et al. [18] study to continuously code MBCSitems from the 24 pre-recorded videotaped maternalcases. Two coders who were knowledge of the MBCS,trained in systematic coding, and who were blinded tomaternal group and to study phase, coded the videotapesin random order, in terms of participants, using theMBCS. Starting with the first videotaped case and the first60 s of the 5 min Pre-HL study phase, the coders exam-ined each 1-s interval and coded the occurrence and dur-ation of each maternal behavior described in the MBCS.Only when each of five 60 s time blocks was coded inWarnock et al. BMC Pregnancy and Childbirth  (2016) 16:264 Page 5 of 12succession for the Pre-HL session did the coders move tocode the five 60 s time blocks of the Post-HL session. Thesame systematic steps were followed to code the two5 min sessions for the remaining 23 maternal videotapes.Excluded from the analysis were behaviors that were notvisible to coders for 20 s or more during any one 60 s timeblock (eg., due to the ill positioning of the video camera orwhen research staff walked in front of the camera) [20].All of the 24 maternal videotapes used in the current ana-lysis had complete data.Of the 14,400 one-second intervals (~240 min) ofcoded maternal behavior (600 s for Pre-Hl + 600 s forPost-HL) (MDA group = 7000 s; control group = 7000 s)20 % were randomly selected and subjected to inter-reliability testing, achieving k = 0.80 or better. Data werethen entered into the General Sequential Querier forWindows (GSEQ 5.1). GSEQ5.1 is a unique data analysisprogram specially designed to calculate precise Prop-Tmeasures of coded behavioral items by case, or by studygroup, or by study phase [20]. Next, we made use ofGSEQ5.1 to combine Prop-T scores of coded MBCSitems that were conceptually related, and that were thengrouped into eight domains. Each domain was furtherstructured into two mutually exclusive categories - thefirst representing typical maternal caregiving behaviorand the other representing atypical behavior. Table 1provides a summary of the eight MBCS main categoriesthat were identified from this dataset, includingdefinitions. Prop-T scores representing maternal atypicalcaregiving behavior and typical behavior for each mater-nal study case were then transferred to SPSS 21 to ad-dress study aims.Infant behavioral measures and coding proceduresThe systematic procedures that Warnock et al. [19] usedto continuously code each of the 21 infant pre-recordedvideotapes were the same as those described above forcoding the 24 maternal pre-recorded videotapes. As re-ported by Warnock et al. [19], the reliably establishedand cross-validated Neonatal Distress Pain Related Be-havioral Coding Schema (ND-BSC) was used to code theinfant videotapes by four coders who were trained in theND-BSC and who were blinded to infant group. How-ever, coders were not blinded to study phase because thelaboratory technician’s hand, used to conduct the HL,was visible to the coder. The ND-BCS is an ethologicallybased behavioral coding schema that consists of itemsfor coding continuously and concurrently infant motormovement, posture, respiration responsiveness and crybehavior. The procedures used to test for inter-reliabilitybetween coders, and to reduce and further analyze datain GSEQ 5.1 were also the same as those describedabove for coding the maternal videotaped cases. Inter-reliability between coders achieved k = 0.80 or better[19]. Sequential and comparative analysis of Prop-Tscores of ND-BCS coded items led to identifying theTable 1 Eight MBCS behaviors with definitionsDefinition/DescriptionCoding Items Typical maternal caregiving behavior Atypical maternal caregiving behaviorEye Gaze Looking or seeking eye contact: Mother lookingstraight at baby’s face, or mother seeking eyecontact with baby.Looking away: Mother looking away from baby.Engages baby and responsive tobaby cues/actions.Interactive, engages baby: Mother makes frequentattempts to interact/engage infant. Mother directlyor indirectly responds to infant cues (baby crying,looking at or touching mother),Minimal or no responsiveness to infant cues.Mother makes minimal, or no attempt tointeract or to engage with the infant. Mothernot responsive - may appear detached.Embracing (positioning) of the baby Mother embracing baby: Close, protective. Baby’sbody is enclosed in mom’s embraceNo embracing or cradling. Baby laying in unsafeposition. Mother does not appear to notice babymay fall off her lap.Direction of mother’s attention Attention directed to baby: Mother focuses attentionon baby,Attention not directed to baby. Mother seemsself-absorbed, her attention is not directed tobaby, to others, or to her environment.Type and quality of facial expressions Regular: Mother facial expression regular, smiling. Not regular: Grimacing, crying quietly, cryingexcessively. Quality of facial expression is flat ormother appears disconnected or “checked out”Comfort Comfortable: Mother appears comfortable or she saysshe is comfortable.Not comfortable: Mother appears uncomfortable(eg., mother sighs, rolls eyes) or says she isuncomfortable.General affect Unbothered: Mother’s generally appears unbotheredsad, or worried.Bothered: Mother appears bothered, worried, sad, upsetor very upset (distraught).Anxiety No such display: Mother does not appear anxious Anxious: Mother bites nails, touches hair,repetitive nervous knee movement.MBCS definitions from Ethogram of Maternal Behavior Coding System [18]Warnock et al. BMC Pregnancy and Childbirth  (2016) 16:264 Page 6 of 12three temporal patterns of newborn pain behavior self-regulation that were suggestive of delay in pain recovery(crying in a weak/exhausted manner, strained/erraticlimb movement and immobility).Data analysisSimple descriptive statistics were obtained for all studyvariables and distributions of continuous variables wereinspected for normality. For the total sample of 24mothers, Mann-Whitney and Wilcoxon Signed Rank testfor non-normally distributed data were used to test thehypothesis that the proportion of time that studymothers spend exhibiting atypical behavior during the5 min Pre-HL and the 5 min Post-HL study phaseswould differ between MDA-exposed mothers and mater-nal controls. For the later, Prop-T scores of maternal be-havior were analyzed when six or more mothers ineither group exhibited MBCS behaviors during Pre-HLor Post-HL. Separate simple linear regressions using ad-justed R2 were performed on the total sample of 24mothers to test whether prenatal MDA (HAM-A,HAM-D and EPDS mean scores) would predict Prop-Tscores of maternal atypical caregiving behavior duringthe 5 min Pre-HL and 5 min Post-HL study phases. Forthe matched subsample of 16 mothers and their infants,we also performed simple regressions to examine ifProp-T scores of types of maternal atypical behavior dur-ing the Pre-HL phase would predict Prop-T scores of thethree atypical patterns of pain behavior self-regulation ininfants previously reported [19] during the HL and post-HL sub-phases of infant HL. Finally, partial correlationswere used to examine the potential contribution of pre-natal maternal drug use (SSRI/SU) on study outcomes asappropriate. All analyses were two-tailed with alpha setat p < .05, as appropriate.ResultsPrenatal mental health measures and maternal and infantcharacteristicsOf the 24 mothers, 12 had scores that exceeded thepredefined cut-off for the HAM-A (range, 8–29), or theHAM-D (range, 8–29) or the EPDS (range, 11–27).These 12 mothers were allocated to the MDA-exposedgroup, and the 12 mothers whose scores fell below thecut-offs were allocated to the non-MDA-exposed group(maternal controls). MDA-exposed mothers had signifi-cantly higher HAM-A, HAM-D and EPDS scores than didthe non MDA-exposed group of mothers (U = 14, p < .001,r = .75; U = 12, p < .001, r = .77; U = 11, p < .001, r = .78, re-spectively). Of interest, we found that ten of 12 mothers al-located to the MDA-exposed group had comorbid anxietyand depression based on exceeding cut-off scores on twoor more of the tools: HAM-A+HAM-D (n = 5) andHAM-A+HAM-D+ EPDS (n = 5). In the subsample of 16mothers, eight had scores that exceeded the predefinedcut-offs, and eight had scores that fell below the cut-offs.Of the eight mothers whose scores exceeded the cut-offs,six had comorbid anxiety and depression: HAM-A+HAM-D (n = 1) and HAM-A+HAM-D+ EPDS (n = 5).The 24 mothers had a mean age of 34 years (SD = 5.6)and a mean of 17.46 years of education (SD = 4.9). Mostwere married (63 %), Caucasian (67 %), and first-timemothers (63 %). The mode of delivery was vaginal (58.1 %)or by C-section (41.7 %). As reported in the Warnock et al.[19] study, infants had a mean gestational age of 39.75 weeks(SD = 1.53), birthweight of 3436 g (SD = .3859), and 62 %were male. There were no statistically significant group dif-ferences on maternal characteristics or on factors consideredas confounders to maternal caregiving behavior such assmoking, infant gender or number of children or on infantcharacteristics. The preceding findings were consistent forthe subsample of 16 mothers and infants.Association and group differences in types of caregivingbehavior between mothers with and without MDA beforeand following infant HLInitial analysis involving the 24 mothers, showed moderatepositive correlation between prenatal maternal anx-iety (HAM-A) and depression (HAM-D, EPDS), andtotal Prop-T scores of maternal atypical caregiving be-havior during routine infant HL (r = .604, p = .002; r = .447,p = .03; r = .631, p < .00, respectively). Both groups ofmothers (MDA-exposed and non-MDA-exposed) exhibitedFig. 1 Group differences and change in Mean proportion of time(total Prop-T score, 95 % CI) that the 24 mothers in the two studygroups [(MDA-exposed (n = 12) and Non-MDA exposed (n = 12)]spent exhibiting atypical caregiving behavior to infant behavioralcues while with their infant for 5 min before the infant had the HL(Pre-HL) and for 5 min after the infant had the HL (Post-HL)Warnock et al. BMC Pregnancy and Childbirth  (2016) 16:264 Page 7 of 12typical caregiving behavior to their infants, during the5 min Pre-HL and 5 min Post-HL study phases. However,as Fig. 1 illustrates, during the two study phases, meanscores of atypical caregiving behavior were higher forMDA-exposed mothers compared to non-MDA exposedmothers with both groups showing little change from thePre-HL phase to the Post-HL phase. Notably, the distri-butions of scores were considerably more varied forthe MDA-exposure mothers than they were for thenon-MDA exposed mothers.The Mann-Whitney tests were conducted to examinegroup differences in Prop-T spent in varying types ofatypical behavior when six or more mothers in eithergroup (MDA-exposed (n = 12), non-MDA exposed (n = 12)exhibited MBCS behaviors during the 5 min Pre-HL or the5 min Post-H study sessions. The results revealed that dur-ing the Pre-HL phase, MDA-exposed mothers were morelikely than maternal controls to not embrace (U = 36,p < .001, r = .55), attend (U = 34, p = .028, r = .45) orengage and respond to the infant’s behavioral paincues (U = 36, p = .038, r = .42). Wilcoxon Signed RankTest showed no change in Prop-T of atypical behaviorbetween the two groups of mothers from the Pre-HLto Post-Hl study phase. However, the results showed,that although six MDA-exposed mothers spent a sig-nificant proportion of the Pre-HL phase not embra-cing, three of the six spent significantly less time innot embracing Post-HL (U = 40, p = .021, r = .51).Table 2 provides a summary of the preceding results.The table does not include results pertaining to atyp-ical expression of MBCS comfort, or general affectand anxiety because the behaviors were not exhibitedby enough mothers (six or more for the study phases).Relationships between prenatal maternal mental healthmeasures and maternal atypical caregiving behaviorbefore and after infant HLSeparate simple linear regressions involving the 24mothers were performed to determine if prenatal MDA(mean scores of HAM-D, or HAM-A or EPDS) wouldpredict Prop-T scores of maternal atypical caregiving be-havior during the Pre-HL and Post-HL study phases. Re-sults showed HAM-D scores predicted Prop-T scores ofatypical caregiving behavior during the Pre-HL (β = .46,t = 2.46, p = .022), but more so during the Post-HL phase(β = .66, t = 4.16, p = .01). HAM-A and EPDS scores alsopredicted Prop-T scores of maternal atypical caregivingbehavior, but only during Post-HL: HAM-A (β = .64, t =3.95, p < .001); EPDS (β = .64, t = 3.92, p < .001).HAM-D scores accounted for a smaller proportion ofvariance in atypical behavior during Pre-HL [adjustedR2 = .180, F (1, 22) = 6.05, p = .022] than during Post-HL[adjusted R2 = .416, F (1, 22) = 17.35, p = .01]. HAM-Aand EPDS scores also accounted for up to 38 % of the vari-ance in atypical expression Post-HL: HAM-A [adjustedR2 = .389, F (1, 22) = 15.66, p < .001], EPDS [adjusted R2 =.385, F (1, 22) = 15.39, p < .001].Relationship between maternal atypical caregiving behaviorduring Pre-HL and infant pain self-regulation behaviorduring the sub-phases of infant HL (HL and post-HL)Results of the final simple linear regressions that involvedthe matched subsample of 16 mothers and their infantsshowed the Prop-T that mothers spent in not engaging/responding or attending to infant’s behavioral cues duringthe 5 min Pre-HL phase, predicted the Prop-T that infantoffspring spent exhibiting strained/erratic limb movementsTable 2 Proportion of time (Prop-T) study mothers spent in five MBCS atypical behavior Pre-HL and Post-HLGroup Phase ZPre-HL (5 min) Post-HL (5 min)n M(SD) Mdn n M(SD) MdnLooking away from baby. Control 10 9.95 (13.89) 5.35 9 10.20 (9.49) 9.00 −314MDA-Exposed 12 22.67 (24.89) 15.50 12 18.72 (18.46) 12.80 −.235Minimal or no responsiveness to baby cues/action. minimal,or no attempt to interact or to engage with the infantControl 12 10.45 (13.70) 4.85 8 9.39 (8.86) 8.00 .000MDA-Exposed 12 28.72 (27.15) 20.50* 12 25.86 (38.86) .110* −1.34Not embracing, cradling baby. Control 0 .000 (.00) .00 0 .000 (.00) .00 .000MDA-Exposed 6 35.39 (45.11) 6.15* 3 9.14 (21.31) .00 −.2.201**Mothers attention not directed towards baby, others, orenvironmentControl 10 10.20 (13.88) 4.85 8 9.05 (8.56) 8.00 −.639MDA-Exposed 12 32.25 (33.30) 20.50* 10 20.77 (23.75) 12.65 .523Type and quality of facial expression not regular. Control 10 17.00 (28.29) 4.20 6 7.19 (14.96) .50 −1.27MDA-Exposed 9 29.28 (36.26) 20.50 9 30.52 (36.65) 19.85 −.533Values represent mean proportion of time (number of seconds behavior expressed/total number of seconds of the observation session) based on 24 mothers (12in MDA-exposed grp, 12 in Control group), n total number of mothers in each group who exhibited the behavior (minimum of 6 required in either phase). *p < .05Mann Whitney U test; **p < .05 Wilcoxon signed-rank testWarnock et al. BMC Pregnancy and Childbirth  (2016) 16:264 Page 8 of 12(β = .552, t = 2.47, p = .027) and immobility (β = .566,t = 2.57, p = .022) during the actual HL. Prop-T scores ofthese maternal behavior explained 25 % of the variance ininfant strained/erratic limb movement [adjusted R2 = .255,F (1, 14) = 6.14, p = .027] and 27 % in immobility [adjustedR2 = .272, F (1, 14) = 6.60, p = .022] during the actual HL.We also found the Prop-T the 16 mothers spent notengaging or attending during the 5 min Pre-HL phase,predicted the Prop-T their infants spent in weak/strainedcry during the post-HL sub-phase (β = .690, t = 3.56, p =.003, and β = .518, t = 2.26, p = .040, respectively). TheProp-T the mothers spent in not engaging or attendingPre-HL explained up to 21 % of the variance in infantweak/strained cry post-HL subphase: [adjusted R2 = .216,F (1, 14) = 5.132, p = .040].DiscussionThe overall goal of this basic observation study usingtime based analytic approaches was to clarify the signifi-cance of MDA and its potential underlying impact onmaternal caregiving behavior and infant pain behaviorself-regulation, in the first few days following infant birth.Acknowledging the complex and many multiple pathwaysof association possible, the precise and in-depth time-based findings generated in this study contribute robustfoundational measures of maternal and infant behaviorthat could not have been generated using conventional ap-proaches. Main findings suggest that MDA may underlieatypical maternal caregiving behavior and that maternalcaregiving behavior may mediate infant pain behaviorself-regulation.As hypothesized, MDA-exposure was associated withtype and temporal quality of atypical maternal caregivingbehavior before and after infant HL. During the Pre-HLphase, MDA-exposed mothers were more likely thanmaternal controls to not engage /respond or attend to in-fant behavioral cues Pre-HL with little change Post-HL.That three of the six MDA-exposed mothers spent lesstime in not embracing their infant Post-HL suggestchange toward more responsive caregiving behavior. Butgiven the very small number of mothers who exhibitedchange, further study is required before conclusion can bedrawn. The considerable variability in Prop-T that the 12mothers with MDA spent exhibiting atypical behaviormay be because 83 % of these mothers had cut-off scoresindicating moderate to severe comorbidity.Our findings of association between MDA and time-based measures of maternal caregiving before and afterroutine infant HL are consistent with findings of a lackof responsiveness and insensitivity behavior in motherswith postpartum depression and/ or anxiety reported instudies that did not involve infant pain [31, 32]. Theyare also consistent with time-based findings of theWarnock et al. [18] study that showed a lack ofengagement and responsiveness in mothers with MDAas they held their infants during the 2 min HL. Ourfindings extend those findings, in that our group ofMDA-exposed mothers exhibited lack of engagementand responsive to infant cues while with their infants,5 min before the 2 min HL and 5 min after the HL.Taken together, findings of the prior study [18] andthis study suggest that MDA-exposed mothers mayexpress atypical patterning in caregiving behavior overthe course of infant HL.In our study, factors that have been acknowledged toinfluence maternal atypical caregiving behavior such asthe number of children, gender of an infant or maternalsmoking did not present as confounders. However, onefactor that we did not examine and that may have con-tributed to our findings of maternal atypical caregivingbehavior is a lack of sleep or physical exhaustion inmothers, especially given that we sampled mothers withindays of giving birth. In a recent study, mothers with anEPDS score of >12 at one week postpartum were signifi-cantly more likely to report being tired [33]. In addition,maternal fatigue in that study was strongly associated withnew onset of depressive symptoms. These maternal vari-ables may have interactive or confounding effects andtherefore warrant consideration in future studies.Our second and third hypotheses that MDA exposure(as measured by 2nd trimester HAM-D, or HAM-A orEPDS scores) would predict Prop-T scores of maternalatypical caregiving behavior and that maternal atypical care-giving behavior Pre-HL would be associated with the threepatterns of atypical infant pain behavior self-regulation re-ported previously [19] were both supported. Similar to thefindings reported by Warnock et al. [18], we found that pre-natal depression and anxiety was positively associated withatypical expression of caregiving behavior. Our findingsextend the prior findings [18] in that prenatal depres-sion, and anxiety (based on independent analysis ofHAM-A, HAM-D and /or EPDS scores) accounted forup to 41 % of the variance in atypical expression ofcaregiving behavior Post-HL. Controlling for prenatalmaternal drug use (SSRIs, crack cocaine) had little im-pact on these findings. Our approach to examining therelationship of MDA to Prop-T scores of maternal care-giving contributed knowledge on the distinct contributionsMDA during the 2nd trimester based on independentanalysis of HAM-A, or HAM-D or EPDS scores. Futurestudies with large sample sizes will help determine whichof the three measures best predict atypical maternalcaregiving and the contributions of comorbidity andpregnancy anxiety at each trimester.We also found that the Prop-T that the 16 mothersin the subsample spent in not embracing and in notengaging/responding or attending to infant behavioralcues during the 5 min Pre-HL phase were associatedWarnock et al. BMC Pregnancy and Childbirth  (2016) 16:264 Page 9 of 12with the Prop-T their infants spent in immobility andin strained/erratic limb movement during actual HL,and in weak/strained cry during the post- HL sub-phase.These findings extend the findings by Warnock et al. [19]in that we included time-based measures of maternalcaregiving in the concurrent analysis. While the priorfindings [19] suggest that infant ability to self-regulate toand from painful stimuli may be impacted by prenatal ex-posure to MDA, the current findings suggest that type/quality of maternal caregiving behavior may play a medi-atory role in this dynamic. However, these results werebased on a sample of16 mothers and their infants. Assuch, the results are preliminary, but they warrant furtherstudy. If the maternal and infant findings are again ob-served in future studies, convergent findings may providethe basis for the development of early clinical interven-tions that promote the caregiving behavior and stressregulatory role of mothers with MDA. Newborn ability tobehaviorally regulate to stressors is a marker of neuro-development [2], and early indication of sustained delayin self-regulation in the full-term necessitate early as-sessment and treatment.The dearth of similar studies in the context of neonatalpain makes it difficult to compare our findings. Otherstudies that did not involve infant pain have reported link-ages between prenatal maternal depression and/or anxietyand postnatal alteration in maternal caregiving behaviorand later child outcomes. For example, findings haveshown that prenatal anxiety predicts depressive symptomsduring the postpartum [34] and that it accounts for10–15 % of adverse behavioral, emotional, cognitiveand mental health outcomes in later childhood [10, 35]such as low social competencies and adaptive functioning[36]. In contrast, other findings have shown that maternalinsensitivity, but not antenatal psychiatric diagnosis,predicts infant responsiveness in a free play situation atfour months post-partum [16]. Potential reasons for thediscrepant findings between that study and our findingsis that we examined caregiving behavior of motherswith MDA during the newborn period and because thefindings were based on the use of ethologically drivenmethods that are specifically designed to help explainbiological mechanisms underlying observed behavior.The in-depth descriptions of the types and temporalqualities of maternal caregiving behavior that were eluci-dated in this study are clinically relevant. Clinicians withinterests in mother driven interventions for neonatalpain may use the findings to consider inclusion of motherswith MDA and their infants. These mothers may repre-sent the 36 % of women who decline participation [8], andit is unclear if these dyads would benefit from the regula-tory properties of the interventions. There is, however,emerging evidence that maternal-infant skin-to-skin con-tact intervention for neonatal pain may have regulatorybenefits for both mothers and infants regardless of ma-ternal mental health status [37]. Clinical recruitmentand future research of this kind will help supportmothers with MDA and their infants and as noted, mayprovide the basis for potential modification of the inter-ventions, as appropriate.This study has limitations that necessitate cautiousinterpretation of study findings. Although this basic ob-servation study yielded foundational data based on ahuge amount of time-based measures, the small subjectsample size limits the generalizability of the findings.Some of the study mothers had taken antidepressantmedications and/or drugs (SSRIs, crack cocaine) duringpregnancy. Although we controlled for these effects sta-tistically, these mothers may exhibit a unique behav-ioral profile due to impacts of the drugs and chronicexposures to environmental adversity and stress. It wasbeyond the present study to have distinguished any be-havioral differences, and this may be an area for futurededicated research. Findings were based on independentmeasures of prenatal depression and anxiety and the studyfocused on maternal and infant behavior. Targeting co-morbidity at recruitment, making use of multivariateanalysis and obtaining physiological and other measures(eg., measures of maternal and infant cortisol levels,heart rate variability) in future larger sized samples willhelp clarify pathways of association.ConclusionsSensitive and responsive maternal caregiving behaviorstrengthens infant self-regulatory capacities, but this power-ful regulatory role may be diminished in some women withMDA. Our findings suggest that mothers and infants with2nd trimester MDA exposure exhibit atypical behavior dur-ing a routine infant pain event and that MDA may underliethese atypical patterning in behavior. The findings are con-sistent with findings of studies that have examined associa-tions between MDA, maternal caregiving behavior that didand did not involve infant pain, and that were conductedduring the postpartum. We recommend early inclusion ofmothers with MDA and their infants in interventionsaimed to strengthen the early mother-infant interactionand a mother’s caregiving regulatory role. MDA and mater-nal caregiving behavior must be considered in future infantpain studies and to examine potential confounding effectsof MDA on effectiveness of mother driven interventions forneonatal pain. We highlight the importance of future re-search on maternal mental health throughout the trajectoryof the perinatal period, particularly during the early new-born period, and on development and implementation ofearly strength-based interventions.AcknowledgementsWe would like to thank all of the mothers and infants who participatedin this study.Warnock et al. BMC Pregnancy and Childbirth  (2016) 16:264 Page 10 of 12FundingThis study was supported by the Michael Smith Foundation for HealthResearch (Scholar award to FW) and by an operating grant from CanadianInstitutes of Health Research (MOP 77769 to FW). The funding bodies did notplay any role in the design of the study or in data collection, interpretationof data or in writing of the manuscript.Availability of data and materialsAll data generated or analyzed during the current study and all data thatsupport the conclusions of this study are included within the article.Authors’ contributionsFW, RB and KC contributed to conception and study design. FW coordinatedthe study and contributed to recruitment, acquisition of study data and trainingof coders. FW and TC performed data analysis. FW, RB, KC, TC and JM allparticipated in the interpretation of study data and to the drafting and criticalrevision of the manuscript making contributions to the content. All authorsread and approved the final manuscript.Competing interestsThe authors declare that they have no competing interests.Consent for publicationNot applicable.Ethics approval and consent to participateThe larger study from which this study and the Warnock et al. [19] studyoriginate, were conducted in accordance with the Declaration of Helsinki.The study was approved by the University of British Columbia ResearchEthics Board and by the Children’s and Women’s Health Centre ResearchReview Committee. All mothers gave written informed consent for theirparticipation and the participation of their infant.Author details1Developmental Neurosciences, Child and Family Research Institute, L408,4480 Oak Street, Vancouver, BC, Canada. 2University of British Columbia (BC),School of Nursing, Vancouver, BC, Canada. 3Department of Psychology,University of British Columbia (BC), Vancouver, BC, Canada. 4Georgia StateUniversity, Atlanta, Georgia 30303, USA. 5University of Goiás Faculty ofNursing, Goiânia, GO, Brazil. 6School of Nursing and Midwifery, TehranUniversity of Medical Sciences, Tehran, Iran.Received: 6 October 2015 Accepted: 25 August 2016References1. Gunnar MR, Quevedo KM. 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Luoma I, Tamminen T, Kaukonen P, Laippala P, Puura K, Salmelin R, Almqvist F.Longitudinal study of maternal depressive symptoms and child well-being.J Am Acad Child Adolesc Psychiatry. 2001;40(12):1367–74.37. Castral T, Warnock F, Dos Santos C, Daré M, Moreira A, Antonini S, Scochi C.Maternal mood and concordant maternal and infant salivary cortisol duringheel lance while in kangaroo care. Eur J Pain. 2015;19(3):429–38.•  We accept pre-submission inquiries •  Our selector tool helps you to find the most relevant journal•  We provide round the clock customer support •  Convenient online submission•  Thorough peer review•  Inclusion in PubMed and all major indexing services •  Maximum visibility for your researchSubmit your manuscript atwww.biomedcentral.com/submitSubmit your next manuscript to BioMed Central and we will help you at every step:Warnock et al. BMC Pregnancy and Childbirth  (2016) 16:264 Page 12 of 12


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