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Harnessing microbiome and probiotic research in sub-Saharan Africa: recommendations from an African workshop Reid, Gregor; Nduti, Nicholas; Sybesma, Wilbert; Kort, Remco; Kollmann, Tobias R; Adam, Rod; Boga, Hamadi; Brown, Eric M; Einerhand, Alexandra; El-Nezami, Hani; Gloor, Gregory B; Kavere, Irene I; Lindahl, Johanna; Manges, Amee; Mamo, Wondu; Martin, Rocio; McMillan, Amy; Obiero, Jael; Ochieng’, Pamela A; Onyango, Arnold; Rulisa, Stephen; Salminen, Eeva; Salminen, Seppo; Sije, Antony; Swann, Jonathan R; van Treuren, William; Waweru, Daniel; Kemp, Steve J Apr 16, 2014

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MEETING REPORT Open AccessHarnessing microbiome and probiotic research insub-Saharan Africa: recommendations from anAfrican workshopGregor Reid1*, Nicholas Nduti2, Wilbert Sybesma3, Remco Kort3,4, Tobias R Kollmann5, Rod Adam6, Hamadi Boga7,Eric M Brown8, Alexandra Einerhand9, Hani El-Nezami10, Gregory B Gloor11, Irene I Kavere12, Johanna Lindahl13,Amee Manges14, Wondu Mamo15, Rocio Martin9, Amy McMillan1, Jael Obiero16, Pamela A Ochieng’12,Arnold Onyango12, Stephen Rulisa17, Eeva Salminen18, Seppo Salminen19, Antony Sije12, Jonathan R Swann20,William van Treuren21, Daniel Waweru12 and Steve J Kemp22AbstractTo augment capacity-building for microbiome and probiotic research in Africa, a workshop was held in Nairobi,Kenya, at which researchers discussed human, animal, insect, and agricultural microbiome and probiotics/prebioticstopics. Five recommendations were made to promote future basic and translational research that benefits Africans.IntroductionThe rapid expansion of microbiome [1-5] and probiotic[6-9] research over the past 10 years and the many spin-offs providing novel insights into human and animal dis-eases, as well as products designed to alleviate them, havebeen primarily driven by sizeable funding from developedcountries, especially Canada, USA and Europe.The first study conducted in Africa was based upon 16SrRNA gene sequencing, utilizing Illumina (San Diego, CA),and revealed a microbiome of relatively high diversity inthe vagina of Tanzanian women infected with HIV [10].This was followed by an intriguing study of children froma rural village in Burkina Faso, whose high-fiber diet issimilar to that eaten in early human settlements at the timeof the birth of agriculture [11]; compared to European chil-dren, the latter study found a significant enrichment inBacteroidetes and depletion in Firmicutes (P < 0.001), witha unique abundance of bacteria from the genus Prevotellaand Xylanibacter, enriched in bacterial genes for celluloseand xylan hydrolysis. Such continental-comparative studiescan be revealing in terms of understanding how the envir-onment and diet influence health, disease and weight gain,especially since it is known that modern diet and lifestylecan cause a dramatic change to the human gut microbiome[12]. Ironically, urban regions of Africa are transitioning to-wards a lifestyle and fast-food diet typical of ‘Westernized’societies, potentially bringing with it an increased risk ofmetabolic diseases, such as diabetes. It will be interestingto see if the gut microbiome, shown to have a higherabundance of Bifidobacterium and a different Bacteroides-Prevotella ratio at 6 months of age in resource disadvan-taged Malawi compared to higher-income Finland, convertsto one similar to Finland or the US [13]. Only minor differ-ences were observed between the microbiota of subjects inFinland and Germany, emphasizing the African deviation[14]. This could have major implications as the microbiotaaffect energy extraction from food, possibly resulting inobesity. On the other hand, a particular nutritious dietmight enhance beneficial microbiota to help lower the riskof diarrheal diseases and improve child health.This improved knowledge of the microbial compositionprovides a new focus to examine the consequences ofintervention studies. The importance of this is illustratedby a Swiss-led study in Ivory Coast which showed that notonly was iron fortification through biscuits ineffective foriron-deficiency anemia, but it worsened the unfavorableratio of fecal Enterobacteriaceae to Bifidobacteriumand Lactobacillus [15]. Other microbiome and com-parative microbial genome studies have contributed to* Correspondence: gregor@uwo.ca1Lawson Health Research Institute and Departments of Microbiology &Immunology, and Surgery, University of Western Ontario, 268 GrosvenorStreet, London, Ontario N6A 4V2, CanadaFull list of author information is available at the end of the article© 2014 Reid et al.; licensee BioMed Central Ltd. This is an Open Access article distributed under the terms of the CreativeCommons Attribution License (, which permits unrestricted use, distribution, andreproduction in any medium, provided the original work is properly credited. The Creative Commons Public DomainDedication waiver ( applies to the data made available in this article,unless otherwise stated.Reid et al. Microbiome 2014, 2:12 understanding of adaptation mechanism of organ-isms in the environment [16] and how these mighthave been impacted by various niches [17,18]. Of par-ticular interest is the gut microbiome of the malariamosquito [19], perhaps as a first step in manipulatingit to lower infectivity of the parasite. Fermented foodshave a long history of use in Africa, and in recentyears efforts have been made to identify the microbialstrains and propagate them as probiotics to conferadditional health benefits [20-23]. Some studies haveshown the benefits of probiotics in the gut and vaginaof HIV-infected patients in Africa [24,25], while in onereport a combination of probiotic and prebiotic failed toresolve acute severe malnutrition in children from Malawi[26]. Knowledge gaps remain to be investigated withrespect to African subjects. For example, studies whichassess the male urinary tract microbiota have beenconducted in Europe [27], but in Africa studies haveexamined the effect of circumcision on the corona sulcusmicrobiota. As the interchange of male and female micro-biota may have important consequences for health, coord-inating such studies amongst different populations wouldbe worthwhile.In agreement with the sentiments brought forth byvan Helden and colleagues [28] that humans, animalsand the environment are inextricably linked and equalattention is needed to ensure optimal health for all, weconvened a workshop in Nairobi, Kenya, at the Inter-national Livestock Research Institute (ILRA). The overallgoal was to develop evidence-based concepts aimed atimproving the health and wealth of people in Africancountries, with emphasis on mother and child, and localproduction and increased accessibility to nutritious andaffordable products, integrated with effective educationand training at community and academic levels. Threespecific objectives of the workshop were: (1) discusshuman, animal, insect, and agricultural microbiome aswell as probiotics/prebiotics research in, or planned for,Africa; (2) engage African scientists and clinicians as wellas help facilitate training focused on basic and transla-tional research in the areas of microbiome investigationsthat promote sustainable, locally derived disease inter-ventions; and (3) create new research initiatives and makerecommendations to enhance African infrastructure, ex-pertise and impact on these globally important areas.The outcomes and conclusions of the meeting arepresented here.A cross section of researchers from across the world,with a track record in studying the microbiome and/orprobiotics in Africa were invited. The meeting waslimited to 40 participants for logistical reasons and toencourage discussion groups to form and come up withtangible concepts. With no funding to support travel ofdelegates, the reliance was upon goodwill and interest inthe topic. Over 70 invitations were made to researchersbased upon their publications in these areas, of which 40accepted but eight cancelled too late for substitution,leaving a total of 32 participants from 10 countries. Onday one, participants identified their interests and wherethey would like progress to be made. Topics for discus-sion were then agreed upon and day two was spent ingroups to identify ways to move the topic forward.There was collective agreement that practical transla-tional efforts should be prioritized that embrace local in-volvement and focus on sustainable outcomes. Cognizantof the realities of funding and the need to develop moreAfrican expertise and infrastructure, there was a com-mitment from all parties to collaborate and make theproposed projects actually happen. Figure 1 provides asummary of the essential components which the partici-pants felt were needed for success, with education, train-ing and research being absolutely essential. The followingis a summary of the ideas, projects and recommendationsfrom these discussions. We welcome interest and contri-butions by members of the larger scientific communitywho read this article.The extended microbiome of African indigenous cattleCattle represent an integral part of society in manyAfrican countries as a source of meat and milk. Diseasesof cattle have major implications for food security aswell as community livelihoods and the economy. Inaddition, exposure of cattle to toxins, such as aflatoxinsin maize or heavy metals in the soil, then become prob-lematic for the consumer of their milk and meat, includ-ing offals. The cattle population is diversified with manybreeds, but one important East African breed is theBoran which is both hardy and productive. Hypothesiz-ing that the microbiome has an important role to play inproductivity and health of cattle, five objectives weredeemed important to better understand the microbiomecomposition.(i) Identify the normal microbiome (bacteria, archaeaand fungi) of Boran cattle, their surface parasitesas well as their feed and environment in threeeco-climatic zones within Kenya. This wouldprovide insight into seasonal effects, grazingconditions and help identify microbes associated withhealth. All sequencing will be performed at ILRI andadded to the metadata of the Earth MicrobiomeProject ( Thiswill also build capacity by training graduatestudents at various East and Central Africanuniversities.(ii) Characterize the functional capabilities of microbialpopulations in the planktonic and mucosal surfaceof the rumen of Boran cattle. This will determineReid et al. Microbiome 2014, 2:12 Page 2 of 13 the organisms are functioning, theirby-products and impact on host immunity.(iii) Determine the difference in microbial functionwhen feed is contaminated with aflatoxins. TheFood and Agriculture Organization estimates that25% of the world’s food crops are affected bymycotoxins, with losses to livestock and poultryproducers from aflatoxin-contaminated feedsresulting in death and effects on immune systemsuppression, reduced growth rates, and losses infeed efficiency. Aflatoxins are secondary metabolitesproduced by species of Aspergillus, specificallyAspergillus flavus and parasiticus fungi, whichgrow well on maize, peanuts and other foodsunder relative humidity/moisture and poor storageconditions. These compounds are highly toxic,mutagenic, teratogenic and carcinogenic, causinghuman hepatic and extrahepatic cancers. Regions ofKenya are known to be at high risk of aflatoxincontamination and this could adversely affect yieldand increase risk for humans who consume themeat and milk. Indeed, one study of 830 animalfeeds and 613 milk samples from four Kenyanurban centers showed 86% of the former werepositive for aflatoxin B1 and 67% of these exceededthe Food and Agriculture Organization/WorldHealth Organization level of 5 μg per kg maizemeal [29]. Seventy two percent of the milk fromdairy farmers, 84% (71/85) from large- andmedium-scale farmers and 99% (88/89) of thepasteurized marketed milk were positive foraflatoxin M1. A major outbreak of aflatoxinpoisoning in 2004 resulted in 317 human cases and125 deaths as well as countless dead wildlife. Thetoxin can also stimulate commensal organisms toexpress other toxic compounds afflicting the cows[30]. The potential increase in kwashiorkor due tomycotoxin exposure is particularly relevant giventhe importance of the microbiome in this condition[31]. The proposed study in Boran cattle willtherefore have implications for livestock productivityand human health. Of importance would be to tryto quantitate aflatoxin levels, as chronic exposureis problematic over time.(iv) Determine differences in microbial rumencomposition and function in cattle associatedwith the presence and transmission of zoonoticpathogens. This study will identify any microbialHandling toxinsFermented food, probioticsand health enhancementHuman microbiome andprevention of diseases 5. DISTRIBUTION MARKETINGCOMMUNICATION7. POLICIES, ETHICS AND GUIDELINES CHECK1. RESEARCH2. EVIDENCE BASED CONCEPTS6. CONSUMEREvaluation of consumer feedback and health effects of food interventions3. TRAINING AND EDUCATION4. LOCAL PRODUCTIONFigure 1 Illustration of the model which we believe is critical for the successful expansion of microbiome and probiotic research andproduct development, as well as the engagement of all parties whose input is needed to the process. Three examples of drivers for theresearch are given: fermented foods, the problems with inadvertent ingestion and handling of environmental toxins, and the need for remediesto treat and prevent disease.Reid et al. Microbiome 2014, 2:12 Page 3 of 13 that might help the host resist infection. Ifbeneficial profiles exist, these could form the basisfor whole microbial transplantation, perhaps soonafter birth. Coprophagy is commonplace in someanimals, either to help develop a digestivemicrobiota or to act as a source of vitamins thatare produced by the gut bacteria and then are partof the stool composition [32].(v) A final component of these studies on Boran cattlewould be to identify viral sequences in thetranscriptome, and bank environmental DNA,RNA and rumen samples for later analysis.The proposed studies are achievable within 2 years andwould form a sound basis for many future approaches tomanagement of livestock. These could include the relationto the effect on health and productivity by the environ-ment, feed quality and composition, toxins, antimicrobials,heavy metals and pesticides. In addition, further insightson the reduction of methane production due to rumenbacteria could be obtained.The African Microbiome ProjectThe outstanding advances made possible through theHuman Microbiome Project [33] have transformed ourperception of health and disease. The current data werelargely derived from North American/European subjects,and extrapolation to African subjects may be pertinent.As very few studies have been performed on microbialdiversity in African humans, soil, insects, birds, fish andanimals, this precludes determination of associationswith health and disease. It would be presumptive to sug-gest skewing of microbial composition linked to negativeimpact on health in developed countries, are applicable inanother setting. Therefore, the studies are worth replicat-ing in Africa. Two important projects are currently under-way: The American Gut Project ( is currently surveying thediversity of 10,000 subjects (all ages, both sexes, no exclu-sions) in North America, and The Asian MicrobiomeProject is comparing diversity of subjects across 11 sites(all ages, both sexes, including a sub-focus on mothers andhealthy children). It is unclear how readily concepts de-rived from these data sets could be extrapolated to Africansubjects. We hereby propose ‘The African MicrobiomeProject’, with the objective of determining taxonomic andfunctional (metagenomic) diversity of the bacteria presentin the feces of 10,000 African subjects.To follow the design of the American and the Asianstudies, the ideal would be to collect the stools acrossaround 10 African sites (approximately 1,000 subjectsper site; Figure 2). These would be processed and thenshipped to ILRI in Nairobi or an equivalent site in Africafor shot-gun sequencing to determine taxonomic compos-ition and metagenomic functional pathway representation.Extensive metadata would be collected on participatingsubjects using a universal form to allow association withclinically important phenotypes.MoroccoGuinea BisseauSouth AfricaGhanaCentral African RepublicEgyptKenyaRwandaMalawiZambiaMadagascarGambiaFigure 2 Countries that can be targeted to perform a clinical trial on probiotics to prevent sepsis in children. The selection is basedupon existing infrastructure and collaborations, as well as extent of the sepsis problem.Reid et al. Microbiome 2014, 2:12 Page 4 of 13 type of metadata to be collected should include:– For pregnant women: number of children, parity,whether term or preterm, vaginal or caesarean birth,and duration of breast-feeding.– For infants: growth (height, weight), status at birthand need for any interventions, developmentalscreening and cognition, whether breast-fed orformula or other, and time of weaning.– For all subjects: race, tribe, diet, foods, bloodpressure, health history, known medications andvaccines received, HIV status, gastrointestinalproblems, household size and density, exposureto animals in the home, duration at presentresidence, hygiene and access to toilet. Urinesamples will also be acquired to allow futuremicrobiota assessment and metabolic/functionalcorrelative analysis [34].The expected data resulting from such a study wouldnot only be a tremendous resource of high-quality dataon the African microbiome (taxonomic and functional),from a broad representation of multiple groups (urban/rural; different cultures; traditional and ‘Westernized’food), but provide a rich platform for hypothesis-gene-rating future studies using well established tools (see“Metadata and data handling” below. The next step cur-rently under way is to identify relevant funding sourcesand align multi-disciplinary and multi-national teams tocommence project planning in 2014.Metadata and data handlingThe group reached consensus that samples collectedin Africa should be analyzed by African trainees onsite where possible. Thus, discussion centered aroundways for this goal to be achieved. With regard to collect-ing, storing and sharing metadata, it would be useful tocommunicate the importance of collecting standardmetadata for all samples [35]. There are a number ofstate-of-the-art and readily accessible resources avail-able for Africans wishing to collect and use metadata,and the MIMARKS standard was put forward as themost widely used and general standard that should beadopted for future studies. A resource list is providedin Table 1.Clinical trial on sepsisIn sub-Saharan Africa, sepsis is the cause of at least 10%of all maternal deaths and 26% of neonatal deaths [36].Many factors contribute to these unacceptable high ratesof infection: poor or delayed diagnosis, access to care,and inadequate therapy. A recent study, so far presentedorally but unpublished except in abstract form [37], ofover 4,000 infants in a resource-disadvantaged setting inIndia reported that daily administration for 1 week ofprobiotic Lactobacillus plantarum with 150 mg fructo-oligosaccharide prebiotic in maltodextrin within 72 hoursof birth reduced death or sepsis by 44%, and occurrenceof pneumonia requiring antibiotics by 36%. The studyTable 1 A list of resourcesMIMARKS provides standards on how to collect and record dataTutorial available at: (free, 2-minute process)then retrieve hundreds of examples.Tools ‘Omics’ data requires bioinformaticpipelines: QIIME, Mothur, LEfSe,MetaPhlAn, USEARCH, UPARSE,PandaSeq, and others. They arerelatively complicated andnon-intuitive, but the following sitesare particularly helpful:QIIME forum:!forum/qiime-forumMothur: clusters As ‘Omics’ tools requirecomputational power, it may befeasible to have a local clusterthrough AWS Educational Grants:,or partner with a bioinformatics labsuch as via Project Rosalind: and ProjectEuler: collection and processingprotocols, bioinformatics pipelinesand technical informationEMP: workshops online asabove, and distance workshopssuch as:STAMPS: tutorials: Carpentry: overviews: courses Open courses are also available:Coursera:,such as Biostatistics boot camp,Machine learning, Bioinformaticsmethods with an MIT site beinghelpful. et al. Microbiome 2014, 2:12 Page 5 of 13 to be based upon an earlier encouraging con-trolled trial [38].Whilst the full details of the study design and actualresults still have to undergo adequate peer-review, withquestions over the availability of a patent-protectedformula, the workshop participants considered that arepetition of this study could be very relevant for thesituation in Africa. The probiotic formulation will haveto be carefully considered, taking into account the localprevailing strains as well as available resources. BesidesLactobacillus plantarum, another option would be Lacto-bacillus rhamnosus Yoba, basically an isolate of the GGstrain, but named differently as LGG is off-patent [39],which is available in African in dried sachets.The GG strain has been used safely in pregnantwomen and infants and has been shown to prevent diar-rhea [40-42], indicating appropriateness for use in clinicalsettings. Additional design issues discussed were focusedto assess not simply clinical outcome but also to beginassessing the mechanism(s) of action (presumed to bereduction of neonatal sepsis). To this end we would wantto enroll the pregnant mother and sample her microbiomeclose to birth in a clinical trial and sample stool, saliva,skin, vagina as close as possible after birth. This wouldallow us to ask: is maternal microbiome-transfer to infantaffected by probiotic intervention? We would also want tocompare microbiome of the enrolled infants over the firstyear (stool, saliva, skin), allowing us to ask “does probioticintervention change infant microbiome?”, and collectblood to test the impact of the probiotic intervention oninnate and adaptive immune development, allowing us toask “does probiotic intervention alter immune develop-ment, and does this correlate with increased protection?”.We would also want to collect blood, urine and milk tomeasure metabolome and aflatoxins of pregnant andlactating women, allowing us to investigate if the probioticintervention alters metabolome and toxin concentration,and the amount transferred to the infant.Embracing African fermented foods and plant-basedmicronutrientsDespite a long history of a large variety of fermentedfoods across Africa [43,44], these are not necessarily be-ing passed down to the next generation or incorporatedin the food-based dietary guidelines. The perceptionconveyed by young urban people is that their generationdoes not have time to wait for traditional fermentedfoods that take a while to prepare or cost too much, orare considered inferior because of their taste and quality(as a result of non-standardized artisanal practices). TheWesternization/urbanization of African society, at leastin cities, was seen as a barrier to embracing mostfermented foods unless they could be made available asan affordable, easy and tasty option. A means to do thiswas discussed, particularly around three popular Kenyanfoods: Uji, Black nightshade and Murzik. Given thereported health benefits of fermented foods [45-47], theview was that consumption of these foods should beencouraged, especially since they are part of the trad-itional healthy diet.The following facets, based upon bottom-of-the-pyra-mid principles [48], believed to be important for a newapproach to fermented foods were: Ability to create Uji or another local food as afreshly made, fast, tasty, affordable option. Standardized starter cultures for consistentproduct quality. Continuous product development and productinnovation based on locally available crops. A single message that fermented foods arebeneficial to health. Aggressive and effective marketing, as percurrent fast food companies, and includinguse of social media. Nutritious and safe original local products. A formulation that has the potential to improvematernal-child and youth health. Education and training of consumers andproducers based on good scientific evidence.In order to succeed, youth and new mothers would betargeted as a means of consumer engagement, and alsoas they are at high risk of obesity and diabetes, and theytend to eat more Westernized fast foods ( While many busi-ness models could work, the idea of franchising hadappeal, where each city site could develop a novel product,share these amongst themselves and deliver a consistentsingle message that fermented foods are beneficial. Themodel is shown in Figure 3. In creating the products,microbial strain identification, storage, handling and re-producible processing would be a priority. For sustaina-bility, cooperation amongst the franchises would allow forcontinuous product innovation, especially when linkedwith universities (different faculties), the Ministries ofAgriculture and Health, and farmers. In addition, collabo-rations would be needed to ensure a continuous supply ofraw materials and account for seasonal variations and cropgrowth cycles.The addition of micronutrient rich plants was recom-mended, and Moringa, already used in community yogurtkitchen projects in Tanzania [49] and widely availableacross Africa, was considered a source of micronutrients,along with amaranth [50] and managu (Solanum pseudo-capsicum) [51]. Inclusion of such locally sourced productswill enhance collaborations between food scientists andReid et al. Microbiome 2014, 2:12 Page 6 of 13 to create nutritious, edible and acceptableproducts. Similarly, local foods have been used for foodsupplements in nutrition intervention studies in Malawi[52,53]. A dairy product has also been developed on thebasis of a traditional dish called mutandabota (made frombaobab fruit pulp and sugar), and is widely consumed inSouthern Africa [23].The challenges and opportunities related to educationand training of consumers, patients, students andprofessionalsIn order to improve the general health situation, it is keyto focus on training and education of consumers, stu-dents and professionals, and national authorities. Forinstance, consumer education is often lacking in Africancountries, with many people not reaching secondaryschool level, and many suffering from poor cognitivefunction due to malnutrition. Often, information ispassed from generation to generation, in some casesleading to detrimental outcomes such as early termin-ation of breast feeding because the milk lacks ‘water’and should be substituted by water (which is often con-taminated by pathogens and causes diarrhea), sugar andother foods. The use of nutritious probiotic and fermentedfoods should be promoted through education of people atrisk for malnutrition. This could involve training coursesand/or lectures in existing school and college curricula, andeducating parents and grandparents through communitymeetings. Potentially, university students could play a roleif material was provided to aid them, and measurementtools created so they can gauge resultant change. Theapproach of the Early Years Collaborative ( inScotland is an example where such locally-based initiativesare tried, tested and transferred across regions as a meansto alter failing processes. It is not yet focused on nutrition,but given the traditionally poor Scottish diet this will needto be addressed. Another example is the ENOUGHprogram (which stands for essential nutrients for optimalunderpinning of growth and health) which uses multi-system approaches (physiological using omics technolo-gies, environmental, genetic, social conditions) to reachtwo billion undernourished people [54]. Specifically indeveloping countries, the use of mass media, includingsocial media, has been advocated to improve child-feedingpractices [55].While scarce funding for research is a problem for theentire global research community, the situation in manylow-income countries is dire. At best, a small fraction ofthe gross domestic product is channeled to supportresearch, which results in heavy reliance on donors andforeign agencies whose agendas do not necessarily reflectthe country’s needs, but who end-up dictating nationalscience agendas. African scientists educated abroad oftenreturn to empty laboratories and large teaching loads. InLIFESTYLE DISEASESPROBLEMFRANCHISESIMPROVING ACCESSINCOME GENERATIONLOCAL RADIO AND SOCIAL MEDIASHAPING ASPIRATIONSFERMENTED FOODSTAILORING LOCAL SOLUTIONSFermented foods as business oppurtunity to combat life style diseases and stimulate economic activitiesFigure 3 Illustration of the problems emanating from lifestyle changes in African countries, in particular leading to changes in diet. Webelieve that fermented food consumption, once a mainstay in many communities, could be re-introduced to counter poor fast foods, but to dothis large efforts are needed in communicating the benefits, and social business models created that permit innovation and independence, andprovide a collective message to the consumer.Reid et al. Microbiome 2014, 2:12 Page 7 of 13 view, the potential is enormous for many brightAfrican students to learn these methodologies and utilizethem at home to study areas of relevance to their countryand population. Thus, increased national funding of re-search based on established priorities is clearly needed.In Kenya, the National Commission for Science,Technology and Innovation has managed to persuadethe Kenyan Government to allocate 2% of the grossdomestic product to research funding which is a positivedevelopment, although it remains to be implemented. Itmay be a good time for researchers of high standing tosupport organizations like the National Commission orequivalent in other countries to provide more support ofresearch. For example, in Canada, an advocacy orga-nization, Research Canada, was formed to engage in influ-encing the public policy process directly and indirectly( Researchers provide for-ums to update Members of Parliament on new advancesin medical science. African scientists also could educatethe public on issues of research progress in various dis-eases and conditions like malnutrition, and other factorsthat affect health and longevity.It is no secret that scientists and policy makers havedifferent goals, attitudes toward information, concept oftime and reporting structures [56]. The lack of under-standing and respect and differing views on prioritiesemphasizes the need to work together, have open dia-logue and information sharing, and develop incentives toadvance evidence-based policy and practice. Given theimportance of the human and animal microbiomes andtheir manipulation via probiotics, efforts to convey infor-mation can only have a positive effect on the publicunderstanding these concepts.Another constructive suggestion is to include in anation’s Food Guide a statement that fermented foodsshould be taken regularly due to their many health bene-fits. The rationale is supported by vast literature on thehealth benefits of these foods through human history.Increasing the impact of probiotics through foodIn recent years, a practical approach has been under-taken to transfer probiotic research and products to vul-nerable adults and children in Tanzania, Kenya, Rwandaand Uganda, including those who are HIV positive. Theconcept utilizes locally sourced food and empowerscommunity members at the bottom-of-the-pyramid toproduce probiotic yogurt. This endeavor was motivatedby the eight United Nations Millennium DevelopmentGoals, established in 2000 as a moral path towardsequality and health for all humankind (; Table 2). Making pro-biotic foods available to the poorest will contribute to allbut goal 2 (achieve universal primary education) of theMillennium Development Goals [22,57-59]. An essentialand sustainable target is to empower local people toestablish social businesses, defined as ‘a non-loss, non-dividend company designed to address a social objectivewithin the highly regulated marketplace of today’ [60], aswell as to make probiotics (both local and international)more accessible to a larger population. The empower-ment of women to create and run these social businesseshas so far proved successful [38,61].However, the kitchen yogurt model requires support atstart-up by local medical research authorities, farmersand foreign partners, and may be unsuitable to reach themillions of people facing poverty, malnutrition, maternaland infant morbidity and mortality and infectious dis-eases. The delegates discussed the challenges in over-coming this barrier.One idea is to provide as many resource disadvantagedpeople as possible with access to probiotic fermentedfoods via affordable sachets containing shelf-stable bene-ficial bacteria and micronutrients. The sachet contentscan be inoculated into milk to make yoghurt or added toother foods and fermented, or simply sprinkled overregular food. Figure 4 shows several production anddistribution channels for probiotic fermented foodsusing existing infrastructures, or via home-use. Collabor-ation across Kenya, Tanzania and Uganda could providean impetus, with efforts conjointly being made to expandto Rwanda, Ethiopia and other neighboring countries(Table 3). The focus for the 5,000 beneficiaries of thecurrent kitchens (10 in Tanzania, 3 in Kenya, 1 in Uganda)is mothers, children, and HIV/AIDS patients. To attain agoal of 500,000 recipients within 5 years, the products willhave to reach the broader population and take account oflocal dietary habits. This might be via goat and camel milkin Ethiopia, or through cereals in other regions.The partnerships form critical components of the set-up. Developed countries provide training for personneland laboratory resources to perform microbiome analysis,genome sequencing, and probiotic research. In Africa,facilities such as at ILRI provide a means for 16S sequen-cing analysis. Collaborations can employ dissemination ofTable 2 The United Nations Millennium DevelopmentGoals established by a target date of 2015Goal number Millennium goalGoal 1 Eradicate extreme hunger and povertyGoal 2 Achieve universal primary educationGoal 3 Promote gender equality and empower womenGoal 4 Reduce child mortalityGoal 5 Improve maternal healthGoal 6 Combat HIV/AIDS, malaria and other diseasesGoal 7 Ensure environmental sustainabilityGoal 8 Develop a global partnership for developmentReid et al. Microbiome 2014, 2:12 Page 8 of 13 about foods and their health benefits, book-keeping, sanitation and food hygiene. This can also allowAfrican concepts to be pursued. For example, a novel pro-biotic yogurt containing L. rhamnosus GR-1 and NN-20created by Kenyans and Canadians is being tested inEmbu, Kenya, for its ability to reduce aflatoxin poisoningfrom ingestion of corn and peanuts, through aflatoxin-binding properties [62-64].Sachets have already been developed by partnersYoba-for-life (, containing L.rhamnosus Yoba and S. thermophilus. Their 1 g driedcontents, manufactured in The Netherlands, are addedto 1 liter pasteurized milk and incubated in existing(small-scale) dairy production plants, then inoculatedinto 50 liters to produce probiotic yogurt. This avoidshaving to produce the probiotic Yoba at a separate site,as currently is required for the L. rhamnosus GR-1 Fitiyogurt produced by the Kenyan and Tanzanian kitchens.The Uganda Industrial Research Institute trains thepersonnel to set up and run their dairy plants, and onecurrently provides yogurt to 1,000 people each day. Theplan is to reach 150,000 people within the next 2 yearsthrough growth of dairy plants. The Yoba strain hasbeen extensively studied and shown to enhance immun-ity and prevent and treat diarrhea which are issues com-mon to the Ugandan consumers living under poverty[39]. Depending on the production and sales point, theyogurt costs approximately 1,400 UGX/L (approximatelyUS$0.56) to produce and is sold for 2,800 UGX/L(approximately US$1.12) to the final consumer, allow-ing a small profit for the employees at the productionand distribution site. This sales price is around 13cents for an equivalent tub of probiotic yogurt sold inCanada for over 43 cents.This initiative, along with making sachets containingL. rhamnosus GR-1 and NN-20, will not be withoutchallenges in education, product handling, control andpricing, but the potential payoff will be significant. At aminimum, re-introducing beneficial microbes into thefood chain and society will counter the negative fastfood, low nutrient products that have swept the market,or staple foods like rice and maize that offer little inFigure 4 In order to provide nutritious, safe, local foods supplemented with probiotics and affordable to the bottom-of-the-pyramid,the following model is proposed. Existing products, Fiti yogurt in Tanzania and Kenya, and Yoba-for-life in Uganda provide stepping stones,and their distribution through community kitchens and mini-plants, and via dried sachets, with the aid of partnerships, is estimated to reach closeto one million people within 5 years.Reid et al. Microbiome 2014, 2:12 Page 9 of 13 value. Throughout this process, the unwaveringaim will be to retain the social business, bottom-of-the-pyramid model [48]. While competitors exist now andwill do so later, at least in the yogurt market, their prod-ucts are expensive and without probiotic added value,and they will always have a market, especially as incomesincrease with developments occurring in the region. But,for as long as millions of children and adults live inpoverty and an environment where infectious diseasesand other ailments affect them, the need for affordable,nutritional products will exist.SummaryThe following recommendations emerged from thisproductive workshop.1. Africa is on the verge of novel and exciting researchon the microbiome and probiotics. We recommendthat partnerships be created or expanded that enablethe science, help train personnel, and translateevidence-based solutions in a continual circle ofactivity which integrates microbiome and probioticresearch with products that benefit societies, nomatter their cultural diversity.2. Studies are critically needed to understand themicrobiome of animals, soil, plants, insects andhumans in the African continent, so as to create aplatform for innovative advances in how health isrestored and maintained.3. Efforts are urgently required to take probioticconcepts in affordable food formulations andfacilitate access to those who need them most. Thiswill help reduce the risk of morbidity and mortalityespecially for women and newborns. Both theproduction and distribution of traditional local andinternational probiotics should be investigated.Probiotics are not a substitute for vaccines, certaindrugs, hygiene practices and nutritious food, butuntil these options reach the most needy, probioticscan help save many lives and turn the societalculture back to some of the traditional foods thatbenefited past generations.4. Programs are needed in primary/secondary schoolsand communities to embrace the healthfulconsumption of traditional foods and to resistdietary myths or new fads of fast, poor nutritionalfoods. Education at the college and university levelsis needed to introduce the new field of microbiomeTable 3 Examples of different approaches for three countries that collectively lead to increased availability ofprobiotic food, including for the very poorest in society; the key engagement of partners is vitalWhere Who What How ForKenya • Teachnical University of Kenya,Jomo Kenyatta University ofAgriculture and Technology• Food Science and Technology,and new product development• Local yoghurt kitchens • People with HIV/AIDS• Ministry of Agriculture, and Ministryof Gender and Social Services• Bottom of pyramid businessdevelopment• Train-the-trainer workshops • People exposed toaflatoxins and otherpopulation• Local production of Fiti yogurt • Lactobacillus rhamnosus GR-1 anti-infective and immunomodulatoryeffects• General population• Distribution networks for sachets • Weissella spp. NN-20 detoxicationeffectsTanzania • Western Heads East internshipprogram• Local production of Fiti yogurt • Local yoghurt kitchens • People with HIV/AIDS• African Probiotic Yogurt Network • Supplemented with Moringa andpotentially other micronutrient-richfoods• Train-the-trainer workshops • General population• National Institute for MedicalResearch support• Distribution networks for sachets • Addition of MoringaUganda • Yoba for Life Foundation • Local production of probiotic Yoba • Local production plants • General population• Uganda Industrial ResearchInstitute• Food Science and Technologyproduct development• Using existing infrastructures• Makarere University • Bottom of pyramid social businessdevelopment• Train-the-trainer workshops• Heifer International • Incubator programs • Lactobacillus rhamnosus Yobafor gut health• Local dairy producers • Distribution networks for sachetsReid et al. Microbiome 2014, 2:12 Page 10 of 13, and to train Africans on the complexitiesof ‘omics’ fields. Likewise, knowledge must beconveyed to the politicians who are the gatekeepersof resources. For that, we suggest the support forResearch Councils composed of respected andinnovative African researchers.5. Lastly, African governments should invest inresearch on the microbiome and probiotics withtangible funding that provides their scientists,physicians and other researchers with the facilitiesand operating grants to train students, and developcommunity-based solutions to community-basedproblems. By doing so, the return on investment willfar outweigh the output, with savings in healthcareand development of new businesses and productsfor exportation. It is no longer an option to rely onforeign philanthropy, when Africans have theknowledge, are keen to acquire the training andalready show the determination to lead the field notfollow it. None of the Millennium DevelopmentGoals can be reached without such an investmentand without the encouragement of two-waypartnerships.AbbreviationILRI: International Livestock Research Institute.Competing interestsThe authors declare that they have no competing interests.Authors’ contributionsGR co-organized the workshop, invited the participants, chaired the meeting,coordinated the manuscript writing and made the final revisions; SK hostedthe event and provided critical input into the manuscript; NN assisted withlocal organization and provided critical input into the manuscript; WS andRK provided assistance with the figures, with leading discussion during theworkshop and critical input into the manuscript; TRK helped provide supportand funding, and critical input into the manuscript; RA, HB, EMB, AE, HEl-N,GBG, IIK, JL, AM, WM, RM, AMc, JO, PAO, AO, SR, ES, SS, AS, JS, WVT, DW - allcontributed to the discussions and critical input into the manuscript.All authors read and approved the final manuscript.AcknowledgementsWe appreciate financial support for logistics from the MIMI Network grantfrom the Canadian Institutes for Health Research; the support of ILRI for theevent; the Ministry of Agriculture of Kenya and International ScientificAssociation for Probiotics and Prebiotics for their support andencouragement. TRK is supported in part by a Career Award in theBiomedical Sciences from the Burroughs Wellcome Fund, and a MichaelSmith Foundation for Health Research Career Investigator Award.Author details1Lawson Health Research Institute and Departments of Microbiology &Immunology, and Surgery, University of Western Ontario, 268 GrosvenorStreet, London, Ontario N6A 4V2, Canada. 2Ministry of Agriculture, WaruhiuAgriculture training Center, P.O. Box 800, Githunguri, Kenya. 3Yoba for LifeFoundation, Hunzestraat 133-A, 1079 WB Amsterdam, The Netherlands. 4TNOMicrobiology and Systems Biology, Utrechtseweg 48, 3704 HE Zeist, andMolecular Cell Physiology, De Boelelaan 1085, 1081 HV, VU University,Amsterdam, The Netherlands. 5Department of Pediatrics, Division ofInfectious Diseases, University of British Columbia, CFRI A5-147, 950 W28thAve, Vancouver, BC V5Z 4H4, Canada. 6Department of Pathology, Aga KhanUniversity Hospital, Nairobi, Kenya. 7Taita Taveta University College, P.O. Box635–80300, Voi, Kenya. 8Michael Smith Laboratories and Department ofMicrobiology and Immunology, University of British Columbia, Vancouver,Canada. 9Danone Nutricia Research, Uppsalalaan 12, 3584 CT, Utrecht, TheNetherlands. 10School of Biological Sciences, University of Hong Kong,Pokfulam Rd, Hong Kong, Hong Kong SAR. 11Department of Biochemistry,University of Western Ontario, London, ON, Canada. 12Jomo KenyattaUniversity of Agriculture and Technology, P.O. Box 62000, (00200) Nairobi,Kenya. 13Consultative Group on International Agricultural Research, ILRI,Nairobi, Kenya. 14School of Population and Public Health, Faculty ofMedicine, University of British Columbia, Vancouver, BC V6T 1Z3, Canada.15Department of Animal Production, College of Veterinary Medicine andAgriculture, Addis Ababa University, Debre Zeyte, Ethiopia. 16Department ofReproductive Health/Biology, Institute of Primate Research, Karen, Nairobi,Kenya. 17University Teaching Hospital of Kigali, National University of Rwanda,Kigali, Rwanda. 18Functional Foods Forum, The Medical School, University ofTurku, 20014 Turku, Finland. 19Department of Oncology, Turku UniversityHospital, 20520 Turku, Finland. 20Department of Food and NutritionalSciences, School of Chemistry, Food and Pharmacy, University of Reading,Reading RG6 6AP, United Kingdom. 21Department of Chemistry andBiochemistry and BioFrontiers Institute, University of Colorado at Boulder,Boulder, CO 80309, USA. 22International Livestock Research Institute, Nairobi,Kenya.Received: 15 January 2014 Accepted: 6 March 2014Published: 16 April 2014References1. 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Food Chem Toxicol 1997, 35:535–545.63. el-Nezami H, Kankaanpää P, Salminen S, Ahokas J: Physicochemicalalterations enhance the ability of dairy strains of lactic acid bacteria toremove aflatoxin from contaminated media. J Food Prot 1998, 61:466–468.64. Lahtinen SJ, Haskard CA, Ouwehand AC, Salminen SJ, Ahokas JT: Binding ofaflatoxin B1 to cell wall components of Lactobacillus rhamnosus strainGG. Food Addit Contam 2004, 21:158–164.doi:10.1186/2049-2618-2-12Cite this article as: Reid et al.: Harnessing microbiome and probioticresearch in sub-Saharan Africa: recommendations from an Africanworkshop. Microbiome 2014 2:12.Submit your next manuscript to BioMed Centraland take full advantage of: • Convenient online submission• Thorough peer review• No space constraints or color figure charges• Immediate publication on acceptance• Inclusion in PubMed, CAS, Scopus and Google Scholar• Research which is freely available for redistributionSubmit your manuscript at et al. 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