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Titelpagina 2004-1-jaarboek

04-marcotty-:Opmaak 1 5/07/11 11:54 Pagina 293 Meded. Zitt. K. Acad. Overzeese Wet.
Bull. Séanc. Acad. R. Sci. Outre-Mer
56 (2010-3): 293-302
Veterinary Medicine and Human Public Health in Africa*
Tanguy MARCOTTY1, 2, Séverine THYS1, Jackie PICARD2 & KEYWORDS. — One Health; Africa; Zoonosis; Perception; Antimicrobial Resistance.
SUMMARY. — The “One Health” concept refers to the fact that animals and humans share many biological, physiological, medical and epidemiological features and advocatesfor increased collaboration between the medical and veterinary sectors to improve bothhuman and animal health. In Africa, intersectoral collaboration is particularly relevant inthe surveillance of emerging diseases and zoonoses, in the control of diseases andzoonoses in humans and animals and in the use of antimicrobials and anthelmintics. Thispaper reports on the importance of brucellosis and zoonotic tuberculosis in sub-SaharanAfrica, on the people’s perception of hydatidosis and hydatidosis control in Morocco andon antibiotic resistance in Klebsiella isolated in surface water in South Africa as illustra-tions of the “One Health” concept.
MOTS-CLES. — One Health; Afrique; Zoonose; Perception; Antibiorésistance.
RESUME. — Médecine vétérinaire et santé publique humaine en Afrique. — Le concept de One Health dérive du fait que l’animal et l’homme partagent de nombreuses caractéris-tiques biologiques, physiologiques, médicales et épidémiologiques. Ce concept préconiseune plus grande collaboration entre les secteurs médicaux et vétérinaires afin d’améliorerla santé humaine et animale. En Afrique, la collaboration intersectorielle se justifie en particulier pour la surveillance des maladies et des zoonoses émergentes, pour le contrôledes maladies et des zoonoses chez l’homme et l’animal et pour l’utilisation d’antibiotiqueset d’anthelminthiques. Afin d’illustrer le concept One Health, cet article aborde l'impactde la brucellose et de la tuberculose zoonotique en Afrique subsaharienne, la perceptionde l’hydatidose et de son contrôle au Maroc, et enfin la résistance aux antibiotiques deKlebsiella isolés dans l'eau de surface en Afrique du Sud.
* Paper presented at the meeting of the Section of Natural and Medical Sciences held on 27 April 2010. Publication decision taken on 23 November 2010. Final text received on 8 December 2010.
Animal Health Department, Institute of Tropical Medicine, Nationalestraat 155, B-2000 Antwerp Veterinary Tropical Diseases Department, University of Pretoria, P Bag X04, Onderstepoort † Late member of the Academy (P. Van den Bossche tragically died in a car crash in Antwerp on 11 November 2010; this article is dedicated to his vision of animal and human health in Africa).
04-marcotty-:Opmaak 1 5/07/11 11:54 Pagina 294 TREFWOORDEN. — One Health; Afrika; Zoönose; Perceptie; Antibioticaresistentie.
SAMENVATTING. — Diergeneeskunde en menselijke volksgezondheid in Afrika. — Het One Health concept verwijst naar het feit dat mens en dier een aantal biologische, fysio-logische, medische en epidemiologische processen delen en streeft naar een nauweresamenwerking tussen de medische en diergeneeskundige sectoren ter bevordering van demenselijke en dierlijke gezondheid. In Afrika is zulk een samenwerking van belang bij hettoezicht op het uitbreken van ziekten, de controle van ziekten bij mens en dier en voor hetstimuleren van een rationeler gebruik van antibiotica en anthelmintica. In deze publicatiewordt het belang van de One Health benadering geïllustreerd a.h.v. de impact van brucel-lose en zoötische tuberculose in Afrika ten zuiden van de Sahara, de invloed van percep-ties in hydatidosebestrijding in Marokko en de ontwikkeling van antibioticaresistentie inKlebsiella in Zuid-Afrika.
The “One Medicine” concept was initially proposed by Calvin Schwabbe, a veterinary epidemiologist, in his book “Veterinary Medicine and Human Health”(1984). His idea referred to the fact that humans and animals share a number ofpathogens, known as zoonotic, as well as many physiological, immunological,pathological, surgical, medical and epidemiological principles. Though CalvinSchwabbe initially restricted the concept to medicine (the art to control and curediseases), the “One Health” concept was, at a later stage, extended to all healthissues (KING et al. 2008). For instance, experimental animals have been extensive-ly used in biomedical and pharmacological research, and improved understandingof immunological and pharmacological mechanisms have greatly contributed tothe development of new drugs and vaccines for use in animals and humans.
Finally, some epidemiological concepts, such as endemic stability, were firstdeveloped in animals (COLEMAN et al. 2001) before being applied in human epidemiology (SARGEANT 2008). The “One Health” concept becomes useful when the collaboration between the medical and the veterinary sectors generates more benefit than a mere sum oftheir respective outcomes. This is the case if, for instance, the knowledge gainedin animal science can be applied to human medicine or when disease surveillanceor control in animals does not only improve animal health but also positivelyaffects human health (ZINSSTAG et al. 2007). In Africa, the field of neglectedzoonoses is probably the area in which collaboration between the veterinary andthe medical professions would be the most profitable, mainly in terms of publichealth (WHO 2006). Neglected zoonoses were listed by WHO and includeanthrax, brucellosis, bovine tuberculosis, leishmaniasis, African trypanosomiasis,hydatidosis, cysticercosis and rabies. Control tools do exist for most of them andwere successfully used in many industrialized countries. The reasons why low-resource countries still fail to control endemic zoonoses might not be technical oreconomic. It is suspected that people’s perception of animals, zoonoses and 04-marcotty-:Opmaak 1 5/07/11 11:54 Pagina 295 control of animal diseases and zoonoses play a major role in the success of disease control programmes. Evaluating the communities’ needs and demand fordisease control and the acceptability and transferability of the different controltools should be a prerequisite to the development and implementation of zoonosiscontrol strategies (MARCOTTY et al. 2009).
The emergence of drug resistance among animal and human pathogens is, on the other hand, a serious threat to public health (WHO 2005). The medicalsector could benefit from the lessons learned in animals with the emergence ofresistance against a large number of anthelmintics when drugs were extensivelyused in the field (GEERTS et al. 1997). A more rational use of drugs employed inhuman and animal medicine could also benefit human health. Enterobacteriaceaecausing diarrhoea in humans are known to acquire resistance in animals beforebeing transmitted to people through the consumption of contaminated food(ANGULO et al. 2004, MOLBAK 2004). This is particularly a problem in elderly andimmunologically compromised populations. In Africa, the development of anti -biotic resistance in Klebsiella species is a serious concern, especially in infantsand children (LAUTENBACH et al. 2005). Klebsiella being a commensal bacteriumwidely found in animals and in the environment, the development of antibioticresistance in animals could be very detrimental to human health.
The aim of this paper is therefore to illustrate the impact of endemic zoonotic diseases in low-resource communities in Africa, to describe the communities’perception of zoonotic diseases and control strategies and to evaluate the risk ofantibiotic resistance transmission from animals to humans in some African settings.
Zoonotic Diseases in Africa:
The Example of Brucellosis and Bovine Tuberculosis
Zoonoses are diseases that are transmissible from animals to humans. They should be distinguished from emerging diseases of animal origin. In fact, it isestimated that 62 % of human pathogens, including the viruses causing AIDS,Ebola, SARS and Chikungunya, originate from animals and have crossed thespecies barrier (TAYLOR et al. 2001). Emerging diseases often break out in developing countries, where people live in close contact with domestic and wildanimals carrying wide and unknown collections of potential pathogens. Unlikeendemic zoonoses, emerging infectious diseases usually attract major interna-tional interest, given their potential threat to the whole world. Brucellosis and bovine tuberculosis are two zoonoses for which animals are the only reservoir (ACHA & SZYFRES 2003a). They are transmitted through directcontact with infected animals or animal products. Zoonotic Brucella species aremainly found in cattle, sheep and pigs where they cause abortion and reduced fertility. In humans, brucellosis causes a flu-like syndrome called undulant fever.
04-marcotty-:Opmaak 1 5/07/11 11:54 Pagina 296 Brucellae were described in numerous domestic and wild species throughout theworld (GODFROID et al. 2005). Vaccinating the young female stock reduces signif-icantly the risk of abortion in animals and the chance of Brucella transmission tohuman beings (MORIYON et al. 2004). In Africa, vaccination is erratic and it isassumed that most of the domestic animals in Africa are unvaccinated (MARCOTTYet al. 2009). Though brucellosis is considered a notifiable disease in most countries (making its declaration compulsory), very few African governmentshave their animals tested and the positives slaughtered. In spite of the absence ofcontrol in animals, human cases are rarely reported. This could be due to lowprevalence in livestock, low transmission from livestock to people, low patho-genicity in people or lack of diagnostic ability (MARCOTTY et al. 2009).
Mycobacterium bovis causes tuberculosis in many mammal species, including man (ACHA & SZYFRES 2003a). In animals, tuberculosis mostly affects cattle anda number of wild mammalian species resulting in a chronic and debilitating disease which may ultimately lead to death. Infection in cattle occurs predom -inantly via the aerial route as evidenced by the formation of granulomas in thelungs and associated lymph nodes. Dissemination of the bacterium from thesesites will result in tuberculous mastitis in about 10 % of cows. In humans,M. bovis tuberculosis cannot be differentiated clinically and on sputum cytologyfrom the human tuberculosis caused by Mycobacterium tuberculosis (GRANGE2001). Mycobacterium bovis is mostly transmitted to humans from cattle throughthe consumption of dairy products causing extra-pulmonary tuberculosis, unlikeM. tuberculosis which is mostly transmitted among humans through the aerialroute. Yet, human beings could also be infected by M. bovis through the aerialroute following close contact with infected cattle.
Much information is available on the prevalence of tuberculosis and brucel- losis in livestock in Africa (COSIVI et al. 1998, MCDERMOTT & ARIMI 2002), butvery little is known on their impact on human health as zoonoses. Internationalexperts have recommended that modern diagnostic tools are made available inlow-resource countries, even if they are not particularly cheap, to ensure accuratediagnosis in humans (MARCOTTY et al. 2009). So as to reduce the cost, the collab-oration between medical and veterinary laboratories and the development ofregional laboratories have been encouraged. As far as control is concerned, it hasbeen admitted that eradication of brucellosis and tuberculosis from livestock inlow-resource countries might not be possible in the near future. Instead, livingwith the diseases and mitigating their effects is viewed as a better approach. Insuch a case, the burden of diseases on animal and human health should be betterquantified and control strategies suiting the communities’ habits and perceptionsshould be developed accordingly.
The prevalence of animal brucellosis in low-resource communities varies greatly. In a recent study in Kenya, values ranging between 20 and 30 % wererecorded in Turkana and Maasai cattle, indicating a state of endemicity (Marcottyet al., in preparation). These pastoral communities usually have little contact with 04-marcotty-:Opmaak 1 5/07/11 11:54 Pagina 297 medical services and the incidence of brucellosis in humans, particularly ininfants and children, is unknown. Other areas in Kenya and Zambia presentedwith a lower prevalence but were also considered as endemic. Arid areas in Kenyaand Ethiopia were found free of brucellosis in cattle (Marcotty et al., in prepara-tion; AMENU et al. 2010). This could be explained by the reduced survival of thebacterium in the environment and, consequently, the reduced transmission fromone animal to another. Brucellosis in small ruminants seems to be rare in sub-Saharan Africa. Brucella melitensis, the main causative agent of brucellosis insheep and goats, relies on large populations of small ruminants and probably failsto survive in areas where animals are scattered, like in most parts of sub-SaharanAfrica. Pigs might be an important source of Brucella in low-resource settings.
Village pigs showed a seroprevalence of 16 % in eastern Zambia (Marcotty et al.,in preparation). There is need to confirm the role of pigs as reservoir in this areasince all Brucellae of pig origin are not pathogenic to humans (ACHA & SZYFRES2003a).
In spite of the absence of tuberculosis control in cattle, tuberculosis seems to be absent or to present a low prevalence in traditional cattle in several sub-Saharan areas. We have observed that in central Ethiopia (AMENU et al. 2010) andin Kwazulu-Natal in South Africa (Geoghegan et al., recent data). The situationin South Africa is particularly striking since cattle raised next to highly infectedbuffalo populations (MICHEL et al. 2009) were found free of tuberculosis. The riskof zoonotic tuberculosis might, however, be substantially higher in commercialsettings or in periurban areas since exotic cattle and cross-breeds were reportedto be more sensitive to tuberculosis (AMENI et al. 2007). Perception of Zoonotic Diseases:
The Example of Hydatidosis in Morocco
Hydatidosis is endemic in several African countries, mainly where sheep are raised (ACHA & SZYFRES 2003b). This parasitic zoonosis is caused by a taeniidworm (Echinococcus granulosus). The adult form is short and found in largenumbers in the intestine of canines. Eggs shed in the environment are infective tosheep and other species, including man. The larval stage develops mostly in theliver and lungs of their host, where they cause large-size hydatid cysts. Thesecysts are infective to dogs when they feed on infected dead animals or offal.
Animals do not seem to suffer much from the infection but livers are usually dis-carded from human consumption due to their unpleasant appearance. In humans,hydatidosis is a chronic but severe disease. Depending on their locations, cystsmay be painful and cause organ failures. Human hydatidosis is usually treatedsurgically. Operations are difficult to implement in low-resource countries andoften prove to be painful and prone to complications (SHAW et al. 2006, ALI et al.
2005, COONEY et al. 2004).
04-marcotty-:Opmaak 1 5/07/11 11:54 Pagina 298 In Morocco, human hydatidosis remains particularly frequent in the Berber community in Atlas (MACPHERSON et al. 2004, AZLAF & DAKKAK 2006) despitenumerous control attempts. In order to address this public health issue, people’sperceptions of the disease and of the way it is transmitted or controlled should bestudied using socio-anthropological and behavioural theories (ELLIS-IVERSEN et al.
2010). Focus-group meetings were therefore organized to identify the importancethe communities were giving to human and animal hydatidosis and to identifypossible control strategies (CHOMEL 2008). Focus-group meetings consist of eightto ten persons brought together and asked to express their views on specific issues(PATTON 2002, DAWSON et al. 1993). These meetings are animated by trained facil -i tators and recorded for analysis purpose. In Morocco, focus groups were carriedout among male and female villagers separately and among butchers. Discussionsmainly focused on the severity of hydatidosis in people, people’s knowledge ofsheep hydatidosis and transmission to man, the role of dogs in society, the controlof stray dogs and how to restrain dogs from feeding on sheep offal. Preliminary results indicate that the communities consider human hydatidosis as a serious and relatively frequent disease but poorly understand the cycle of theparasite (Thys et al., in preparation). Actually, the cycle is rather complicated andpeople tend to believe that humans are infected through contact or consumptionof infected sheep. Very few of them are aware that dogs and dog faeces are theonly source of infection for other species. The communities are aware that straydogs may be harmful and that feeding dogs with offal is not a good practice.
However, dogs play an important role in the communities in terms of herding andsecurity. Dogs are usually not fed and have to find food on their own, often onmarkets, abattoirs and butcheries. People fear stray dogs, mostly for attacks, bitesand rabies, but have no means to control them. Butchers claim to have no alter-native to dispose of offal though, by law, they should be appropriately dealt with.
Finally, living without dogs does not seem to prevent people from hydatidosis.
Contamination of the water system by dog faeces might explain why hydatidosiscases remain so frequent in the area even in the absence of dogs in villages.
Klebsiella Resistance against Antibiotics
Klebsiella, a commensal bacterium widely found in the environment and in animals, is a frequent cause of human infection and septicaemia in Africa(SIMEUNOVIC et al. 2009, OKESOLA & KEHINDE 2008, IREGBU et al. 2006). ResistantKlebsiella, especially those that are resistant to sulphonamides, aminoglycosidesand the broad-spectrum beta-lactam drugs, are getting commonplace in humaninfections (LAUTENBACH et al. 2005). The emergence of antibiotic resistance in anumber of human enterobacteria (E. coli, Salmonella and Campylobacter) wasattributed to the use of antibiotics in animals, especially as food additives for pigsand chickens (ANGULO et al. 2004, MOLBAK 2004). In a recent study, we therefore 04-marcotty-:Opmaak 1 5/07/11 11:54 Pagina 299 tried to confirm whether industrial animal production settings contaminated sur-face water with antibiotic resistant Klebsiella. Klebsiella bacteria were isolatedfrom two polluted rivers in Johannesburg (South Africa), in the vicinity of humansettlements or industrial animal production units, and tested for their resistanceto antibiotics used in veterinary and human medicine. Resistant Klebsiella weremainly isolated in surface water in high human activity areas (Picard et al., inpreparation). Furthermore, resistance was mainly observed against drugs that arenot used in animals. Therefore, this study tends to demonstrate that the emer-gence of antibiotic resistance in Klebsiella in Johannesburg is most likely causedby the use of antibiotics in human patients and that the role played by animal husbandry in the emergence of Klebsiella resistance against antibiotics is marginal. Interestingly, this study and a small pilot study done in poultry work-ers and broilers indicate that tetracycline resistance is more common in Klebsiellaof animal origin. Thus, resistance to this class of antibiotic may act as a markerfor animal to human transfer of resistance. Yet, the use of critically importantantibiotics should be reserved to humans and not be allowed in animals, as sug-gested by WHO ( 2005), to reduce by all means the risk of resistance emergenceagainst these drugs. Conclusion
The “One Health” concept advocates for increased collaboration between the veterinary and the medical sectors, in particular in the field where collaborationgenerates added value. In Africa, intersectoral collaboration would be most need-ed for surveillance of endemic zoonoses, diseases emerging from animals andantibiotic resistance development. As far as the control of neglected zoonoses isconcerned, it is crucial to better quantify the burden of these zoonoses on humanand animal health before control strategies are developed. Control strategiesshould meet the needs and expectancies of the medical and veterinary sectors, beacceptable by and transferable to the target populations, and be cost-effective.
The occurrence and transmission of zoonotic diseases are sometimes difficult tounderstand by local communities. It would be important, if justified by the burden on human health, to improve people’s education on zoonoses so that thecommunities could contribute to the development of more adapted control strat -egies, taking into account, for instance, the role that animals play in society andthe relationship between humans and animals. The cost of zoonoses controlstrategies should ideally be equitably borne by the medical and the veterinarysectors. This is often the problem in developing countries, where the veterinaryservices are expected to control zoonoses in animals for the benefit of humanhealth. Veterinary services often fail to meet their responsibilities due to lack offunding. More coordinated actions will hopefully result in more cost-effectivesurveillance and control of diseases transmissible from animals to man in Africa.
04-marcotty-:Opmaak 1 5/07/11 11:54 Pagina 300 These studies were carried out in the context of the framework agreement (FW-3, Strategic Network on Zoonoses) between the Belgian Directorate General of DevelopmentCooperation (DGDC) and the Institute of Tropical Medicine (ITM), Antwerp. The finan-cial support of DGDC was greatly acknowledged. The involvement of various departmentsof the ITM, the Department of Veterinary Tropical Diseases, Pretoria, the Laboratoire deParasitologie, Institut Agronomique et Vétérinaire, Rabat, and the Veterinary andAgrochemical Research Centre, Brussels, was much appreciated.
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