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Emerging or re-emerging bacterial zoonoses [Foreword] Jean de Rycke, B Chomel To cite this version: Jean de Rycke, B Chomel. Emerging or re-emerging bacterial zoonoses [Foreword]. Veterinary Re- search, BioMed Central, 2005, 36 (3), pp.265-266. �hal-02670898� HAL Id: hal-02670898 https://hal.inrae.fr/hal-02670898 Submitted on 31 May 2020 HAL is a multi-disciplinary open access L’archive ouverte pluridisciplinaire HAL, est archive for the deposit and dissemination of sci- destinée au dépôt et à la diffusion de documents entific research documents, whether they are pub- scientifiques de niveau recherche, publiés ou non, lished or not. The documents may come from émanant des établissements d’enseignement et de teaching and research institutions in France or recherche français ou étrangers, des laboratoires abroad, or from public or private research centers. publics ou privés. Copyright
Vet. Res. 36 (2005) 507–522 507 © INRA, EDP Sciences, 2005 DOI: 10.1051/vetres:2005008 Review article Emerging or re-emerging bacterial zoonoses: factors of emergence, surveillance and control Jean BLANCOUa**, Bruno B. CHOMELb*, Albino BELOTTOc, François Xavier MESLINd a Honorary Director General of the Office International des Epizooties, 11 rue Descombes, 75017 Paris, France b WHO/PAHO Collaborating Center on New and Emerging Zoonoses, Department of Population Health and Reproduction, School of Veterinary Medicine, University of California, Davis, CA 95616, USA c Veterinary Public Health Unit, Pan American Health Organization, 525 Twenty-third Street N.W., Washington, DC 20037, USA d Strategy Development and Monitoring of Zoonoses, Food-borne Diseases and Kinetoplastidae (ZFK), Communicable Diseases Control Prevention and Eradication (CPE), 20 avenue Appia, 1211 Geneva 27, Switzerland (Received 21 September 2004; accepted 22 November 2004) Abstract – Surveillance and control of emerging bacterial zoonoses is essential in order to prevent both human and animal deaths and to avoid potential economic disorders created by trade barriers or a ban on free circulation of human or animal populations. An increased risk of exposition to zoonotic agents, the breakdown of the host’s defenses, the emergence of bacterial strains resistant to antibiotics and their widespread distribution as well as conjunctural causes associated with the action or inaction of man have been identified as the main factors leading to the emergence or re- emergence of bacterial zoonoses. After an in-depth review of these various factors, the present manuscript reviews the main components of detection and surveillance of emerging or re-emerging bacterial zoonoses. A description of the systems of control and the main obstacles to their success is also presented. Detection and surveillance of emerging zoonoses have greatly benefited from technical progress in diagnostics. The success of detection and control of emerging bacterial zoonoses is largely based on international solidarity and cooperation between countries. emerging bacterial zoonoses / control / surveillance / factors of emergence Table of contents 1. Introduction ..................................................................................................................................... 508 2. Historical context ............................................................................................................................ 508 3. Factors of emergence or re-emergence of bacterial zoonoses ........................................................ 510 3.1. An increased risk of exposition to zoonotic agents ................................................................ 510 3.2. Breakdown of the host’s defenses .......................................................................................... 511 3.3. Emergence of bacterial strains resistant to antibiotics and their widespread distribution ..... 512 3.4. Conjunctural causes associated with the action or inaction of man ....................................... 512 * Corresponding author: bbchomel@ucdavis.edu ** Jean Blancou was General Director of OIE from 1991 to 2000
508 J. Blancou et al. 4. Surveillance systems .......................................................................................................................514 4.1. National or regional systems ...................................................................................................514 4.2. The world system ....................................................................................................................515 5. Methods of control ..........................................................................................................................516 5.1. Current methods ......................................................................................................................516 5.1.1. Sanitary prophylaxis ....................................................................................................516 5.1.2. Medical prophylaxis ....................................................................................................517 5.2. Obstacles for controlling zoonotic bacterial infections ..........................................................517 5.2.1. Main obstacles .............................................................................................................517 5.2.2. Some more specific difficulties ...................................................................................518 6. Conclusion .......................................................................................................................................519 6.1. Technical progress ..................................................................................................................519 6.2. Solidarity and international cooperation .................................................................................519 1. INTRODUCTION have recently been identified, giving a pre- cise etiology to diseases that were already At times when basic rules of hygiene known or whose zoonotic characteristics were not properly applied and vaccines nor were discovered or validated recently. This antibiotics had been discovered yet, bacte- is the case for numerous rickettsial infec- rial zoonoses such as bubonic plague, glan- tions (see [46]) or for the identification of ders, bovine tuberculosis and brucellosis the agent of cat-scratch disease, Bartonella caused more human deaths than they ever henselae, and other pathologies associated will again. However, the incidence and with this bacterium (see [7]). impact of some bacterial zoonoses appear to have been increasing over the last several decades and new bacterial zoonoses could 2. HISTORICAL CONTEXT arise. It is this latter possibility that is dis- In October 1347, human plague was cussed in most of the articles included in imported to Europe from the Orient during this special edition. However, in order to the siege of Caffa (Crimea, Ukraine) by the better understand these analyses, it is impor- Mongolians, when plague entered into the tant to set these emerging or re-emerging port of Messina, Sicily. It then spread to zoonoses within their historical context, to most of Occidental Europe, where 25 mil- explain what are the factors favorable to the lion people died in less than five years, that emergence or re-emergence of bacterial is one death for every three or four inhabit- zoonoses and how they are currently sur- ants [58]. In contrast, 36 876 cases of veyed and controlled, as well as the strength human plague (with 2 847 deaths) were and weaknesses of these surveillance sys- officially reported in 24 countries (11 in tems. Despite the considerable technologi- Africa, eight in Asia and five in the Amer- cal progress made during the last thirty icas) for the period 1987–2001. Although, years, there is still a risk of emergence of since the beginning of the 1990s an increase new bacterial zoonoses, notably those that in the incidence of human plague has been are foodborne. Food-borne zoonoses account observed, especially in Africa, none of for most of the emerging bacterial zoonoses these sporadic cases has caused a serious due to the globalization of food resources epidemic in these regions, or even a pan- and their worldwide distribution, which can demic [25, 59]. be illustrated by the emergence of Escheri- The reason for this progress is that cur- chia coli O157:H7 [10] or Salmonella rent methods of rapid specific diagnosis, the Enteritidis [54]. In addition, new bacteria establishment of a world epidemiological
Surveillance and control of emerging bacterial zoonoses 509 alert system, modern hygiene measures and positive culture results, M. bovis accounted the availability of efficient antibiotic treat- for 33.9% and M. tuberculosis for 66.1% of ments have completely modified the condi- the cases. This high percentage of M. bovis tions of development of bacterial zoonoses. infection was largely attributable to its con- The three following examples are an illus- tribution to extra pulmonary TB (55.2% of tration of these changes: all culture-positive specimens). Of course, – In 1887, Bruce was able to isolate in most human cases of tuberculosis are essen- goats raised on the Island of Malta the agent tially due to M. tuberculosis which caused that causes Malta fever (also known as bru- the death of 30 million humans between cellosis) in man, a disease which was wide- 1990 and 1999, mainly in developing coun- spread in the region at that time [43]. This tries where access to treatment is difficult discovery led to the prohibition, in 1905, of due to limited human and financial resources the consumption of raw goat’s milk. The [17]. In 2001, the incidence rate of tubercu- role of other animal species in the contam- losis in the world was still increasing at ination of man was shown later on, due to about 0.4% per year, but much more rapidly progress in bacteriology and serology. The in sub-Saharan Africa and in the ex-Soviet sanitary or medical control of animal bru- Union countries [60]. cellosis, according to the epidemiological – In 1890 again, the systematic use of mal- conditions and the resources of the infected lein was a revolution in the fight against country, has allowed to control or even equine glanders [3]. Discovered by Hel- eradicate the pathogenic agent reservoir in mann and Kalning (who died of the dis- many parts of the world [15]. This incon- ease), the bacilli extract plays the same role testable success of veterinary services has in the sanitary prophylaxis of glanders as led to a major reduction in the number of tuberculin for bovine tuberculosis control. human cases in most countries, even if bru- Its use allowed detecting and slaughtering cellosis is still a very common bacterial infected animals before they could contam- zoonosis in many parts of the world. inate other equines and/or humans. This – In 1890, the discovery of tuberculin by short historical background emphasizes the Koch, its use for the diagnosis of bovine considerable progress that has already been tuberculosis in cattle by Guttman and the made in the fight against bacterial zoonoses generalization of the method led by Bang, and the uncountable number of human lives Nocard or Johne were the basis for the erad- saved or protected due to such progress [6]. ication of the disease in Europe within a half The “resistance pockets” of bacterial zoon- a century [5]. Even before antibiotics became oses appeared therefore very reduced. How- available, this eradication had efficiently ever, over the last thirty to twenty years we reduced the risks of human tuberculosis of have been observing the emergence or re- bovine origin. However, a non-negligible emergence of several bacterial zoonoses [8, number of cases are still caused by bovine 56]. In most cases, these diseases are the bacilli excreted in the milk of infected cows, ones that humans have contracted either since 5 to 10% of human cases are caused when ingesting contaminated foods or by by Mycobacterium bovis [19, 45]. In a recent exposing themselves to wild bacterial res- review of tuberculosis (TB) in 563 children ervoirs or their vectors. Fortunately, these living along the United States/Mexico bor- infections produce fewer victims than in the der for the period 1980–1997, M. bovis caused past. The availability of antibiotic treat- 10.8% of all TB cases [18]. The yearly inci- ments has made their prognosis much less dence of pediatric tuberculosis cases began severe than that of zoonoses due to viruses rising in 1989 and peaked in the mid-1990s, or non-conventional transmissible agents, with Hispanics constituting 78.9% of the such as transmissible spongiform encepha- patients. Amongst the 180 patients with lopathies.
510 J. Blancou et al. 3. FACTORS OF EMERGENCE – Increased densities of production animal OR RE-EMERGENCE or wildlife populations, associated with OF BACTERIAL ZOONOSES modern breeding methods for domestic ani- mals: this has naturally favored the devel- The conditions for the emergence or re- opment of some pathogens such as Myco- emergence and spread of bacterial zoonoses bacterium bovis, Brucella spp. or Francisella still seem to be present at the beginning of tularensis [20, 21, 64]. In addition, the the XXIst century, even if the severity of increase in the number of pets in developed such infections seems to be less serious than countries and the increased interest for for many emerging viral zoonoses. Many exotic pets has led to the emergence of new national sanitary statistics have reported an viral and bacterial infections or parasitic infestations. The recent tularemia epidemic increase in the prevalence and the incidence detected in prairie dogs sold as pets under- of some bacterial zoonoses [11, 37, 38, 52], lines such an emerging risk [48, 49]. and the specific causes of such an increase are discussed by several authors in the – Human or animal population displace- ment (voluntary or not, notably following present issue [7, 10, 25, 46, 48, 54]. Indeed, socio-economic disorders) or translocation an ensemble of causes favorable to the mul- (game release, zoological Parks, wildlife tiplication and diffusion of zoonotic bacte- safari Parks), as well as changes in the activ- ria exist that can be identified for most of ity period of wild animals (diurnal/noctur- these zoonoses, as previously reported [8, nal) under the pressure of hunting [20, 40, 13, 26, 28, 38, 41, 52, 53]. However, it is 42] have direct effects on the emergence of useful to list them again for a better surveil- bacterial zoonoses. Increased contact between lance and control of the diffusion of the dis- human and livestock populations in Africa eases that they cause. have led to major health problems [32]. As reported by Kock et al. [32] “in recent 3.1. An increased risk of exposition years, the growth in livestock populations to zoonotic agents has slowed, owing to a cycle of degradation and disease, affecting especially traditional One of the principal causes of emergence pastoral systems with a close physical asso- or re-emergence is an increased risk of expo- ciation between people, livestock, and wild sure to certain pathogenic bacteria, depend- animals”. The recent outbreaks of M. bovis ing on different factors, such as: in wildlife in the Kruger National Park were likely the consequence of initial infection – Animal and human diet changes: thus, via an infected cattle herd [51]. A similar the number of human food-borne infections hypothesis was raised for the presence of due to the ingestion of pathogenic bacteria, tuberculosis in wildlife in the Donana such as Campylobacter, enterohemorragic National Park in Spain, since no cases of Escherichia coli (including E. coli O157:H7) tuberculosis were detected before the uncon- or Salmonella (in particular S. Enteritidis or trolled increase in the cattle population [1]. S. Typhimurium DT104) has considerably – Increased contacts with a wildlife reser- increased with the development of large voir, associated with the development of scale industrial food processing and the various outdoor leisure activities, such as development of fast-food restaurants. Food- hunting, fishing or tourism, especially eco- borne infections caused by zoonotic agents tourism may expose humans to bacteria have become more frequent throughout the excreted by healthy animal carriers, such as last decades [53]. As far as animal food is F. tularensis, Leptospira spp. and Bartonella concerned, the same is true for Listeria spp. [14, 48], or with arthropods that are monocytogenes carried by cattle ingesting vectors of bacteria, such as Borrelia burg- contaminated silage [61]. dorferi, responsible for Lyme disease or
Surveillance and control of emerging bacterial zoonoses 511 Coxiella burnetii, the agent of Q fever [24]. may provide an important economic benefit For instance, a high seroprevalence was through ecotourism, exposure to human detected for several zoonotic agents among pathogens may represent a health risk for hunters in Austria when compared to non- wildlife, as illustrated by outbreaks of hunter controls [24]. The high seropreva- M. tuberculosis, a human pathogen, in free- lence especially to Borrelia burgdorferi ranging banded mongooses (Mungos mungo) s.l., Ehrlichia spp., Leptospira interrogans, in Botswana and suricates (Suricata suri- E. granulosus, E. multilocularis, encepha- catta) in South Africa, which were recently lomyocarditis virus and Puumala virus reported for the first time [2]. demonstrated that hunters are particularly – Accelerated degradation of the natural exposed to zoonotic pathogens. This may environment, notably in developed coun- also be the case with Mycobacterium bovis, tries (by deforestation, building of dams, which is spreading to new wildlife reser- land consolidation) may cause wildlife spe- voirs, including wild carnivores, deer or cies to move to new areas, favoring their wild boars [20, 42]. Ecotourism can also be relocation in suburban zones, therefore a contributor to the emergence of new entering into contact with humans [12, 28, zoonotic diseases. Ecotourism has been one 40, 41]. This risk may also be created by of the fastest growing sectors of the tourism humans, when translocating some species industry with an annual growth rate of 10– in order to populate or repopulate a territory 30% and comprises about 20% of the world for fauna diversity or hunting purposes travel market (The International Ecotour- [42]. All species translocation (sometimes ism Society (TIES): Ecotourism statistical between continents) is accompanied by the fact sheet presented in: USDA-APHIS: stirring of infectious agents, which may Nature and Ecotourism: Animal and Human lead to unexpected exchanges of genetic Health concerns: October 2001. 10 pages. material. It seems that following such a stir- http://www.aphis.usda.gov/vs/ceah/cei/ ring, in the 1980s, a commensal E. coli of ecotourism.pdf). It can be a source of the human intestine acquired an aggravated human exposure to zoonotic agents [62]. pathogenic power therefore becoming vero- The increasing popularity of foreign travel cytotoxic (E. coli O157:H7), by exchang- and ecotourism places travelers at increased ing genetic material with a bacteria from the risk for some tick-borne diseases. During Shigella genus [53]. The same type of risk the last decade, some 400 cases of tick- can exist on farms, where the coexistence of borne rickettsioses have been reported in different animal species can facilitate the international travellers, the vast majority development of severe Salmonella and being African tick bite fever caused by Campylobacter infections [53]. Rickettsia africae and Mediterranean spot- ted fever caused by Rickettsia conorii. [31, – Global warming caused by human activ- 46]. From 1999 through 2002, 31 cases of ities is also a cause of concern in the emer- imported spotted fever-group rickettsioses gence of viral and bacterial vector-borne (SFGR) in United States residents reporting diseases. For instance, outbreaks of plague travel to Africa were confirmed by labora- have been associated with increased rainfall tory testing at the Centers for Disease Con- in both Africa and North America (see [25]). trol and Prevention [35]. Nineteen patients Similarly, an association was reported (61%) reported visiting South Africa prior between plague outbreaks and the El Nino to onset of illness [35]. Expansion of ecot- southern oscillations effect (see [25]). ourism-based industries, changes in land-use practices, and escalating competition for 3.2. Breakdown of the host’s defenses resources have increased contact between free-ranging wildlife and humans [2]. The second cause of the emergence/ Although human presence in wildlife areas re-emergence of bacterial zoonoses is the
512 J. Blancou et al. breakdown of the host’s defenses. This break- preceding onset of illness [29]. These authors down of the host’s defenses can be associated concluded that prudent antimicrobial agent with an immunodepression, either follow- use among humans and among veterinari- ing medication or infection caused by path- ans and food-animal producers is necessary ogenic agents capable of weakening the to reduce the burden of drug-resistant sal- host’s immune defenses allowing infection monellosis in humans. by opportunistic organisms. The best known example is that of the acquired Immunode- ficiency syndrome (AIDS) during which 3.4. Conjunctural causes associated certain bacteria, for which humans are usu- with the action or inaction of man ally healthy carriers, multiply to a level such that they lead to the death of their host At last, other conjunctural causes asso- [57]. This may explain in certain cases the ciated with the action or inaction of humans re-emergence of M. bovis or L. monocy- exist. togenes infections. Out of 225 cases of lis- – Humans could have contributed, and teriosis reported in France in 1997, 73% could still contribute to the re-emergence of were observed in immunodepressed indi- certain zoonoses. Zoonotic agents may be viduals, who for the most part were AIDS considered for deliberate release to cause victims [33]. harm, since they can simultaneously and adversely affect human and animal health 3.3. Emergence of bacterial strains [44]. Such attempts have been made or pro- resistant to antibiotics and their jected during the last two World Wars, but widespread distribution without any harm. For glanders (caused by Burkholderia mallei), the horses willingly Another cause of the increased incidence infected to cause an epizootic were not able of bacterial zoonoses is the appearance of to infect the opposite army’s horses, and for bacterial strains resistant to antibiotics and anthrax (caused by Bacillus anthracis) the their widespread distribution, following an people responsible for the attack finally did excessive usage or misuse in both human not dare to use the five million “anthrax and veterinary medicines. The existence of cakes” they had prepared [4]. However, these multi-resistant strains considerably Bacillus anthracis was recently used in the hinders the control of certain infections. United States of America, but without seri- They are often the consequence of an ous dispersal. The attack was mainly aimed increase in the number of these infections at specifically chosen persons, to whom a (largely nosocomial), which offer many letter was sent; but unfortunately some occasions for the appearance of resistant postal workers were also infected. mutants amongst zoonotic bacteria. This is certainly one of the explanations for the – The industrialization of food production emergence or re-emergence of food–borne for animals and humans followed by its pathogens such as Salmonella Enteritidis or worldwide distribution can also increase Typhimurium or by certain colibacilli. the risk of contamination. In humans, the A recent report indicated that compared number of infections due to food-borne with both control subjects and patients zoonotic agents has increased and has been infected with pansensitive strains of Salmo- maintained since the end of the last century, nella Typhimurium, patients with multid- despite the considerable progress in hygiene rug-resistant (MDR) S. Typhimurium infec- made during this period. For instance, in tion were significantly more likely to have 1997, 730 cases per one million inhabitants received an antimicrobial agent, particu- per year of salmonellosis were accounted larly an agent to which the Salmonella iso- for in the countries of the European Union, late was resistant, during the four weeks as well as 300 cases of campylobacteriosis,
Surveillance and control of emerging bacterial zoonoses 513 20 cases of yersinosis, 10 cases of brucel- their animals after the “Bovine Spongiform losis and 2 cases of listeriosis [53]. How- Encephalopathy crisis”, are good opportu- ever, even if it is impossible to obtain sta- nities for foxes, stray dogs, prey birds as tistics as precise for the previous decades, well as marauders, especially seagulls to it is probable that despite the lower number pick up and disperse pathogenic enterobac- of reported cases, their prognostic was teria or the agents of tuberculosis or brucel- then much more serious. Thus in France, losis [28]. For instance, the recent out- 124 persons died of bacterial gastro-intes- breaks of M. tuberculosis in free-ranging tinal infections in 1995 (to be compared banded mongooses and suricates in south- with 23 513 deaths caused by alcoholism!), ern Africa, as previously mentioned, were whereas a century earlier, 4 000 people died related to the proximity of garbage pits, of “typhoid fever” infection [39]. However, where banded mongooses were observed several of these so-called “typhoid fever” feeding regularly [2]. cases could have been unrecognized cases – The lack of coordination or harmoniza- of zoonotic Salmonella infection [39]. tion of control systems, when two neigh- – In some countries, the re-emergence of boring countries practice different methods bacterial zoonoses may be due to a lack of of prophylaxis, can be a factor of re-emer- surveillance or a lack of appropriate control gence. Thus a country practicing a rigorous measures associated with the breakdown of stamping-out strategy that succeeds in erad- public services [41]. This is caused more icating a zoonosis may have that zoonosis often by a lack of financial and human reappear at its border with a neighboring resources, which may be the consequence country that practices only limited sanitary of economic crisis, social uprising, wars or prophylaxis or no prevention at all. The natural disasters. The re-emergence of some case is well known for tuberculosis and bru- zoonoses, especially water or food-borne cellosis. zoonoses, is very often associated with an Another factor in the emergence or influx of refugees or insalubrity of poor dis- reemergence of bacterial zoonoses is the tricts in which the sanitary services can no impoverishment of some human popula- longer exercise a control. For instance, a tions amongst which all zoonoses can find large outbreak of tularemia was reported in suitable hosts due to poor hygiene. In devel- Kosovo in the early postwar period, 1999– oping countries, this impoverishment forces 2000 [50]. Environmental circumstances in some of these populations to move further war-torn Kosovo led to epizootic rodent into areas where animal reservoirs of poten- tularemia and it spread to resettled rural tial zoonotic agents exist, as reported for populations living under circumstances of retroviruses [63] or the Ebola virus [55]. As substandard housing, hygiene, and sanita- mentioned by Wolfe et al. [63]: “Contact tion. Professional risks also increase as soon with non-human primates, such as happens as governments lack resources to enforce during hunting and butchering, can play a hygiene or security standards in places such part in the emergence of human retroviruses as slaughterhouses or shelters, leading to an and the reduction of primate bushmeat hunt- increase in cases of brucellosis, Q fever or ing has the potential to decrease the fre- anthrax among professionals during certain quency of disease emergence”. periods or in specific countries. – Paradoxically, in other cases the risks are Environmental pollution may expose associated with the financial ease of upper wildlife species to causal agents of diseases social classes, which makes hobbies easier that they can then disseminate: open-air to practice, such as tourism, hunting, or fish- landfill sites, manure dispersal and more ing. By practicing these hobbies, people may recently the supplementary costs for breed- come in contact with potentially infected ers for the destruction of the carcasses of wild animals. The risk is even greater when
514 J. Blancou et al. new “exotic pets” are brought into their animal production sectors. These networks home. The danger of Salmonella being car- provide the collection and diffusion of infor- ried by reptiles has still not discouraged mation on animal diseases, some of which owners of turtles, iguanas or snakes [12, are zoonotic, affecting poultry, horses, fish 28]. As reported by Mermin et al. [36] in or wildlife. Their main objective is to pro- two case-control studies of human salmo- tect this type of commodity against the dis- nellosis occurring during 1996–1997 in the persal of contagious diseases by providing USA, “the population attributable fraction the professionals with all useful informa- for reptile or amphibian contact was 6% for tion on the situation of these diseases at all sporadic Salmonella infections and 11% national or international levels. The access among persons < 21 years old”. It is there- to these networks is generally restricted to fore estimated that reptile and amphibian professional members of that commodity exposure is associated with approximately and sharing with public health services is 74 000 Salmonella infections annually in seldom done, since they usually do not con- the United States. tribute financially to their start-up funding – For food-borne infections, the most unfa- or to their regular activities. vorable factor is the integration and glo- Since the recent occurrence of several balization of food treatment chains, which severe sanitary crises (notably associated multiply the risk of contaminations in an with bovine spongiform encephalopathy exponential way [53]. (BSE) in Europe), the necessity of a territo- rial “web” that allows rapid alert of national health authorities, has become evident to the 4. SURVEILLANCE SYSTEMS government of most countries. In response, most of them have created agencies or insti- 4.1. National or regional systems tutions that are specifically dedicated to set- ting up a specific surveillance network that The organization of regional or national reinforces or coordinates the action of the surveillance systems for bacterial zoonoses already existing services. However, the effi- is based on the analysis and synthesis of cacy of such surveillance systems may be information usually collected by official hampered by various obstacles. For instance, public health or animal health systems. one limitation of such systems can be the Data may be provided to health authorities increasing disinterest of medical practition- through partnership and networks organ- ers (both veterinarians or physicians) for ized with the help of medical practitioners, veterinarians, animal health and wildlife practicing in rural areas, which deprives specialists or livestock breeders grouped national authorities of a precious sanitary together for the sanitary defense of their observatory. Similarly, the disengagement livestock (for example, “Groupements de of the government (sometimes recommended Défense Sanitaire”(GDS) in France), as or requested by world financial organiza- developed in many countries by commodi- tions) in some developing countries has also ties, such as cattle farmer associations, egg led to the accelerated and counter-produc- producer associations. Such networks usu- tive privatization of health professionals. ally receive some financial aid form their A good example of annual surveillance government for setting prevention meas- of zoonotic diseases, including bacterial ures. zoonoses, at the national level is given by In some countries, this surveillance sys- the Swiss Zoonoses report 2003 (accessible tem may also be completed by the develop- on the Web at: http://www.bvet.admin.ch/ ment of some more confidential (and some- info-service/e/publikationen/magazin/2004/ times competing) networks, led by different 3_gesamt.pdf).
Surveillance and control of emerging bacterial zoonoses 515 However, only a limited number of Web However, this system is based only on active sites are available for surveillance systems surveillance for laboratory-diagnosed ill- of bacterial zoonotic diseases and most of ness. Similar sites have been developed in them relates to food-borne zoonoses. Here Europe for foodborne diseases, such as the are some examples of such sites. Salm-net network for human salmonellosis United Kingdom: the Health Protection (http://www.eurosurveillance.org). Agency has a specific section on zoonotic diseases (http://www.hpa.org.uk/infections/ 4.2. The world system topics_az/zoonoses/menu.asp) and zoonotic surveillance at its web site: http://www.hpa. The value of a worldwide network for org.uk/infections/topics_az/zoonoses/ zoonoses surveillance can only be the result zoo_surveillance.htm of that of national networks, since any inter- Ireland: http://www.fsai.ie/surveillance/ ference into the zoo-sanitary information of human/surveillance_human_zoonoses.asp a country is currently impossible without Netherlands (Netherlands Institute for the agreement of this country. The estab- Scientific Information Services): http:// lishment of such worldwide networks has www.niwi.knaw.nl/en/oi/nod/onderzoek/ still to overcome several obstacles. How- OND1287428/toon ever, such systems are important to be set France: http://www.invs.sante.fr/pub- in a more and more interdependent econ- lications/2002/def_priorite_zoonoses/ omy and are usually a booster for improving Within the European Union, recent direc- national systems. At the global level, there tives have also been set to establish are a number of recognized surveillance sys- Zoonotic diseases surveillance, especially tems, including the World Health Organiza- for bacterial food borne pathogens (see tion (WHO)-Global Outbreak Alert and Web site: http://europa.eu.int/scadplus/leg/ Response Network (GPHIN). The surveil- fr/lvb/f83004.htm). lance systems for food-borne diseases In the United States of America, differ- include Global Salmonella Surveillance ent networks are also available for bacterial (Global Salm-Surv), the SIRVETA system zoonoses surveillance either at the state (diarrhea syndrome surveillance) coordinated level (for example for California: http:// by INPPAZ (Pan American Institute for food www.dhs.ca.gov/ps/dcdc/disb/disbindex.htm) protection and zoonoses) which include coun- or at the federal level, mainly within the US tries from South America and the Caribbean) Public Health Services or the US Depart- (see web sites: www.panalimentos.org and ment of Agriculture. Specific sites for food- www.PAHO.org) or the EnterNet System borne diseases, including bacterial zoon- from WHO. For instance, Global Salm- oses (http://www.cdc.gov/foodnet/) or vec- Surv is a global network of laboratories and tor-borne bacterial zoonoses have been individuals under the WHO coordination developed by the federal Centers for Dis- involved in surveillance, isolation, identifi- ease control and Prevention (CDC) (http:// cation and antimicrobial resistance testing of www.cdc.gov/ncidod/dvbid/misc/bzb.htm). Salmonella. The methods used by these dif- Specifically, the Foodborne Diseases Active ferent surveillance systems may vary from Surveillance Network (FoodNet) is the prin- laboratory-based sentinel surveillance to cipal foodborne disease component of active and intensive epidemiological inves- CDC’s Emerging Infections Program (EIP). tigations, with sometimes an overlap in FoodNet provides a network for responding these various systems. to new and emerging foodborne diseases of Indeed, some countries have not been national importance, monitoring the burden able to or have not shown the willingness of foodborne diseases, and identifying the to set-up a regular surveillance of zoonoses, sources of specific foodborne diseases. and animal diseases in general. Others do
516 J. Blancou et al. have such a network, but screen the infor- of original data should be given to compe- mation collected, publishing only those that tent epidemiologists, equipped with an effi- have no risk to penalize their international cient computer and networking system. trade or their tourism industry. This strat- The diffusion of such data should first be egy may lead them to sell their animal prod- performed at a local level, in order to per- ucts at low cost to countries whose food manently motivate the people responsible shortage or political pressure forces them to for their collection. But they should also be take sanitary risks. Over recent years, a con- assured at the national level and beyond the siderable effort has been made to improve national borders, in order to inform the the passive system of collection of world international community of the evolution of zoo-sanitary information, in particular by developing an active system of collection at the zoo-sanitary situation in a specific region the Office International des Epizooties (OIE) and demonstrate the capacity of that coun- (www.oie.int), at the World Health Organ- try to follow the sanitary situation. ization (WHO) (www.who.int) or at the The “need” to sometimes keep under con- Food and Agriculture Organization (FAO) trol (often delayed reporting, sometimes (www.fao.org) of the United Nations. For lack of reporting, especially to international instance, FAO started in the mid 1990s the organizations) the diffusion of information surveillance system Empres early warning by health authorities can be explained by system (http://www.fao.org/ag/AGA/AGAH/ the political and financial consequences EMPRES). Specific agreements have been that can be attached to the announcement of signed between these organizations (for the first appearance of a deadly zoonosis. example http://www.oie.int/eng/OIE/accords/ Without willingly hiding the truth, some en_accord_fao_2004.htm). Some of these governments delay the first official report systems are shared between these interna- of this appearance on their territory, to the tional institutions, such as the FAO-OIE- detriment of the general interest. They thus WHO initiative called GLEWS (Global leave themselves the time to set-up a plan Early Warning System for trans-boundary for the control of the disease, to modify their animal diseases). The sources of informa- trade networks or to prepare their constitu- tion developed by these organizations are ents to such devastating news. not systematically and mandatorily validated by national authorities (e.g. the Empress bulletin of the FAO). Other sources of 5. METHODS OF CONTROL information include the Promed network developed in the United States, networks of Current methods used to control bacte- specialized information per region, by ani- rial zoonoses are mainly aimed at reducing mal sector production (in particular in avi- the burden of the zoonotic agent in its ani- culture and aquaculture) or by disease. The mal reservoir, or eradicating it, using the reports of non-governmental organizations classical methods of sanitary or medical (NGO) or laboratories in the private sector, prophylaxis. as well as articles published in the local press, can also be very interesting and use- ful information, even though these data are 5.1. Current methods not always validated. Once the data are collected, they must be 5.1.1. Sanitary prophylaxis used and diffused by competent and moti- vated persons. This is not always the case, Sanitary prophylaxis of zoonoses, which and it is not rare, in some countries, to consists in slaughtering and/or destroying observe a pile of reports on animal diseases all infected or contaminated animals (stamp- that have never been read. The exploitation ing-out method), has largely been proven
Surveillance and control of emerging bacterial zoonoses 517 useful for the control of bovine tuberculo- cial and human obstacles rather than tech- sis. Therefore, in many countries, humans nical limitations. are safely protected from any risk of con- The financial resources needed to effi- tamination by M. bovis. This same method ciently fight against zoonotic agents are not has succeeded or is in the process of suc- available for all countries. Only the inter- ceeding to also eradicate Brucella bovis or national community’s financial support, B. melitensis in many parts of the world. could, notably, allow developing countries However, this method reaches its own to organize a proper control of zoonotic dis- limits when wild animal reservoirs are con- eases, but it is rare that this is materialized cerned or when a disease is spread all over as a financial gift and mobilization of spe- the world. All hope to one day eliminate the cific funds, even by well-known interna- animal reservoirs of anthrax, tularemia, lept- tional organizations (such as WHO, FAO, ospirosis, or any other ubiquitous disease OIE), is limited for such diseases. Due to all seems vain. these difficulties, many sanitary authorities of these countries have given up the estab- 5.1.2. Medical prophylaxis lishment of such prevention programs. Oth- ers manage, with a lot of perseverance, to Medical prophylaxis of zoonoses, based elaborate complicated multilateral financial on either parenteral vaccination of animals arrangements. This allows punctual projects or on chemoprophylaxis, is usually more to be realized, but rarely to establish the expensive than sanitary prophylaxis on the long-term prophylaxis plans that they really long run and also prevents to achieve the need. eradication of the pathogen from its animal When financial and material problems reservoir, since some vaccinated individu- are supposedly solved, human-related dif- als can remain healthy carriers. Further- ficulties should not be underestimated. These more, it is often very difficult to differenti- difficulties can originate within the services ate antibodies produced by naturally infected in charge of applying the national prophy- animals and vaccinated animals based on laxis plans, when these services are not most serodiagnostic tests used for the detec- themselves convinced of the good use of tion of bacterial diseases. It is thus reduced these plans, or when they do not seem to get to a minimum in many industrialized coun- specific benefits from it. The obstacles tries (e.g. control of brucellosis), but it is sometimes result from a lack of cooperation still practiced in some developing countries between specific professional categories, where vaccination campaigns using inex- amongst which figure breeders, as well as pensive vaccines are still organized in order livestock brokers or even veterinarians to reduce the burden of zoonotic diseases such as brucellosis, anthrax or animal ery- bothered by the application of certain pro- sipelas, since financial efforts required for grams of control or the limited incentive eradication cannot be sustained. given by the health authorities for perform- ing prophylaxis tasks. Finally, the obstacle to such plans may be caused by the active 5.2. Obstacles for controlling zoonotic opposition of the public opinion to certain bacterial infections methods of control. This is notably the case for the hostility of some groups to the mass 5.2.1. Main obstacles slaughtering of animals during epizootics, or to the use of vaccines issued from genetic The main obstacles that are encountered engineering. By lack of an appropriate con- in the control of bacterial zoonoses are the sensus, the control of some zoonotic dis- same as those opposed to the control of any eases may simply be impossible in some infectious disease, that is most often finan- countries.
518 J. Blancou et al. 5.2.2. Some more specific difficulties els or goats, for example). In some of these countries, the development of a wide fraud Some more specific factors can also on veterinary pharmaceutical products can hamper an effective control plan, such as, also worsen this problem. – The availability of treatment for humans. – Administrative difficulties. Finally, some The fact that, on the contrary to zoonoses purely administrative difficulties can also due to viruses or non-conventional trans- complicate the control of some zoonoses. missible agents, bacterial zoonoses can be cured with an appropriate antibiotic treat- This is the case for the control of zoonotic ment can represent an obstacle to their con- diseases whose consequences are very trol. Indeed, in many countries, health author- severe for humans, whereas they have only ities are not giving a high priority to the a very negligible impact on animal hus- control of such zoonoses, since they know bandry or are considered as phenomena of that infected people can be treated. These natural regulation of wild populations. If same authorities will, at the same time, pay the Ministry of Health requires the Ministry less attention to prevention programs or to of Agriculture (or Environment) to cover in public information on the risk of zoonotic their own budget the expenses for a control bacteria. The overall result will be that program, it may become very difficult to deaths due to some bacterial zoonoses may find the resources necessary to conduct the be higher than those due to some viral dis- prophylaxis programs, since these pro- eases. grams will never be a priority within these – The existence of a wildlife reservoir. administrations. In several occasions, some Many pathogenic bacteria may find a ref- programs for zoonosis control (e.g. rabies, uge in wild species, in particular when their brucellosis, tularemia) have been aban- domestic hosts are protected by vaccination doned or severely reduced because the or chemo-prophylaxis. The control of the prophylaxis of foot and mouth disease was zoonoses that they cause immediately absorbing most of the budget allotted to the becomes more difficult, since the species veterinary services. Controlling the exist- are generally inaccessible to human inter- ing zoonoses, in some regions of the world, ventions. The strategies of sanitary proph- can also be added to these difficulties, as it ylaxis, founded on the limitation of these does not allow to investigate and to finan- populations, encounter technical and even cially support programs on new and emerg- more ethical problems. Oral vaccination ing zoonoses. The programs of control may strategies, which were able to eradicate be hindered by the existence of civil or mil- wildlife rabies in many European countries itary insecure zones, which prevent proper [47] and in North America [34], are only at management and the eradication of a zoo- the development stage for two bacterial nosis in the territories where their risks of zoonoses: tuberculosis [9], especially in development are at the highest. In other badgers [23], possum [16] and deer [30] and regions, the failure results from a disagree- brucellosis, in bison, elk or wild boars [22]. ment on the choice of the prophylaxis – A new emerging difficulty is becoming method to be adopted, notably when a apparent: the progressive unavailability of choice must be made between a sanitary some veterinary drugs illustrated by the prophylaxis and a medical prophylaxis. The progressive disappearance, due to the lack wealthy countries within a given region of a profitable market, of some drugs generally prefer the former strategy, which intended for the prevention or treatment of costs more but is more rapid and radical, existing diseases in some domestic animal whereas their neighbors with lower income species living in developing countries (cam- can only afford the latter.
Surveillance and control of emerging bacterial zoonoses 519 6. CONCLUSION nated animals have been developed, mainly for viral infections, but are starting to All political analysts agree today that the emerge for bacterial infections. The use of big challenge of the XXIst century will be to such vaccines allows to combine the sani- reduce the gap which is increasing between tary and medical methods of prophylaxis the rich and poor countries of the planet in for some zoonoses, such as brucellosis. the interest of everyone. This seems to be Research on oral vaccination methods especially true for the health sector. Hope- against zoonoses carried by wildlife has fully, favorable factors for the development already allowed obtaining spectacular suc- of a better surveillance and more efficient cess in the eradication of rabies, and they control of zoonotic diseases, including bac- are promising for the control of tuberculosis terial zoonoses, currently seem to override and brucellosis in wildlife. many unfavorable factors. Notably, two of In the field of food hygiene, a more rig- these favorable factors allow much opti- orous control of production chains or trans- mism concerning the prevention and con- formation of food based on the Hazard trol of bacterial zoonoses. Analysis Critical Control Point (HACCP) method has considerably reduced the risk of 6.1. Technical progress food-borne bacterial infections. More in- depth genetic analysis of bacterial isolates The surveillance of bacterial zoonoses also allows tracing back the origin of these has been facilitated and boosted by the infections, sometimes avoiding their diffu- development of many biological tests and sion from a common source. benefited from the molecular biology rev- olution, which has successively made tests, such as ELISA serology, the use of mono- 6.2. Solidarity and international clonal antibodies, and finally gene amplifi- cooperation cation, using the polymerase chain reaction (PCR) available to health authorities. The An international concerted control has introduction of these techniques has made better chances to succeed than when organ- diagnostics become more rapidly available ized only at regional or national levels, at a lower cost and with a higher accuracy since it reduces prophylaxis costs, and spe- and precision. They also allow, in many cifically improves the overall results by cases, the traceability of contamination, thus avoiding new contamination of one country avoiding new outbreaks. Such progress by another. In addition, international coop- allowed, during the last decade, in associa- eration programs may more easily receive tion with standard virus isolation, the very financial, material or technical aid than with rapid identification of very severe viral national programs and they can benefit zoonoses, such as the Hendra virus in horses from the advice of the best international in Australia, Nipah virus in humans and experts. Their existence largely encourages pigs in Malaysia or the severe acute respi- all participating countries, which are much ratory syndrome (SARS) in the People’s more active in this collective work since the Republic of China and the recognition of results are better recognized, or even the emergence of bacterial zoonoses such as rewarded, at the international level. Lyme disease [27] or rickettsial zoonoses As we stated in the introduction, it is [46]. clear that bacterial zoonoses do not present Similarly, the control of such zoonoses the same danger today as they did a century has benefited from very important techno- ago. The development of hygiene and asep- logical progress that has been made in recent sis and then the discovery of vaccines, and years. Vaccines with serological markers later of sulfones and antibiotics, have ended distinguishing between infected and vacci- the ancestral scare of bubonic plague, or
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