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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�

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                                              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
520                                         J. Blancou et al.

more insidious dangers such as glanders,                   tuberculosis in wildlife reservoirs, Vet.
tuberculosis or brucellosis, despite some                  Immunol. Immunopathol. 74 (2000) 1–16.
recent fears from bioterrorism threats.               [10] Caprioli A., Morabito S., Brugère H., Oswald
                                                           E., Enterohaemorrhagic Escherichia coli:
    Even though the emergence factor that is               emerging issues on virulence and modes of
to be the most feared today for bacterial                  transmission, Vet. Res. 36 (2005) 289–311.
zoonoses is the resistance of bacteria to             [11] Childs J., Shope R.E., Fish D., Meslin F.X.,
antibiotics, medical and veterinary author-                Peters C.J., Johnson K., Debess E., Dennis D.,
ities should remain extremely vigilant con-                Jenkins S., Emerging zoonoses, Emerg. Infect.
cerning emerging bacterial zoonoses.                       Dis. 4 (1998) 453–454.
                                                      [12] Chomel B.B., New emerging zoonoses: a
                                                           challenge and an opportunity for the veteri-
                                                           nary profession, Comp. Immunol. Microbiol.
ACKNOWLEDGEMENTS                                           Infect. Dis. 21 (1998) 1–14.

    The authors would like to thank Wendy             [13] Chomel B.B., Control and prevention of
                                                           emerging zoonoses, J. Vet. Med. Educ. 30
Brand-Williams, Station de Génétique Quanti-               (2003) 145–147.
tative et Appliquée, INRA, Jouy-en-Josas (France),
for translating the manuscript into English.          [14] Chomel B.B., Kikuchi Y., Martenson J.S.,
                                                           Roelke-Parker M.E., Chang C.C., Kasten
                                                           R.W., Foley J.E., Laudre J., Murphy K., Swift
                                                           P.K., Kramer V.L., O’Brien S.J., Seropreva-
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