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Ebola and Great Apes in Central Africa: current status and future needs.

Bull Soc Pathol Exot, 2005, 98, 3, 237-238 237

Z

oonotic diseases, pathogens that transcend the “Darwi- nian divide”, have been in existence for as long as humans and animals have walked the Earth. Through the centuries, diseases such as the bubonic plague, rabies, anthrax, tuber- culosis, rift valley fever, and salmonellosis, have crossed from the animal world to the human realm. Recently, zoonosis have captured international attention as SARS and Ebola outbreaks take their toll on human populations around the world. Ebola Hemorrhagic Fever Virus (EHFV) is only one of a hundred infectious agents that humans and great apes share in common.

Ebola has been known to the scientific and medical com- munity since it was first identified in 1976 (1, 7). Since that time it has entered into human populations at least a dozen times in six different countries of Equatorial Africa. The most recent epidemic in Central Africa made headlines as gorilla (Gorilla gorilla), chimpanzee (Pan troglodytes) and human populations were hard hit (11). In a small area in Northwest Republic of Congo, this devastating disease killed over 130 humans and was estimated to have killed approximately 600 great apes from a population of roughly 1200. Entire family groups of gorillas and chimpanzees could not be found during and following the outbreak. This was associated with EHFV, which was confirmed by laboratory testing of samples collec- ted from gorilla carcasses. Some family groups of gorillas sur- vived even after members in the group died of EHFV. Though caused by a different strain of EHFV, this is consistent with

observations in chimpanzee mortalities due to EHFV in the Côte-d'Ivoire, where some family group members died and others did not (2).

The worst-case scenario for EHFV in great apes may have been demonstrated in the Minkebe forest region of northeas- tern Gabon where lowland gorilla and chimpanzee popula- tions have come close to disappearing during the period of the human EHFV outbreaks in 1994 and 1996 (3). Up to tens of thousands of gorillas and chimpanzees may have died due to EHFV. Unfortunately, no one was working in the forested areas during the human outbreak periods to collect either samples or observations on wildlife to determine conclusively if or how EHFV affected the ape populations.

Proceeding the 2002/2003 outbreaks, the Wildlife Conser- vation Society and ECOFAC had been working together to train national park and protected areas management staff in the Republic of Congo and the Republic of Gabon in wildlife censusing techniques, wildlife health monitoring techniques, post-mortem examinations and standardized data collection methods with proper biosecurity procedures. Diagnostic capabilities were provided by the International Center for Medical Research Franceville (CIRMF). These efforts have resulted in the collection of samples proving mortality of gorillas due to EHFV, direct genetic linkages of the virus in great apes with human outbreaks, and evidence of multiple, genetically different EHFV types circulating in the forest

E bola and great apes in Central Africa:

current status and future needs.

Résumé : Le virus Ebola et les primates anthropoïdes en Afrique centrale : état actuel et besoins futurs.

La communauté scientifique et médicale a appris l’existence du virus Ebola lors de sa première iden- tification en 1976. Depuis ce jour, le virus est passé chez l’homme au moins une douzaine de fois dans six pays différents de l’Afrique équatoriale. L’épidémie la plus récente fit les gros titres : gorilles, chimpanzés et populations humaines étaient durement touchés. Suite aux épidémies 2002/2003, la Wildlife conservation society et l’ECOFAC ont travaillé ensemble pour former le personnel de direc- tion du parc national et des zones protégées en République du Congo et République du Gabon, formation intégrant les techniques de recensement des animaux sauvages, ainsi que les techniques de surveillance sanitaire, les autopsies et les méthodes de collecte de données standardisées.

Ces équipes qualifiées, mises en place pour prévenir les prochaines épidémies de fièvre hémorragi- que due au virus Ebola, ou autre maladie, et la mise en relation toute aussi indispensable entre les villageois du coin et les chasseurs, ont permis aux équipes de terrain de détecter et de rendre compte de la mortalité chez le grand singe causée par le virus Ebola, des mois avant les premiers cas chez l’homme. L’évaluation des cas répertoriés en période d’épidémie d’Ebola en Afrique centrale a mon- tré qu’il existe un rapport avec la manipulation des gorilles ou des chimpanzés infectés par le virus Ebola. En diminuant la fréquence de cet itinéraire de contact par le biais de programmes éducatifs et de systèmes d’alerte précoce, cela pourrait réduire l’incidence d’épidémies chez l’homme tout en réduisant l’impact sur la chasse des populations de gorilles et chimpanzés.

W. Karesh & P. Reed

Field Veterinary Program Wildlife Conservation Society, 2300 Southern Blvd. Bronx, NY, 10460 USA.

Tel. : 718-220-5892 , Fax : 718-220-7126, E-mail : wkaresh@wcs.org

Courte note n° 2761-1. “Atelier sur les fièvres hémorragiques virales”. Reçue le 21 janvier 2005. Acceptée le 24 mai 2005.

Ebola zoonose gorille chimpanzé primate anthropoïde Afrique intertropicale

É COLOGIE

Ebola zoonotic disease gorilla chimpanzee great ape Sub Saharan Africa

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Écologie 238

W. Karesh & P. Reed

at the same time (4), suggesting the possibility of multiple reservoir species or a guild of species. Due to these trained teams being in place in anticipation of the subsequent EHFV epidemics or another disease event, and equally essential, esta- blished relationships with local villagers and hunters, field teams were able to detect and report great ape mortalities due to EHFV weeks to months before the first human cases (9). In the last decade, assessment of EHFV outbreak index cases in Central Africa have shown a link with the handling of either EHFV infected gorillas or chimpanzees (4). Reducing the frequency of this contact route could reduce the incidence of human outbreaks as well as reduce the impact of hunting on gorilla and chimpanzee populations.

Work is still underway to identify the natural reservoir of EHFV. Laboratory experiments have shown not only that some species of bats (Chiroptera) can survive infection with EHFV, but the virus was observed to replicate in their blood and they shed the organism in their excrement, though stu- dies were not continued beyond 30 days (10). Field work in the Central African Republic has found at least fragments of EHFV particles using PCR genetic techniques in a number of rodent species (6), and similar work in the Republic of Congo has found similar results in bats (E. LEROY, pers. com., 2004). At least one black-blacked duiker (Cephalophus dor- salis) also tested positive for EHFV by PCR, and an indirect observation of an approximate 50% decline in duiker popu- lations during an EHFV outbreak in Congo (4, 9) and reports from local hunters of increased mortality observations adds another piece of information to the puzzle. Forest duikers, while generally herbivorous, are noted as ungulates for their predilection for frugivory and also for occasional carnivory or scavenging which would put them in multiple behavioural categories overlapping with gorillas, chimpanzees and humans living in the same forests. In all cases, caution must be taken when interpreting PCR findings since these sensitive techni- ques determine only the presence of the genetic material but do not indicate live or viable virus. Other studies have shown the presence of antibodies, indicative of previous exposure and immune responses, in apparently healthy humans and primates in the Central African region (5, 6).

The scientific evidence to date suggests that EHFV is wides- pread in Equatorial Africa and persists in nature between observed outbreaks. At this time, the conditions in which the virus passes from its natural host or hosts, where it likely causes minimal disease problems at the population scale, to inadvertent host species which have lower survival rates are unknown. The rate of individual to individual spread of the disease in non-human species is also poorly understood.

MORVAN et al. suggest that rather than being a virus of deep forest refugia, EHFV is actually more common in forest peri- pheries, fragments and mosaics (6). That observation could stem from the preferred habitats of the potential reservoir species or could be descriptive of the type of habitat in which transmission events among the reservoir species and other species are more likely to occur. Changes in climate or vegeta- tion patterns with resultant changes in ecological relationships of animal populations may stimulate the transfer of the virus among species as is seen with other viral diseases. Though a mechanism has not been identified, correlations of EHFV outbreaks in humans with greater than average variance in climate and/or vegetation changes has been reported by PIN-

ZON et al. (8).

In order to better understand the disease caused by EHFV and develop methods to prevent its spread both in humans and wildlife (as well as understand and prevent the effects of other diseases on great apes) the following objectives need to be addressed:

1) anticipate EHFV outbreaks and populations at risk in order to provide better support to areas that could be affected by the virus;

2) establish monitoring teams to determine the existence and progression of the EHFV and other serious infectious disease agents in the forest, and their impact on wildlife (affected spe- cies, mortality rates and resistance, natural barriers, etc.);

3) establish response plans to alert appropriate people to fin- dings of the presence of EHFV and other diseases;

4) improve knowledge of the EHFV and its ecology (reser- voir, mode of transmission inter and intra-specific, strains, immunity, etc.);

5) evaluate ways of reducing the effect of EHFV and other infectious diseases on great apes using techniques such as vaccination programs, separation of reservoir species and affected species in time and space, meta-population manage- ment approaches, and other preventive medicine and hygiene practices.

6) using EHFV as an example of disease risks, improve local community education and awareness campaigns to reduce human contact with great apes and reduce hunting of great apes.

Références bibliographiques

1. Anon. Ebola haemorrhagic fever in Zaire, 1976. Bull Org Mond Santé, 1978, 56, 271-293.

2. FORMENTY P, BOESCH C, WYERS M, STEINER C, DONATI F et al. - Ebola virus outbreak among wild chimpanzees living in a rain forest of Côte-d’Ivoire. J Infect Dis, 1999, 179 (Suppl 1), S120-S126.

3. HUIJBREGTS B, & DE WACHTER P - Ebola and the decline of gorilla Gorilla gorilla and chimpanzee Pan troglodytes populations in the Minkebe Forest, north-eastern Gabon.

Oryx, 2003 37, 437-443.

4. LEROY EM, ROUQUET P, FORMENTY P, SOUQUIERE S, KIL- BOURNE A et al. - Multiple Ebola virus transmission events and rapid decline of Central African wildlife. Science, 2004, 303, 387-390.

5. LEROY EM, TELFER P, KUULUNGUI B, YABA P, ROUQUET P et al. - A serological survey of Ebola virus infection in Central African nonhuman primates. J Infect Dis, 2004, 190, 1895- 1899.

6. MORVAN JM, DEUBEL V, GOUNON P, NAKOUNE E, BARRIE- RE P et al. - Identification of Ebola virus sequences present as RNA or DNA in organs of terrestrial small mammals of the Central African Republic. Microbes and Infections, 1999, 1, 1193-1201.

7. PETERS CJ & LEDUC JW - An introduction to Ebola: the virus and the disease. J Inf Dis, 1999, 179 (Suppl 1), S170-S176.

8. PINZON JE, WILSON JM, TUCKER CJ, ARTHUR R, JAHRLING PB & FORMENTY P - Trigger events: Enviroclimatic coupling of Ebola hemorrhagic fever outbreaks. Am J Trop Med Hyg, 2004, 71, 664-674.

9. ROUQUET P, FROMENT JM , BERMEJO M, KILBOURNE A, KARESH W et al. - Wild animal mortality monitoring in Gabon and Republic of Congo (2001-2003): results and implications for the prevention of human Ebola outbreaks.

Emerg Infect Dis, 2005, 11, 283-290

10. SWANNEPOEL R, LEMAN A, BURT F, ZACHARIADES NA, BRAACK LEO et al. - Experimental inoculation of plants and animals with Ebola virus. Emerg Infect Dis, 1996, 2, 321-325.

11. VOGEL G. Can great apes be saved from Ebola? Science, 2003, 300, 1645.

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