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Filovirues

by Dr. Richard J. Hatchett, MD

Summary of available data pertaining to nonhuman primate-to-human transmission of filoviruses: 1) Both Ebola and the related virus Marburg appear to be pathogenic in all species of primates. Although primates are thought not to be a primary reservoir for filoviruses, nonhuman primate-to-human transmission of the Ebola and Marburg viruses has been documented on four occasions: in the original outbreak of Marburg Virus in Germany and Yugoslavia in 1967, when vervet monkeys captured in Uganda infected 30+ labworkers; in the Reston, Virginia outbreak of 1989, when four quarantine workers appear to have been infected by Ebola-Reston while handling infected macaques from the Philippines; in the single human infection with Ebola-Cote d'Ivoire, which occurred in November 1994 after an ecologist at the Tai Forest National Park in western Cote d'Ivoire became infected after performing an autopsy on an infected chimp; and in the Mayibouth II outbreak in norheast Gabon at the end of January 1996, when 20-22 villagers became infected after cleaning and cooking a chimp found dead in the forest by some teenage boys (the resulting epidemic led to infection of a total of 37 individuals). Ebola, which replicates in the dermis of infected primates, can now be diagnosed using an inexpensive skin biopsy kit available from CDC and appears to be transmissible via skin-to-skin contact. Animals suspected of being infected should obviously be treated with extreme caution. In human-to-human infections, contact with body fluids does not appear to be necessary for transmission to occur.

2) Primate deaths have been temporally associated with at least three human epidemics -- in the autumn 1996 Booue, Gabon outbreak, when virus was isolated from a chimp found dead near Booue; and anecdotally from the aforementioned Mayibouth II outbreak and a previous outbreak at Minkouka, Gabon in December, 1994 (this latter outbreak was identified only retrospectively, but inhabitants near Minkouka recall finding dead chimps and gorillas in the forest at around the same time). Chimp dieoffs were observed in the Tai Forest during August, September and October of 1992 and November of 1994 and both are now attributed to filovirus infection, although so far as I know the first outbreak was never confirmed serologically. We heard rumors of unusual primate deaths near Mekob, a village of the Ivindo river basin, which were supposed to have occurred in August 1997 but after following up on these came to the conclusion that the informing source was unreliable.

Interestingly, all the primate deaths have occurred at the end of the local rainy seasons or during the dry season. The Minkouka outbreak occurred in December of 1994, when rainfall recorded at Makokou, the nearest weather station showed an unusually early and sharp decline of precipitation after the long rainy season; the Mayibouth II outbreak occurred at the end of the long rainy season, again during an unusually dry period (based on records at Makokou); and the Booue outbreak began in the summer of 1996, during the dry season. The two chimp dieoffs in the Tai Forest occurred at the end of the rainy season. I think this may be a very important clue as to the identity of the reservoir species, though no one I've talked to knows exactly what to make of it.

Some researchers have speculated that the reservoir species is one that habitually confines itself to relatively inaccessible places, such as the rain forest canopy, and that certain species of primates, perhaps because of hunting or foraging strategies, may inadvertently place themselves at risk of exposure to the reservoir species and thus to the virus. Another interesting fact is that certain species of insectivorous and frugivorous bats have been experimentally infected with Ebola-Zaire, the most lethal of the filoviruses, and found to suffer no ill effects (although the virus replicates and the bats secrete infectious particles in body fluids, feces, etc.). It's a leap but this just MIGHT imply adaptation of virus and bat to each other, for whatever reason, either because bats are the reservoir species or because they frequently run into the virus because of what they do or eat.

My question to the readers of Primate Talk: can you think of any ways in which the nocturnal activities of primates or their hunting and foraging strategies change during periods of relative aridity? What might they be exposing themselves to at the end of the rainy season or during the dry season that so far as we know they don't encounter at other times?

With respect to these questions, please bear in mind an observation of Dr. Greg Laden of the Department of Anthropology of the University of Minnesota. Ebola infections have now been documented on both sides of the Congo and Cross Rivers and on either side of the "Dahomey" gap, all of which are important biogeographic barriers. Moreover, viral circulation seems to occur only in ecosystems with annual dry seasons of greater than 60 days duration.

3) Given the widespread consumption of primates in Central Africa and, again so far as we know, the relative rarity of filovirus outbreaks, the risk of nonhuman primate-to-human transmission of filovirus infections must be vanishingly low. Villagers and Baka pygmies whom we interviewed in Gabon in the company of Dr. Barry Hewlitt, a medical anthropologist with an interest in local explanatory models of hemorrhagic fevers, revealed that although traditional models of witchcraft were invoked to explain the outbreaks, the actual symptom complex presented by filovirus infections was previously unfamiliar. This may indicate that viral transmission to human communities, at least in northeast Gabon, is occurring with a recently increased frequency. Why viral circulation would have increased in this remote area, where traditional cultures are largely intact, human population densities extremely low, and the rain forest in remarkably good shape, is entirely unclear.

4) Although hemorrhagic fevers remain more of a curiosity than a genuine public health threat, there are other reasons, obviously, to be concerned about nohuman primate-to-human transmission of viruses. The best object lesson, of course, is HIV (the first human case of which has been definitively backdated to 1959, in Zaire -- there was a recent article about this in the New York Times), but there is also monkeypox, which is related to the smallpox virus, caused a significant outbreak in Zaire last year, and even provoked discussion on Pro-MED about revaccinating persons at risk with the smallpox vaccine, which affords protection against monkeypox; Herpes B virus, which fatally infected a college student at Emory last year (thanks to Dr. Janette Wallis for reminding me of this case); and no doubt others.


Richard J. Hatchett, MD
Department of Medicine
New York Hospital - Cornell Medical Center
Newe York, NY 10021
E-mail: rhatchet@nyhs.med.cornell.edu