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Ebola Virus Outbreak among Wild Chimpanzees Living in a Rain Forest of Cote d’Ivoire. Erin Goode. Introduction. ~25% of a 43 member troop of wild chimpanzees disappeared or were found dead in the Tai National Park, Cote d’Ivoire
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Ebola Virus Outbreak among Wild Chimpanzees Living in a Rain Forest of Cote d’Ivoire Erin Goode
Introduction • ~25% of a 43 member troop of wild chimpanzees disappeared or were found dead in the Tai National Park, Cote d’Ivoire • In November 1994, primatologists studying the chimp community in the park found 8 dead chimps, and absences of many others • Epidemiologic survey was done to discover the cause of death
con’t • This is the first outbreak of Ebola to be described in the wild • This article discusses the results of investigations leading to the identification of a new subtype of the Ebola virus (EBO-CI) in chimpanzees
Background: Tai Chimps • Tai National Park is the largest and last remnant of the tropical rain forest belt in West Africa (436,000ha) • Since 1979, wild chimpanzee troop has been studied in the National Park • The home range of these chimpanzees is ~27 square km, and located in the western park of the park. • A similar outbreak of Ebola also occurred in November 1992 among same chimp troop
Location of October-November 1994 Ebola outbreak among chimps
Background:Ebola virus • Ebola (EBO) epidemics occurred in the Democratic Republic of Congo (DRC) and Sudan in 1976 • Investigations did not find the virus in insects or mammals • EBO caused one lethal case in DRC in 1977 and an outbreak in Sudan in 1979 • A new subtype of EBO (subtype Reston: EBO-R) occurred in a cynomolgus monkeys colony at a quarantine facility in Reston, Va in 1989
con’t • EBO-R was responsible for 3 other outbreaks in monkeys in the USA in 1990 and 1 in Italy in 1992 • Investigations traced the source of these EBO-R outbreaks to a primate exporter in the Philippines • The mode of contamination of this facility has not been determined
Materials and Methods:outbreak investigation • A case of Ebola infection- a chimp from the community who was missing or found dead during Oct, Nov, or Dec of 1994 • A definite case- a dead chimp with a confirmed presence of EBO virus via laboratory testing • A probable case- a chimp whose dead body was found • A possible case- a chimp who went missing, with a unexplained disappearance
con’t • Cases identified from daily records of investigators • Date of onset- the first day clinical signs were recorded in the chimpanzees (2 cases) or day of disappearance (10 cases) • This is based on the presumption that chimps isolate themselves after they feel sick • Date of death determined from the condition of the body
Materials and Methods:epidemiologic investigations • Study done with data available from surveys in Park with the troop since 1979 for identifying risk factors for cases • Study from October to December 1994 • Presence and physical status of all chimps recorded on a daily basis • Behaviors noted: sexual activity of females, duration of meat consumption (min) in hunting season, and situation of group
con’t • All social interactions with cases recorded, including: grooming, behavior while discovering dead bodies, and behavior with sick animals • Contact chimp- any chimp observed with direct contact with a case-chimp, during period between 2 days prior to the onset of symptoms and death of the case
Materials and Methods:specimen collection • 2 necropsies were conducted in field in November 1994 • First necropsy done by investigators not aware of proper sampling methods- samples not usable for classic microbiologic testing • Second necropsy- samples of kidney, spleen, lung, liver, lymph nodes, and intestinal tissue collected from a 45 month old female for histologic and bacteriologic studies. Not tested for viruses
con’t • Blood specimens taken from 3 live chimps during 1st week in Dec. 1994 for complete blood cell counts and serologic tests • Blood smears prepared from blood to look for malaria or trypanosome parasites
Materials and Methods:laboratory studies • Tissues fixed and embedded in paraffin wax • 4m sections stained with hematoxylin, eosin, and saffron • Immunohistochemistry studies done using a pool of monoclonal antibodies known to cross-react with subtypes of EBO • Mouse polyclonal antibodies prepared with EBO-CI and EBO were also used in immunohistochemical tests • Part of each tissue sample used in bacteriologic investigations
con’t • Platelet, leukocyte, RBC, and WBC counts determined • Hemoglobin and hematocrit levels determined • ELISAs done to identify presence of IgG and IgM antibodies for Rift Valley and Crimean-Congo hemorrhagic fever viruses, hantaviruses, chikungunya, yellow fever, and dengue viruses • ELISAs for IgG and IgM antibodies against EBO and EBO-CI viruses also tested
Results:epidemiologic investigation • Beginning of October 1994 chimp community had 43 individuals: 13 infants, 4 young adults, and 26 adults • From October to December- 12 members died or went missing • Of these: 1 definite EBO case, 7 probable cases, 4 possible cases • None of other 4 missing chimps seen since outbreak
con’t • Of 12 cases, included 2 infants (virus attack rate = 15%) and 10 adults (attack rate = 38%) • No significant differences in attack rates between males and females • Attack rates highest among adults • Mothers of both infant cases also died or disappeared • First case of EBO recorded on Oct. 25, 1994 with last on Nov. 27th • Geographic distribution of dead chimps shows clustered distribution in most commonly used area of the territory
Results:risk factors • Activities involving case-contact were not significant risk factors. Including touching dead chimps or grooming a case patient • Infants had a very high risk factor when their mother was an EBO case • Chimps engaging in sexual activity from Oct to Nov had a relative risk of 2.5 • Chimps who consumed meat had a relative risk of 5.2, the risk increase with quantity of meat ingested
Results:observations • Before outbreak, chimp group fed on fruit from 1 fig tree from Oct 10-19 • Pigeons seen feeding on same tree everyday • Chimps seen hunting twice from Oct to Nov • First hunt occurred 7 days before outbreak- young red colobus monkey killed and eaten • 2 main consumers of monkey were among early cases • Last 2 cases fed on adult red colobus 11 days before disappearing
Results:histopathology • Liver lesions contained many small sites of necrosis • Spleen showed extensive areas of necrosis in the red pulp • Single, large, inclusion bodies in cytoplasm of macrophages of red pulp of spleen, some hepatic Kupffer cells, and hepatocytes • In mesenteric lymph node, cortical pulp showed pyknosis and necrosis of centrofollicular areas
con’t • Several macrophages in lymph nodes contained big inclusion bodies- that were compatible with viral inclusions • EBO-specific immunohistochemistry of liver, spleen, lymph nodes, and lung positive • Large distribution of virus in all organs • Mf, esp. vascular Mf, in spleen and liver were the immunopositive cells • Bacterial cultures and serologic tests for Rift Valley, Crimean-Congo fevers, and chikungunya, hantaviruses negative
con’t • 3 live chimps had IgG but not IgM antibodies against yellow fever and dengue viruses • 3 live chimps sampled had no antibodies against new subtype EBO-CI
Discussion • Immunohistochemistry diagnosed EBO infection in 1 chimp who died in Nov 1994 • During this epidemic, the other dead and missing most likely died from same pathogen • Findings indicate a short illness followed by sudden death • 3 surviving chimps with high risk factors for EBO, from eating meat, were negative for EBO-CI • Indicates they were never infected- supports idea that case fatality rate is near 100% in infected
con’t • Lesions described similar to lesions observed in experimentally infected monkeys • Contrary to reports of naturally infected humans and experimentally infected monkeys- no hemorrhagic, thrombotic, or vascular lesions present • But pathologic features of EBO-CI could be different from other EBO infections • Results of risk factors are compatible with dissemination patterns in human EBO outbreaks
Discussion con’t • Chimps not at risk for EBO-CI from touching or grooming infected animal • But very close contact is a risk factor, like sexual activities (low risk) or mother-infant contact (high risk) • During this outbreak, infection seemed to have originated from a point source and spread through community • Data shows that highest risk factor for infection was meat consumption between Sept and Oct
Discussion:Colobus connection? • Chimpanzees may be infected from eating their prey- 85% of which is red colobus • 1st colobus hunted could have been cause for early cases, and 2nd colobus for last 2 • But last 2 infected were in contact with the definite case and therefore may be secondary cases • If colobus are EBO source and carriers, epidemics should occur throughout year/hunting season but it does not
Discussion:Colobus con’t • Red colobus are widely distributed in Tai Forest, 1/3 of monkeys in Park • Colobus may be intermediate hosts, being contaminated at the true reservoir in Oct-Nov at end of chimpanzee hunting season • Red colobus are strictly vegetarian spending most of time in canopy and emergent trees • Their niche might be where EBO virus reservoir goes into hiding • Could be contaminated via virus in food, other animals, or contact with small mammal secretions
Discussion:Fig tree of death? • Before beginning of outbreak, chimp community spent large amounts of time in a fruiting fig tree (F. goliath) • Observers saw many birds in the tree during day, and argue that rodents, fruit bats, and other species were feeding there at night • This fig tree was a focal point for many species and could have allowed transmission of the virus between species
Discussion:the human role • Habitat has been constantly modified by human migration from northern regions of the forest belt • Process has increased dramatically over last 6 years since start of Liberian civil war • Influx of refugees doubled local populations from early 1992 to early 1993, then again in 1994 • Causes increased deforestation –crop activities and poaching in the park, leading to a large farmland and broken forest only 2km from chimp home range
Discussion:results of human interference • Emergence of infectious diseases are often linked to ecologic changes • Environmental and climatological disturbances recorded in Tai could have combined to change parts of the EBO reservoir or parts of its behavior • Outbreak occurred at end of rainy season in Tai, which includes larger numbers of small mammals and insects which could explain outbreaks at that time
Discussion:further studies • Studies to investigate the natural EBO virus reservoir • Study would give better understanding of the transmission mechanisms of EBO within and between species • More research on the capacity for EBO to leave the forest and emerge in human populations
Implications: • There is a current EBO outbreak among critical chimpanzee and gorilla populations throughout Central Africa • Primatologists say that nearly 2/3 of a gorilla population wiped out in Lossi Sanctuary in Republic of Congo. From 1,200 gorillas to 450. Leads to renewed fear for already critically endangered species, including mountain gorillas • This massive gorilla and chimp disaster has drawn the attention of the WHO & UN
References • Some slides quoted from: Formenty, Pierre et al. Ebola Virus Outbreak among Wild Chimpanzees Living in a Rain Forest of Cote d’Ivoire. Journal of Infectious Diseases. Volume 179, February 1999. Pp S120-S126. • Tsoumou, Christian. Ebola kills 100 in Congo, wipes out gorillas. http://www.enn.com/news/2003-03-12/s_3346.asp