Cross-species retroviral transmission from macaques to human beings

doi:10.1016/S0140-6736(02)09597-1

The Lancet

Volume 360, Issue 9330, 3 August 2002, Pages 387-388

https://doi.org/10.1016/S0140-6736(02)09597-1 Get rights and content

Summary

Cross-species transmission of simian foamy virus (SFV) to human beings from chimpanzees, baboons, and African green monkeys has been described. Although macaques are the non-human primate most often handled in research, human infection with SFV from macaques has not been reported. Two of 46 primatefacility workers tested positive for antibodies that reacted with an immunoblot that contained macaque foamy virus antigens. Phylogenetic assessment of a 96-bp fragment of amplified proviral DNA isolated from peripheral-blood mononuclear cells from one infected individual was consistent with SFV infection of macaque origin. Frequent use of macaques in biomedical research, and identification of persistent retroviral infection from macaques to human beings, could have implications for publichealth policy and occupational health and safety.

References (5)

PA Sandstrom et al.
Simian foamy virus infection among zoo keepers
Lancet
(2000)
CD Meiering et al.
Historical perspectives of foamy virus epidemiology and infection
Clin Microbiol Rev
(2001)

There are more references available in the full text version of this article.

Cited by (66)

Evolutionary Medicine of Retroviruses in the Human Genome
2019, American Journal of the Medical Sciences
Humans are infected with many viruses, and the immune system mostly removes viruses and the infected cells. However, certain viruses have entered the human genome. Of the human genome, ∼45% is composed of transposable elements (long interspersed nuclear elements [LINEs], short interspersed nuclear elements [SINEs] and transposons) and 5-8% is derived from viral sequences with similarity to infectious retroviruses. If integration of retrovirus occurs in a germline, the integrated viral sequences are heritable. Accumulation of viral sequences has created the current human genome. This article summarizes recent studies of retroviruses in humans and bridges clinical fields and evolutionary genetics. First, we report the repertories of human-infective retroviruses. Second, we review endogenous retroviruses in the human genome and diseases associated with endogenous retroviruses. Third, we discuss the biological functions of endogenous retroviruses and propose the concept of accelerated human evolution via viruses. Finally, we present perspectives of virology in the field of evolutionary medicine.
Spumaretroviruses: Updated taxonomy and nomenclature
2018, Virology
Citation Excerpt :
The first “human” spumaretrovirus isolate was obtained from cultures of a human nasopharyngeal carcinoma in 1971 and was originally designated “human foamy virus (HFV)” (Achong et al., 1971a, 1971b), but was later found to be of chimpanzee origin based upon sequence identity to chimpanzee foamy virus and renamed as prototype foamy virus (PFV) (Meiering and Linial, 2001; Herchenroder et al., 1994). Cross-species transmissions of simian foamy viruses (SFVs) to humans have occurred by exposure to fluids or tissues from infected NHPs (Betsem et al., 2011; Calattini et al., 2007; Engel et al., 2013; Heneine et al., 2003, 1998; Mouinga-Ondémé et al., 2012; Schweizer et al., 1995; Stenbak et al., 2014; Switzer et al., 2004, 2012; Wolfe et al., 2004; Khan, 2009; Brooks et al., 2002; Callahan et al., 1999). Although foamy viruses are exogenously transmitted viruses, endogenous foamy virus sequences have been identified and characterized in genomes of many species, including aye-aye (Daubentonia madagascariensis), sloth (Choloepus hoffmanni), Cape golden mole (Chrysochloris asiatica), coelacanth (Latimeria chalumnae), platyfish (Xiphophorus maculatus), and zebrafish (Danio rerio) (Katzourakis et al., 2014, 2009; Aiewsakun and Katzourakis, 2017; Han and Worobey, 2012a, 2012b, 2014; Ruboyianes and Worobey, 2016).
Spumaretroviruses, commonly referred to as foamy viruses, are complex retroviruses belonging to the subfamily Spumaretrovirinae, family Retroviridae, which naturally infect a variety of animals including nonhuman primates (NHPs). Additionally, cross-species transmissions of simian foamy viruses (SFVs) to humans have occurred following exposure to tissues of infected NHPs. Recent research has led to the identification of previously unknown exogenous foamy viruses, and to the discovery of endogenous spumaretrovirus sequences in a variety of host genomes. Here, we describe an updated spumaretrovirus taxonomy that has been recently accepted by the International Committee on Taxonomy of Viruses (ICTV) Executive Committee, and describe a virus nomenclature that is generally consistent with that used for other retroviruses, such as lentiviruses and deltaretroviruses. This taxonomy can be applied to distinguish different, but closely related, primate (e.g., human, ape, simian) foamy viruses as well as those from other hosts. This proposal accounts for host-virus co-speciation and cross-species transmission.
Bayesian inference reveals ancient origin of simian foamy virus in orangutans
2017, Infection, Genetics and Evolution
Citation Excerpt :
Research on SFV in chimpanzees has shown that in general, DNA makes up < 50% of viral genomes, with no evidence of particle-associated DNA genomes in fecal samples (Liu et al., 2008). SFVs have received significant public health interest because of the potential ease of transmission to workers handling nonhuman primate(s) (NHP) in research facilities, and at zoos (Brooks et al., 2002; Heneine et al., 1998; Huang et al., 2012; Murphy et al., 2006; Sandstrom et al., 2000; Stenbak et al., 2014; Switzer et al., 2004), the transmission of SFVs through hunting and butchering of NHPs in the wild (Betsem et al., 2011; Calattini et al., 2007, 2011; Gessain et al., 2013; Mouinga-Ondémé and Kazanji, 2013; Smith et al., 2012: Switzer et al., 2012; Wolfe et al., 2004), transmission to tourists or those living in close association with free-ranging NHPs and performing monkeys in Asia (Engel et al., 2013; Jones-Engel et al., 2005, 2008; Schillaci et al., 2005), and the potential threat of SFVs to the safety of the blood supply from infected persons who donate blood (Boneva et al., 2002; Brooks et al., 2007; Schillaci et al., 2008), FVs, including SFVs, have also been of scientific interest given the strong evidence of ancient co-evolution within and among host species (Katzourakis et al., 2009).
Simian foamy viruses (SFVs) infect most nonhuman primate species and appears to co-evolve with its hosts. This co-evolutionary signal is particularly strong among great apes, including orangutans (genus Pongo). Previous studies have identified three distinct orangutan SFV clades. The first of these three clades is composed of SFV from P. abelii from Sumatra, the second consists of SFV from P. pygmaeus from Borneo, while the third clade is mixed, comprising an SFV strain found in both species of orangutan. The existence of the mixed clade has been attributed to an expansion of P. pygmaeus into Sumatra following the Mount Toba super-volcanic eruption about 73,000 years ago. Divergence dating, however, has yet to be performed to establish a temporal association with the Toba eruption. Here, we use a Bayesian framework and a relaxed molecular clock model with fossil calibrations to test the Toba hypothesis and to gain a more complete understanding of the evolutionary history of orangutan SFV. As with previous studies, our results show a similar three-clade orangutan SFV phylogeny, along with strong statistical support for SFV-host co-evolution in orangutans. Using Bayesian inference, we date the origin of orangutan SFV to > 4.7 million years ago (mya), while the mixed species clade dates to approximately 1.7 mya, > 1.6 million years older than the Toba super-eruption. These results, combined with fossil and paleogeographic evidence, suggest that the origin of SFV in Sumatran and Bornean orangutans, including the mixed species clade, likely occurred on the mainland of Indo-China during the Late Pliocene and Calabrian stage of the Pleistocene, respectively.
Mechanisms of viral emergence and interspecies transmission: The exemple of simian foamy viruses in Central Africa
2013, Bulletin de l'Academie Nationale de Medecine
La plupart des agents viraux pathogènes, ayant émergé durant les dernières décennies chez l’Homme, est d’origine animale (Coronavirus du SRAS, virus de la grippe aviaire, Hantavirus, virus Ebola, virus Marburg, virus Nipah, etc.). Après le contact initial qui a conduit à la transmission inter-espèces per se, ces virus, principalement à ARN, se sont ensuite, souvent adaptés à leur nouvel hôte par des mécanismes variés, puis ont disséminé dans l’espèce humaine par différentes voies. Alors que ces mécanismes évolutifs d’adaptation et ces voies de dissémination inter-humaine ont été largement étudiées, les connaissances concernant les premières étapes de l’émergence virale (comment, par quels moyens, dans quelles conditions, etc.) demeurent encore souvent rudimentaires. La veille microbiologique, associant des travaux épidémiologiques de terrain à des études sérologiques et viromoléculaires, dans des populations à haut risque de transmission inter-espèces, est donc nécessaire pour mieux comprendre les premières étapes de l’émergence virale. Les primates non-humains représentent une importante source potentielle d’agents infectieux transmissibles à l’Homme. Cela a été bien démontré pour les virus de l’immunodéficience simienne (SIV) et les rétrovirus T lymphotropes simiens (STLV). Nous présenterons ici les résultats d’enquêtes sérologiques et moléculaires, réalisées parmi des populations humaines du Sud-Cameroun, pour découvrir et caractériser de nouveaux rétrovirus chez l’Homme. Ces études multidisciplinaires, associant médecins, épidémiologistes, anthropologues et virologues, ont été menées dans des populations villageoises, soit d’origine Bantou, soit d’origine Pygmée, vivant dans la grande forêt équatoriale, dans des régions très proches des habitats des populations de primates non-humains, en particulier chimpanzés, gorilles, mandrills, cercopithèques, etc. La première étude concerne la découverte d’un nouveau rétrovirus humain ; l’HTLV-3, ainsi que sa caractérisation viro-moléculaire. La seconde étude, que nous détaillerons davantage dans cet article, concerne la mise en évidence de la transmission fréquente de rétrovirus foamy simiens aux Hommes, en particulier par des morsures de gorilles et de chimpanzés et la caractérisation des facteurs de risque de cette transmission.
A large proportion of viral pathogens that have emerged during the last decades in humans are considered to have originated from various animal species. This is well exemplified by several recent epidemics such as those of Nipah, Severe Acute Respiratory Syndrome, Avian flu, Ebola, Monkeypox, and Hantaviruses. After the initial interspecies transmission per se, the viruses can disseminate into the human population through various and distinct mechanisms. Some of them are well characterized and understood, thus allowing a certain level of risk control and prevention. Surprisingly and in contrast, the initial steps that lead to the emergence of several viruses, and of their associated diseases, remain still poorly understood. Epidemiological field studies conducted in certain specific high-risk populations are thus necessary to obtain new insights into the early events of this emergence process. Human infections by simian viruses represent increasing public health concerns. Indeed, by virtue of their genetic and physiological similarities, non-human primates (NHPs) are considered to be likely the sources of viruses that can infect humans and thus may pose a significant threat to human population. This is well illustrated by retroviruses, which have the ability to cross species, adapt to a new host and sometimes spread within these new species. Sequence comparison and phylogenetic studies have thus clearly showed that the emergence of human immunodeficiency virus type 1 (HIV-1) and HIV-2 in humans have resulted from several independent interspecies transmissions of different SIV types from Chimpanzees and African monkeys (including sooty mangabeys), respectively, probably during the first part of the last century. The situation for Human T cell Lymphotropic virus type 1 (HTLV-1) is, for certain aspects, quite comparable. Indeed, the origin of most HTLV-1 subtypes appears to be linked to interspecies transmission between STLV-1-infected monkeys and humans, followed by variable periods of evolution in the human host. In this review, after an introduction on emerging viruses, we will briefly present the results of a large epidemiological study performed in groups of Bantus and Pygmies living in villages and settlements located in the rain forest of the South region of Cameroon. These populations are living nearby the habitats of several monkeys and apes, often naturally infected by different retroviruses including SIV, STLV and simian foamy virus. Most of the persons included in this study were hunters of such NHPs, thus at high risk of contact with infected body fluids (blood, saliva,...) during hunting activities. After reviewing the current available data on the discovery, cross-species transmission from monkeys and apes to humans of the simian foamy retroviruses, we will report the results of our study. Such infection is a unique natural model to study the different mechanisms of restriction of retroviral emergence in Humans.
HTLV-3/4 and simian foamy retroviruses in humans: Discovery, epidemiology, cross-species transmission and molecular virology
2013, Virology
Citation Excerpt :
After these initial studies, a Center for Diseases Control (CDC) team demonstrated that, some workers occupationally exposed to NHPs were SFV infected (Heneine et al., 1998). Another study demonstrated the presence of SFV infection in workers from a primate facility in Canada (Brooks et al., 2002). Interestingly, among 187 persons occupationally exposed to NHPs from the large CDC cohort, SFV infection was found to be much more frequent (3.4%) than infection by other simian retroviruses such as SIV (0.06%), STLV (0%) or simian type D retrovirus (0.5%) (Switzer et al., 2004).
Non-human primates are considered to be likely sources of viruses that can infect humans and thus pose a significant threat to human population. This is well illustrated by some retroviruses, as the simian immunodeficiency viruses and the simian T lymphotropic viruses, which have the ability to cross-species, adapt to a new host and sometimes spread. This leads to a pandemic situation for HIV-1 or an endemic one for HTLV-1. Here, we present the available data on the discovery, epidemiology, cross-species transmission and molecular virology of the recently discovered HTLV-3 and HTLV-4 deltaretroviruses, as well as the simian foamy retroviruses present in different human populations at risk, especially in central African hunters. We discuss also the natural history in humans of these retroviruses of zoonotic origin (magnitude and geographical distribution, possible inter-human transmission). In Central Africa, the increase of the bushmeat trade during the last decades has opened new possibilities for retroviral emergence in humans, especially in immuno-compromised persons.
Intestinal parasites of endangered orangutans (Pongo pygmaeus) in Central and East Kalimantan, Borneo, Indonesia
2010, Parasitology

View all citing articles on Scopus

View full text

Research LettersCross-species retroviral transmission from macaques to human beings

Summary

Lancet

Historical perspectives of foamy virus epidemiology and infection

Clin Microbiol Rev

Research Letters
Cross-species retroviral transmission from macaques to human beings