Feline immunodeficiency virus (FIV) in wild Pallas’ cats

Abstract

Feline immunodeficiency virus (FIV), a feline lentivirus related to HIV, causes immune dysfunction in domestic and wild cats. The Pallas’ cat is the only species from Asia known to harbor a species-specific strain of FIV designated FIV_Oma in natural populations. Here, a 25% seroprevalence of FIV is reported from 28 wild Mongolian Pallas’ cats sampled from 2000 to 2008. Phylogenetic analysis of proviral RT-Pol from eight FIV_Oma isolates from Mongolia, Russia, China and Kazakhstan reveals a unique monophyletic lineage of the virus within the Pallas’ cat population, most closely related to the African cheetah and leopard FIV strains. Histopathological examination of lymph node and spleen from infected and uninfected Pallas’ cats suggests that FIV_Oma causes immune depletion in its’ native host.

Introduction

Pallas’ cat (Otocolobus manul) is a rare but widely distributed small Felidae species resident in arid, rocky shrub steppe habitats in Central Asia. It is classified as Near Threatened (Convention on International Trade in Threatened Species, 2006) primarily because of habitat loss, over-hunting and prey base depletion through poisoning (Ross, 2009). Pallas’ cats in captivity have a unique and marked susceptibility to infectious agents, especially Toxoplasma gondii, in comparison to other captive non-domestic cat species (Brown et al., 2005). These and other cases of opportunistic infections have been associated with suspected (Ketz-Riley et al., 2003) and confirmed (Barr et al., 1995) cases of immunodeficiency due to feline immunodeficiency virus (FIV) in captive Pallas’ cats.

FIV causes immune dysfunction in domestic cats, resulting in depletion of CD4+ cells, increased susceptibility to opportunistic infections, and sometimes death (Pedersen et al., 1989). FIV is also found in nondomestic felids; a serosurvey of over 3000 specimens from 35 felidae species identified 11 free-ranging felid species infected with FIV (Troyer et al., 2005). Monophyly of FIV proviral sequence within distinct Felidae species suggests that FIV transfer between cat species is an infrequent event (Carpenter et al., 1996, Troyer et al., 2008). FIV is endemic, in African cat species and in species of Hyaenidae and infects nearly all South American felid species (Carpenter et al., 1996, Troyer et al., 2005). Within populations in the wild, seroprevalence is highest in African felids (68–74%), lower in South American felids (5–28%) and nearly absent in Asia and Europe (Troyer et al., 2005). Free-ranging Pallas’ cats are the only known species from Asia that have a species-specific strain of FIV (Barr et al., 1995). Only one other case of FIV has been reported in free-ranging Asian cats; a Japanese leopard cat population was infected with a domestic cat FIV_Fca strain (Nishimura et al., 1999) through suspected cross-species transmission.

Pallas’ cat FIV, designated FIV_Oma, was first isolated from a wild-born male Pallas’ cat imported into the United States from Kazakhstan (termed Oma-Barr herein) (Barr et al., 1995). As in recent reports of immune depletion associated with FIV infection in lions and pumas (Roelke et al., 2006, Roelke et al., 2009), the infected Pallas’ cat also exhibited a low CD4+/CD8+ T-cell ratio and was co-infected with opportunistic infections of Trypanosoma species and Hepatozoon canis. In vitro characterization of this FIV_Oma isolate found it to be highly cytopathic in Crandell feline kidney cells in contrast to other isolates of domestic cat FIV (Barr et al., 1995).

In this study, samples from wild Pallas’ cats living in central Mongolia were assessed for FIV seroprevalence. Proviral DNA was amplified from Pallas’ cats, and cloned FIV sequences from three wild Pallas’ cats were analyzed phylogenetically in relation to other known FIV_Oma and FIV sequences isolated from other species. FIV_Oma was found to be monophyletic with little genetic distance among FIV isolates from disparate geographic locations, suggestive of either a 20th century introduction, a re-emergence of a new strain of FIV, and/or a selective adaptation leading to a unique monophyletic lineage within Pallas’ cat populations. In addition, spleen and lymph node from normal and infected Pallas’ cats were compared to assess the impact of FIV_Oma on immune function of the animal.