Reduced transmission and prevalence of simian T-cell lymphotropic virus in a closed breeding colony of chimpanzees (Pan troglodytes verus)

H. Niphuis1, E. J. Verschoor1, I. Bontjer1, M. Peeters2 and J. L. Heeney1

1 Department of Virology, Biomedical Primate Research Centre, Lange Kleiweg 139, 2288 GJ Rijswijk, The Netherlands
2 Laboratoire Retrovirus, UR36 IRD, 911 Avenue Agropolis, BP 5045, 34032 Montpellier Cedex 1, France

Correspondence
Jonathan Heeney
heeney{at}bprc.nl


   ABSTRACT
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ABSTRACT
INTRODUCTION
METHODS
RESULTS
DISCUSSION
REFERENCES
 
A retrospective study spanning 20 years was undertaken to investigate the prevalence and modes of transmission of a simian T-cell lymphotropic virus (STLV) in a closed breeding colony of chimpanzees. Of the 197 animals tested, 22 had antibodies that were cross-reactive with human T-cell lymphotropic virus type-1 (HTLV-I) antigens. The specificity of the antibody response was confirmed by Western blot analysis and the presence of a persistent virus infection was established by PCR analysis of DNA from peripheral blood mononuclear cells. Sequence analysis revealed that the virus infecting these chimpanzees was not HTLV-I but STLVcpz, a virus that naturally infects chimpanzees. The limited number of transmission events suggested that management practices of social housing of family units away from troops of mature males might have prevented the majority of cases of transmission. Evidence for transmission by blood-to-blood contact was documented clearly in at least one instance. In contrast, transmission from infected mother to child was not observed, suggesting that this is not a common route of transmission for STLV in this species, which is in contrast to HTLV-1 in humans.

EMBL database accession numbers of the STLVcpz sequences described in this study are Y18902, Y18903 and AJ493584–AJ493594.

Published ahead of print on 11 December 2002 as DOI 10.1099/vir.0.18778-0.


   INTRODUCTION
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ABSTRACT
INTRODUCTION
METHODS
RESULTS
DISCUSSION
REFERENCES
 
Human T-lymphotropic viruses type I (HTLV-I) belong to the genus Deltaretrovirus, of which bovine leukaemia virus is the type species. In humans, HTLV-I is associated with adult T-cell leukaemia and HTLV-I-associated slowly progressive myelopathy (Gessain et al., 1985; Poiesz et al., 1980). HTLV-I is transmitted between sexually active partners (Schreiber et al., 1997), from mother to child, commonly through breast-feeding (Miyoshi et al., 1992), and by blood-to-blood contact (Schreiber et al., 1997).

In 1982, the existence of naturally occurring HTLV-related viruses in non-human primates was first demonstrated by the presence of anti-HTLV antibodies in Japanese macaques (Macaca fuscata) (Miyoshi et al., 1982). Since then, many simian T-cell lymphotropic viruses (STLV) from different lineages (STLV-I, STLV-II, STLV-L) have been characterized from a wide range of non-human primate species (Digilio et al., 1997; Giri et al., 1994; Goubau et al.; 1994; Ishikawa et al., 1987; Mahieux et al., 1997a; Meertens et al., 2001; errienet et al., 2001; NSaksena et al., 1994; Takemura et al., 2002; Vandamme et al., 1996). With regard to the presence of STLV-I infections in great apes, serologically related, but clearly distinct, viruses have been found in orangutans (Ibuki et al., 1997; Verschoor et al., 1998), common chimpanzees, pygmy chimpanzees and gorillas (Giri et al., 1994; Ishikawa et al., 1987; Koralnik et al., 1994; Saksena et al., 1994; Vandamme et al., 1996; Voevodin et al., 1997). STLV-I primarily causes asymptomatic infections in their natural hosts but rare cases of STLV-associated leukaemia and/or lymphoma have been reported in African green monkeys, baboons, macaques and gorillas (Franchini & Reitz, 1994). HTLV-I and STLV-I cannot be separated into different phylogenetic clusters or clades (Saksena et al., 1993), suggestive of multiple inter-species virus transmissions in the past and present (Koralnik et al., 1994).

Little is known about the modes of transmission of STLV in non-human primates. In this study, we examined the incidence and possible modes of transmission of HTLV-I-like infections in a closed breeding colony of Western common chimpanzees (Pan troglodytes verus), all descending from a group of founder animals originating from Sierra Leone. A reduced rate of transmission was monitored of a virus characterized as STLVcpz, a virus that naturally infects chimpanzees.


   METHODS
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ABSTRACT
INTRODUCTION
METHODS
RESULTS
DISCUSSION
REFERENCES
 
Chimpanzees and samples collected.
Blood samples were collected over the period between 1980 and 2000 from a closed breeding colony of chimpanzees housed at the Biomedical Primate Research Centre (BPRC), Rijswijk, The Netherlands. The colony was founded in 1963 with 37 animals (originating from Sierra Leone) that belong to the subspecies Pan troglodytes verus, the Western common chimpanzee.

Blood was drawn from all colony animals on a regular yearly basis as part of the routine health surveillance programme. Serum and peripheral blood mononuclear cells (PBMCs) were separated and stored at -20 and -80 °C, respectively. Few serum samples were available prior to 1980.

Detection of antibodies cross-reactive with HTLV-I antigens.
Serum samples from the chimpanzees were assayed for antibodies to HTLV-I antigens by an ELISA developed in-house (Warren et al., 1998). The specificity of the ELISA responses was confirmed by Western blot (WB) analysis using HTLV blot 2.4 (Genelabs Diagnostics), which detects both anti-HTLV-I and anti-HTLV-II antibodies.

PCR and sequence analysis.
Genomic DNA was isolated from PBMCs using standard DNA isolation procedures. Primers env-1, env-2 and env-22 were used in a semi-nested PCR for the amplification of a 522 bp fragment from the envelope gene of HTLV-I/STLV-I (Ibrahim et al., 1995; Koralnik et al., 1994). Genomic DNA (1 µg) was used as template for each PCR assay. Amplification reactions were performed in the presence of 200 µM of each dNTP, 50 pmol of each primer, 10 mM Tris/HCl (pH 8·3), 50 mM KCl and 1·25 U TaqGold (Applied Biosystems). The reaction mixtures for the env PCR contained 2·3 and 2·1 mM MgCl2 in combination with the outer and semi-nested primer sets, respectively. Both amplification reactions were performed for 35 cycles consisting of a 30 s denaturation step at 94 °C, a 30 s annealing step at 56 °C and an elongation step of 1 min at 72 °C.

PCR fragments were analysed on a 1·5 % agarose gel, bands were cut out and PCR fragments isolated using the QIAquick Gel Extraction kit (Qiagen). Fragments were cloned in the pGEM-T cloning vector (Promega) and sequenced using the Sequenase DNA Sequencing kit, version 2.0 (USB). Sequences were analysed using GENEWORKS, version 2.3 (IntelliGenetics).

Phylogenetic analysis.
Analysis of the HTLV/STLV sequences was performed using the MACVECTOR, version 6.0, and ASSEMBLYLIGN software packages (Oxford Molecular). Phylogenetic analysis of nucleotide sequences was performed using PAUP, version 4.0b10 (Swofford, 2002). Pairwise distances were calculated using the HKY85 method and the neighbour-joining method was used to create a phylogram.


   RESULTS
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ABSTRACT
INTRODUCTION
METHODS
RESULTS
DISCUSSION
REFERENCES
 
Sera of 197 chimpanzees were analysed for antibodies against HTLV-I antigens by ELISA. Samples included sera from the 37 founder animals and the 160 offspring that were born since the colony was established. Serum sampling began in 1980 on a regular yearly basis; few samples were available for testing prior to 1980.

Of all 197 chimpanzees tested, 22 showed antibodies to HTLV-I antigens in their blood (Table 1). The majority of cases (n=20) were found in the group of founder animals, while only two HTLV-positive animals were detected in the offspring born in the colony. All positive ELISA results were confirmed by HTLV WB analysis.


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Table 1. Relationship between infection, origin and sex of chimpanzees

Number positive tested/total number tested.

 
To determine if the virus infecting these animals was iatrogenically introduced HTLV-I or a naturally occurring chimpanzee virus, PBMC DNA from seropositive chimpanzees was examined for HTLV/STLV env sequences by nested PCR. DNA was available for PCR and sequence analysis from 13 animals. The 522 bp fragment that was amplified from the env region was compared with published HTLV-I and STLV-I sequences. The phylogenetic tree is shown in Fig. 1. New virus sequences obtained were most closely related to published sequences obtained from other STLV-I-infected chimpanzees (PTR114.1, PTR-3570 and PTR-X43) and all belong to the HTLV-I/STLV-I subtype B lineage. Interestingly, the new viruses divide into two well-supported subclusters (89 and 100 % bootstrap support).



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Fig. 1. Phylogenetic relationship of the new STLVcpz with other primate lymphotropic type 1 viruses based on the analysis of a 522 bp env fragment. Distances were determined using the HKY85 method and the tree was constructed using the neighbour-joining method. The numbers at the nodes indicate the percentage probability after analysis of 1000 bootstrap re-samplings. Major STLV-I and HTLV-I lineages are indicated according to Nerrienet et al. (2001). The sequences obtained from 13 founder animals are indicated in bold. Animals infected while in captivity are indicated by a #. All HTLV-I and STLV-I sequences were obtained from GenBank/EMBL and are indicated by H or S, strain denomination and their host species, respectively.

 
The frequency of STLVcpz infection in the colony was examined further with regard to origin, familial group, sex and age. The frequency of seropositive animals among the original founder group was 54 % (20/37). This figure is in sharp contrast with the incidence of STLV infections among the animals born in captivity, of which only 1 % (2/160) of offspring were STLV-positive (Table 1). No significant difference in overall infection rate was found between the female (14/107) and the male (8/90) chimpanzees. However, in the founder group, infection rates were 70 and 48 % between males and females, while in the offspring the numbers of infected males and females were both 1 %.

From the compiled data of the entire chimpanzee colony over two decades, it is clear that transmission of this virus was a relatively rare event. Prior to 1986, one seroconversion event was documented, while between 1986 and 2001, only two seroconversions were observed. Ch-So is an adult female belonging to the founder population. Serum samples from Ch-So, which were collected prior to 1973, were negative in ELISA and WB analyses (Fig. 2, lane 3) but this animal seroconverted in 1973 (Fig. 2, lane 4). The two other seroconversions occurred more recently in adult chimpanzees that were born in captivity in the colony. These infections were linked to two separate events. One transmission of STLVcpz occurred during a fight between two males, Ch-Co and Ch-Bi. During this event, the aggressor, Ch-Bi, who drew blood, later became STLVcpz-seropositive (Fig. 2, lanes 5–6, Ch-Bi and lane 7, Ch-Co). The other case involved a seronegative female, Ch-Ev, who was in a breeding programme with a male, Ch-Fr, who was unknowingly infected with STLV. The actual event associated with transmission could not be documented specifically but seroconversion occurred shortly after conception (Fig. 2, lanes 8–9, Ch-Ev and lane 10, Ch-Fr).



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Fig. 2. WB analysis of transmission events of STLVcpz in the chimpanzee colony. Lanes: 1 and 2, blots incubated with positive and negative control sera, respectively; 3 and 4, sera from Ch-So before (1 January 1973) and after (1974) transmission; 5 and 6, negative (26 October 1992) and positive (9 January 1996) sera from Ch-Bi; 7, sera from Ch-Co; 8 and 9, negative (5 November 1991) and positive (21 November 1995) sera from Ch-Ev; 10, sera from Ch-Fr.

 

   DISCUSSION
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ABSTRACT
INTRODUCTION
METHODS
RESULTS
DISCUSSION
REFERENCES
 
STLV infections are common in many different species of non-human primates but very little is known about their natural routes of transmission. A high prevalence of STLVcpz infection (54 %) was detected in the group of animals that founded this colony of Western common chimpanzees (Pan troglodytes verus). In contrast to these figures, only two cases of STLVcpz infection were detected in the 160 offspring born in captivity (1 % infection rate). Several authors have published on the incidence of STLV-I infections in non-human primates in the wild (Ishikawa et al., 1987; Meertens et al., 2001; Nerrienet et al., 2001; Saksena et al., 1994; Warren et al., 1998). In wild animals, infection rates varied between 0 and 80 % depending on the species examined. However, in general, reported infection rates of great apes (orangutans, gorillas and chimpanzees) have been lower (2–13 %). Studies of captive populations have noted great differences in prevalence (Georges-Courbot et al., 1996; Ibuki et al., 1997; Kalter et al., 1997; Lerche et al., 1994; Mahieux et al., 1997b). In an earlier study of STLV infections in chimpanzees, a study that failed to discriminate between founder and offspring animals, 19 % of captive chimpanzees were found to be seropositive (Voevodin et al., 1997).

The discrepancy between incidence rates of founder animals and offspring in our colony (54 versus 1 %) can, in part, be explained by the history of the older animals. In the 1970s, five female founder animals received blood cell transfusions and/or skin grafts from donors now recognized as STLVcpz carriers. The likelihood of iatrogenic transmission is made plausible by the documented seroconversion of Ch-So. This animal first tested positive shortly after having received a blood transfusion and skin transplantation from Ch-Lo who was STLVcpz-infected, as tested in retrospect on sera from 1975 and 1986. Analysis of plasma from Ch-So sampled 23 years after the transfusion event revealed infection with a variant that differed in only 3 aa with the sequence of the donor, Ch-Lo. Comparable sequence differences were described by others who also reported minor sequence differences 8 years after transmission of STLV from macaques to baboons (Voevodin et al., 1996). The 15 other STLV-positive founders (41 %) have not had comparable treatment and most likely acquired the infection via a natural route of transmission. Since that time, serological monitoring of virus infections in our colony has minimized the chance of iatrogenic transfer of STLVcpz infection. Indeed, the infection rate of animals born in this colony has dropped to only two cases of transmission in 160 animals (1 %).

In humans, HTLV-I is transmitted commonly from mother-to-child through breast-feeding (Chiodo et al., 1986; Miyoshi et al., 1992; Nyambi et al., 1996). In contrast to the human situation, this appears to be an uncommon mode of transmission in this chimpanzee breeding colony. A considerable proportion of the 160 animal offspring, 79animals, were natural births from STLV-positive females. Depending on the individual situation, all the animals were breast-fed for a minimum of 3 months before weaning but the majority continued to nurse for periods of a year or more. After weaning, none of the babies were found to be infected with STLVcpz. Anti-STLV antibodies in milk and transient maternal antibody titres in sera from newborn animals were detectable by ELISA, but PCR analysis from milk samples from infected nursing females did not reveal the presence of virus (data not shown).

When compared to the data of the wild-derived founder chimpanzees, the transmission rate in the colony after 1986 was very low. The nature of social management of the colony may have attributed to the low number of new infections. Over the past 20 years, these animals have been socially grouped into stable family units and age-related peer groups. We propose that such social configurations reduce transmission, which may occur in the wild following blood-to-blood contact resulting from territorial fighting of competitive family groups or raids by troops of mature males. The latter may be an explanation for the 70 % infection rate among the wild-caught male founders when related to the figures of naturally infected female founders (eight animals; 30 %).

Clearly, the virus found in our colony was introduced by a number of naturally infected founder animals and is not an HTLV-I strain introduced by iatrogenic transfer. We have characterized the virus as STLVcpz belonging to a larger group of chimpanzee viruses, comprising STLV PTR-114.1, -3570 and -X43, and members of the large HTLV-I/STLV-I central African subtype B clade. Several authors (Koralnik et al., 1994; Voevodin et al., 1997) have speculated that chimpanzees may be infected with distinct STLV strains depending on the subspecies and geographical distribution. The STLVcpz from previous studies were derived from chimpanzees that had either an indeterminate geographical origin or may have acquired the infection while in captivity with animals from other subspecies or origin. Since the specific origin and subspecies of the colony of animals is known, our data imply that the origin of this group of STLVcpz is Pan troglodytes verus of the Sierra Leone region.

From our study, it is apparent that mother-to child transmission in chimpanzees is very uncommon. Based on only a few examples, we suspect that the majority of transmission events in the wild occurs during social conflicts among rival troops or families. Furthermore, to sustain this STLV infection in chimpanzee populations, such events must occur relatively frequently in wild, free-ranging chimpanzees.


   ACKNOWLEDGEMENTS
 
We are endebted to the very dedicated animal care staff and especially Loek van Hoek who has cared for many of these animals since the colony was established by TNO. This information has been made possible by the BPRC's colony health and virus surveillance programme.


   REFERENCES
Top
ABSTRACT
INTRODUCTION
METHODS
RESULTS
DISCUSSION
REFERENCES
 
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Received 15 August 2002; accepted 27 November 2002.