Durand, J. P.

Galat Luong, Anh

Galat, Gérard

Jeannel, D.

Maison, P.

Thé, G. de

Tuppin, P.

Horizon / Pleins textes

' "*I 
I 'i 
AIDS RESEARCH AND HUMAN RETROVIRUSES 
Volume 11, Number 8, 1995 
Mary Ann Liebert, Inc. 
¿ 8- 
* 
i 
4- 
Short Communication 
Increased Risk for a Second Retroviral Infection (SIV or 
STLV Type I) for Wild'African Green Monkeys Already 
Infected by One Retrovirus in Senegal (West Africa) 
JEAN-PAUL DURAND,' PHILIPPE TUPPIN,2 PATRICK MAISON,' GÉRARD GALAT,3 
ANH GALAT-LUONG,3 DOMINIQUE JEANNEL,' and GUY DE TH@ 
H E  MOST WIDELY DISTRIBUTED simian group in Africa, from 
Ethiopia to Senegal and from Sudan to South Africa, is 
Cercopithecus aethiops, with the subspecies in Senegal being 
C. a. sabueus (commonly named green monkey [GM]). Simian 
immunodeficiency virus (SIV) seroprevalence is high in wild 
GMs from East Africa and in captive sooty mangabeys from 
West Africa.'-3 Natural infection of GMs and sooty mangabeys 
with their respective SIV strain is not associated with overt im- 
munosuppressive disease. On the other hand, the seroprevalence 
of simian T cell lymphotropic virus type I (STLV-I) is high in 
several Old World species, which may exhibit spontaneous ma- 
lignant lymphomas."* The GM is known to be the Old World 
species with the highest SIV and STLV-I seroprevalence. 
Available literature on SIV or STLV-I mainly concerns captive 
monkeys, which could have been accidentally or artificially in- 
fected after capture. Reports on SIV/STLV-I dual infection are 
scarce, except for semifree range colonies of sooty mangabeys 
and  mandrill^.^-^ However, to our knowledge, no survey has 
been carried out on the distribution of the two viruses in feral 
monkeys. Thus we compared seroprevalences of SIV and 
STLV-I in GM and analyzed determinants for double infection 
with the viruses. 
The study areas were Kedougou in southeast Senegal, near 
the Guinean border, and Sine-Saloum in central Senegal near 
the Gambian border. While both areas are forested savannah, 
they are geographically separated by a distance of 600 km. The 
simian population for the study comprised 171 monkeys. One 
hundred and twenty were killed during yellow fever control in 
1981 and 1982 in Kedougou; peripheral blood was obtained by 
cardiac puncture for SIV and STLV-I serology. The remaining 
51 monkeys were trapped in 1989 and 1991 in Sine-Saloum, 
and blood samples were withdrawn under ketamine anesthesia 
from the femoral vein. All animals were examined by prima- 
tologists (G.G. and A.G.-L.). The monkeys were classified ac- 
cording to their body weight and sexual maturity. Green mon- 
keys are semiterrestrial, living in multimale troops with 
multimale-multifemale mating behavior. 
Sera from monkeys were stored at the Pasteur Institute in 
Dakar, They were tested for SIV by enzyme-linked im- 
munosorbent assay (ELISA) (Elavia-Mixt 1-2; Diagnostics 
Pasteur, Marnes la Coquette, France) at the beginning of the 
study, and after the isolation of an SIV, strain from a GM 
living in Sine-Saloum, as reported elsewhere,'O sera were tested 
a second time by ELISA using this strain. All ELISA-positive 
sera were confirmed as SIV positive by Western blot using cul- 
ture supernatants of cells infected with the isolated SIV,, 
strain. Antibodies to STLV-I were detected by a commercially 
available ELISA kit (Du Pont de Nemours, Wilmington, DE) 
and by immunofluorescence assay. Positive sera were con- 
f m e d  by HTLV-I Western blot (Du Pont de Nemours). The 
reliability of the human HTLV-I commercial test to detect 
STLV-I was good in view of the high sequence homology be- 
tween these two viruses. Crude odds ratios (ORs) were calcu- 
lated. The data were subjected to stepwise logistic regression 
analysis to select significant and independent determinants for 
SIV and/or STLV-I seropositivity, As shown in Table 1, the 
seroprevalence of SIV antibodies was high in GMs in both ar- 
eas. The risk of SIV seropositivity in monkeys was significantly 
associated with sexual maturity (OR = 4.9, p < 0.0601) and 
seropositivity to STLV-I (OR = 3.2, p < 0.001). Increased risk 
of STLV-I seropositivity in GMs was significantly associated 
with two independent factors, i.e., SIV seropositivity (OR = 
4.4, p < 0.0001) and geographic location in Kedougou (OR = 
2.4, p < 0.05) (Table 1). These results disclosed that the two 
retroviruses might interact so as to increase the risk of double 
infection. The increased risk of SIV is associated with infec- 
tion by STLV-I and vice versa. 
The question arises as to whether the fact that mature mon- 
keys are more prone to be captured or hunted than immature 
ones has created biased results. Samples from animals in Sine- 
Saloum should be representative of the population because the 
troops were trapped, then released. Also, the age structure of 
the Sine-Saloum monkeys used in our study did not differ from 
that reported.' I In Kedougou, the STLV-I seroprevalence was 
similar to that found in 1984-1985 in the same region12 (40.8 
vs. 41%, respectively). In our care to avoid possible biases, we 
'Institut de Médecine Tropicale du Service de SantC des Années, Parc du Pharo, 13007 Marseille, France. 
*Unité d'Epidémiologie des Virus Oncogènes. Institut Pasteur, 28, rue du Dr. Roux, 75015 Paris, France. 
'ORSTOM, Dakar, Senegal. ~ . "  
985 
TABLE 1. GREEN MONKEYS: ODDS RATIO FOR PRESENCE OF SIV, STLV, SIV AND STLV ANTIBODIES BY AREA, SEX, AND AGE 
SN STLV SN and STLV 
Parameter 1'4 n i -  % ORa p ORb p n+ % ORa P ORb p n+ % ORa P ORb p 
~ ~~ ~~ ~~ 
Prevalence 171 66 38.6 61 35.7 37 21.6 
Area 
Kedougou 120 47 39.2 1.1 49 40.8 2.2 <0.05 2.4 C0.05 31 25.8 2.6 (0.05 
Sine-Saloum 51 19 37.3 1 12 37.2 1 1 6 11.8 1 
Male 103 33 32.0 0.5 <0.05 38 36.9 1.1 21 20.4 0.8 
Female 68 33 48.5 1 23 33.8 1 16 23.5 1 
Sex 
Age 
Young 79 14 17.7 1 1 17 21.5 1 5 6.3 1 1 
Negative 110 29 26.4 1 1 
Negative 105 24 22.8 1 1 
Adult 92 52 56.5 6.0 <0.0001 4.9 <0.0001 44 47.8 3.3 (0.001 32 34.8 7.9 <0.0001 7.9 <0.001 
STLV 
Positive 61 37 60.7 4.3 <0.0001 3.2 <0.001 
SIV 
Positive 66 37 56.1 4.3 <0.0001 4.4 <0.0001 
aCrude OR. 
bOR obtained by a stepwise logistic regression including age, sex, area, and presence of antibodies to the second retrovirus. For SIV/STLV only age, sex, and area were 
included. 
‘I 
DEPENDENCE OF SIVlSTLV INFECTIONS I N  GREEN MONKEYS 987 
grouped the monkeys according to their sexual maturity prior 
to analysis. Because SIV- or STLV-positive monkeys generally 
do not present pathologies associated with the viruses, biases 
due to hunting more easily infected monkeys than noninfected 
ones remain unlikely. 
We calculated the expected numbers of coinfected monkeys, 
assuming that the two viruses are independently distributed. 
However, significant differences between the expected and ob- 
served numbers of coinfections implied a dependence in the. 
distribution of the two viruses. To  compare our results post hoc 
with those already published for other species with different be- 
haviors, we calculated the expected and observed numbers from 
two studies reporting SIV-STLV coinfections: mandrills in a 
semifree-range colony in Gabong and sooty mangabeys in a 
breeding colony in  the United  state^.^ The results disclosed a 
significant excess of coinfected animals (Table 2). We also 
compared HIV-IR and HTLV-I/II coinfections in different ge- 
ographic areas and risk groups within which both viruses were 
present. In the 1980s, intravenous drug users (IVDUs) had a 
significant excess of both HTV-I and HTLV-III1 infections in 
the northeastern United States, that is, New Jersey, Baltimore, 
Manhattan, and B r ~ o k l y n l ~ - ’ ~  (Table 2). The findings could be 
due to the high proportion of’ blacks in the study samples, be- 
cause African Americans are known to have a higher HTLV- 
I / IJ  seroprevalence compared with that of whites or hispanics. 
Preinfection with HTLV-ILI may also increase the susceptibil- 
ity to HIV infections as well. In populations with predominantly 
heterosexual transmission of HIV and HTLV, an association 
between the two viruses has been reported in Haiti (HIV- 
I/HTLV-I) and Guinea-Bissau (HIV-2/HTLV-I).’8-1g 
The results from our survey on endemic simian retroviruses 
and retrospective analysis of published data indicate that dual 
infection occurs more frequently than expected in several species 
with different mating behaviors. Thus, one retroviral infection 
may induce an enhanced susceptibility of the host to a second 
retrovirus. It could be further investigated in several species of 
monkeys for whom the immunosuppression linked to SN in- 
fection is not present and could not facilitate infection by STLV. 
Potential disease manifestations of dual infection have been 
described i n  green monkeys. A study of wild-caught monkeys 
points out a high level of T lymphocytes and a low henioglo- 
bin level in coinfected monkeys compared with monkeys 
seronegative for both viruses, but no comparisons were done 
between coinfected monkeys and monkeys infected by only one 
of the viruses.?O A lymphoproliferative disease and immuno- 
deficiency were reported for a monkey dually infected, sug- 
gesting an  alternative reciprocal activation of SIV by STLV-I, 
which could havc resulted in immunosuppression and compro- 
mised immune surveillance, thereby promoting unchecked pro- 
liferation of rare STLV-transformed cells.8 The similarity found 
T-LE 2. DEPENDENCE O F  RETROVIRAL INFECTIONS IN MONKEYS AND HUMANS 
Sample (re$) 
S N  STLV SIV/STL V SN/STLV 
N f%) f%) (% observed) (% expected) P 
Monkeys 
C. aethiops“ 
Sooty mangabey (3) 
Mandrill (9) 
Humans 
Total 
Manhatan 
Brooklyn 
New Jersey 
Total 
New Jersey 
Total 
Black people 
IVDA, 1991 (14) 
Baltimore 
Baltimore 
Haiti, 1988-1989 (18) 
Hospitalized 
Guinea-Bissau, 1991 (19) 
Hospitalized 
Policemen 
IVDA, 1985- I987 ( 13) 
IVDA, 1987- I988 ( 16) 
JVDA, 1987-1989 (17) 
171 
138 
40 
1160 
139 
666 
175 
1800 
284 
387 
228 
356 
575 
628 
987 
512 
38.6 35.7 21.6 13.8 
57.0 33.0 27.0 18.8 
12.5 12.5 7.5 1.6 
HIV HTLV HI V/HTL V HN/HTLV 
f%)  f %) (% obsenied) (% expected) 
39.1 
39.6 
48.5 
34.9 
21.2 
24.3 
7.8 
3.9 
6.5 
4.2 
49.8 
19.6 
13.7 
12.2 
23.7 
8.3 
8.6 
11.5 
2.8 
16.8 
24.6 
1.4 
2.3 
11.5 
6.7 
3.7 
5.8 
15.1 
5. I 
5.7 
2.7 
I .9 
2.3 
7.9 
1.1 
I .6 
8.9 
2.9 
3.5 
4.8 
9.4 
4.0 
3.0 
2.4 
0.7 
1.3 
1 .o 
o. 1 
o. 1 
5.7 
1.3 
0.5 
<0.01 
<0.05 
<0.01 
NS 
<0.05 
NS 
C0.05 
NS 
<0.05 
NS 
C0.05 
<o.ooo 1 
<0.0001 
<0.001 
<o.ooo I 
<o.o001 
“This study. 
Abbrevialion: IVDA, Intravenous drug abuser; NS, not significant 
\ 
r $  
j 
988 DURAND ET AL. 
between the results of our survey and post hoc analysis of hu- 
simians might be extended to humans. The susceptibility to an 
infection by a second retrovirus should be explored by a fol- 
low-up of two groups of monkeys or humans infected, or not 
infected, by STLV or HTLV to compare the incidence of SIV 
or HIV infection in both groups, taking into account behavioral 
patterns, to disclose different levels of exposure to SIV or HIV 
in these groups. 
I man populations suggests the possibility that the findings in 
c 
k '1 
C 
ACKNOWLEDGMENTS 
This study was supported by the Agence Nationale dc la 
Recherche sur le SIDA ( A M s )  and the Pasteur Institute of 
Dakar. P. Tuppin was the recipient of a fellowship from the 
Caisse Nationale d'Assurance Maladie and Pasteur Institute. 
Thanks to L. Ferrara, R. Chateau, and F. Legros at ORSTOM 
for their help in hunting the monkeys and Dr. R. Bomford and 
T. Suzuki for their assistance in the preparation of this manu- 
script. 
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Address reprints requests to: 
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UiiirP d'Epide'tniologie des Virus 0tlcogètle.s 
Irisrifur Pasfeur 
26, rue du Dr. Rou.r 
7501.5 Pnris, Frunce 


Increased risk for a second retroviral infection (SIV or STLV type 1) for wild African green monkeys already infected by one retrovirus in Senegal (West Africa)

Increased risk for a second retroviral infection (SIV or STLV type 1) for wild African green monkeys already infected by one retrovirus in Senegal (West Africa)

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