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doi: 10.1097/QAD.0b013e32832403e8
Research Letters

Decline in human T-cell lymphotropic virus-1 prevalence in urban areas of Bissau, Guinea-Bissau: exploring the association with HIV infections

da Silva, Zacarias Ja,b; Nielsen, Jensa,e; Andersen, Andreasa; Oliveira, Inésa,e; Dias, Franciscob; Rodrigues, Amabéliaa; Holmgren, Birgittac; Andersson, Sörend; Aaby, Petera,f

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aBandim Health Project, Indepth Network, Sweden

bNational Public Health Laboratory, Bissau, Guinea-Bissau, Sweden

cDepartment of Laboratory Medicine, Division of Medical Microbiology/Virology, Lund University, Lund, Sweden

dSwedish Institute of Infectious Disease Control, Stockholm, Sweden

eBandim Health Project, Statens Serum Institut, Denmark

fClinical Research Centre, Copenhagen University, Hvidovre Hospital, Copenhagen, Denmark.

Received 29 October, 2008

Revised 21 November, 2008

Accepted 25 November, 2008

Correspondence to Zacarias Jose da Silva, Bandim Health Project, Apt. 861, 1004 Bissau Codex, Guinea-Bissau. Tel: +245 201489; fax: +245 201672; e-mail: z.dasilva@bandim.org

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Abstract

In 2006, a cross-sectional survey of 384 randomly selected houses within a community-based follow-up study was conducted to assess the human T-cell lymphotropic virus (HTLV) prevalence in Bissau. Changes in prevalence and incidence rates were assessed based on a similar survey carried out 10 years earlier. The prevalence of HTLV-1 declined significantly from 3.5% in 1996 to 2.3% in 2006. The incidence between 1996 and 2006 was only 0.9/1000 person-years and tended to be higher for women than for men.

Over 20 million persons around the world are estimated to be infected with human T-cell lymphotropic virus type 1 or 2 (HTLV-1/HTLV-2) [1]. The majority are located in the Caribbean region, Japan and large areas of sub-Saharan Africa [2].

The human retroviruses HIV and HTLV are endemic in Guinea-Bissau. In 1989, a population-based cohort of elderly people (≥50 years) estimated a HTLV prevalence of 12.4% in women compared to 4.6% in men [3]. No HTLV-2 was found at that time. The first general population-based serosurvey on the spread of HTLV among adults was carried out in 1996. The HTLV-1 prevalence was estimated to be 3.6%, being 4.6% for women and 2.2% for men [4]. The present study assessed the changes in HTLV prevalence and incidence in this cohort 10 years later. The study included individuals aged 15 years and older from 384 randomly selected houses from three urban districts of the Bandim Health Project's study area in the capital Bissau. All interviews were conducted and blood samples collected between May 2004 and January 2007. Serum samples from 2547 participants were examined in the National Public Health Laboratory by a screening assay for antibodies to HTLV-1 and HTLV-2 (Murex Diagnostics Limited, Dartford, UK). Confirmation and discrimination of the presence of type-specific antibodies was tested using INNO-LIA HTLV-I/II score test (Innogenetics NV, Ghent, Belgium). Blood samples were also tested for HIV-1 and HIV-2 as described elsewhere [5].

The HTLV-1 prevalence was found to be 2.3% (Table 1). The prevalence was lower in men, with the female/male prevalence ratio being 1.77 [95% confidence interval (CI) = 0.98–3.21] adjusted for age and HIV-status. The incidence between 1996 and 2006 was only 0.9/1000 person-years and was higher for women than for men (likelihood ratio test, P = 0.03). The HTLV prevalence for HIV-positive individuals was 2.7-fold higher relative to HIV-negative participants among both sexes, with a slightly higher prevalence among HIV-2 infected individuals. The prevalence of HTLV infection increased equally with age for both sexes [trend: 1.04 (95% CI = 1.02–1.05) per year], and it was three-fold higher for participants 45 years of age or older compared with younger participants (Table 1).

Table 1
Table 1
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The prevalence of HTLV-1 had earlier been estimated to be 3.6% (76/2127) [4]. However, 11 (0.5%) did not have a confirmed test for HIV seroconversion. We restricted our analyses to the 2116 participants, who had confirmed HIV tests in 1996; 940 men and 1176 women, with a median age of 28 years (minimum 15, maximum 88), the same as in 2006 (P = 0.16). In 1996, the prevalence was 3.4% (72/2116). In 2006, the prevalence declined significantly with 34% (prevalence ratio = 0.66; 95% CI = 0.47–0.94) to 2.3%. The median age of HTLV-infected had increased from 36.5 years in 1996 to 39 years in the last survey (P = 0.68). The decline in HTLV prevalence was equal for men and women, for older (45+ years) and young individuals, as well as for HIV-negative and positive individuals. However, the decline tended to be stronger for HIV-1 (dual infections included)-infected individuals (prevalence ratio = 0.22; 95% CI = 0.07–0.74) than for HIV-2-single-infected individuals (prevalence ratio = 0.88; 95% CI = 0.39–1.97; P = 0.09). In 1996, the prevalence of HTLV among persons who have had a history of blood transfusion was 2.37 (95% CI = 1.07–5.27) fold higher than for those who had not received blood. In 2006, a history of blood transfusion was no longer a risk factor. The prevalence had decreased significantly between 1996 and 2006 among individuals with a history of blood transfusion (prevalence ratio = 0.11, 95% CI = 0.01–0.91).

The pattern of relatively higher prevalence among women has also been reported in two studies from 1996 and 2000 in a community-based cohort in Guinea-Bissau [4,6], from Benin [1,2] and from several other studies of HTLV infection from West Africa. We observed a three-fold higher prevalence for persons 45 years of age or older compared with younger persons. An increased prevalence of HTLV-1 with age has also been observed in studies of blood donors in Senegal, specifically in the southern part of Senegal bordering Guinea-Bissau [7]. The increased prevalence of HTLV-1 infection with age has also been reported in a study of pregnant women from Guinea-Bissau [8]. However, all five new infections of HTLV in this cohort were among women who were younger than 45 years of age in 1996. Hence, as for HIV-1 infection, there may be a shift towards transmission of HTLV at a younger age [6].

As HTLV, HIV-2 has declined in Guinea-Bissau over the past 10 years, whereas HIV-1 has doubled in the same period [6]. This would suggest that it is not safer sex practices that have caused the decline. Hence, the question is why HTLV is no longer acquired by HIV-infected individuals. Screening for HTLV infection of blood donations has not been implemented in Guinea-Bissau. However, blood transfusions were undoubtedly important in the initial transmission of HIV-2 and HTLV was also associated with blood transfusions. Once transfusions were controlled for HIV infection, this source of combined HIV and HTLV infection would also have disappeared. It may be worth noting that the association with HIV-1 was mostly among individuals with dual HIV-1 and HIV-2 infections. For reasons that remain to be explained, dual infections have declined two-fold in this community over the past 10 years at the same time as HIV-1 single infection has increased three-fold [6]. This change may have contributed to the decline in HTLV.

Given the low prevalence and the unequal sex-distribution in the 15–24 years age group, it seems unlikely that maternal transmission contributes much to the prevalence of HTLV infection among adults. Previous studies from urban [4] and rural parts of the country [6] could not identify any association between HTLV-1-status and having an HTLV-seropositive mother. In this West African community, HTLV infection is probably mostly sexual and blood-borne after 15 years of age.

The results of this study indicate that HTLV-1 prevalence is declining and the high prevalence among older individuals may be a cohort effect. Given that it is a very inefficient sexual-transmitted infection, the HTLV-1 prevalence is likely to decline further.

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Acknowledgements

We are thankful to the laboratory technicians at the National Public Health Laboratory, field assistants and office staff at the Bandim DSS site for making this study possible. The study was supported by grants from the Danish International Development Agency (DANIDA)/ENRECA and Swedish International Development Cooperation Agency, Department for Research Cooperation (SIDA/SAREC).

The study was planned by Z.J. da S. and P.A. and executed by Z.J. da S. A.R. and I.O. were involved with supervision and interpretation of data. J.N. and A.A. were responsible for the statistical analyses. B.H. had carried out the previous cohort studies. S.A. and F.D. were responsible for the laboratory testing strategies. Z.J. da S. wrote the first draft and all authors contributed to the final version of the article.

Neither of the authors have a commercial or other association that might pose a conflict of interest.

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References

1. Dumas M, Houinato D, Verdier M, Zohoun J, Josse R, Bomis J, et al. Seropidemiology of human T-cell lymphotropic virus type I/II in Benin (West Africa). AIDS Res Hum Retroviruses 1991; 7:447–451.

2. Houinato D, Verdier M, Josse R, Zohoun T, Letenneur L, Salamon R, et al. Seroepidemiological study of retroviruses (HTLV I/II, HIV-1, HIV-2) in the Department of Atacora, Northern Benin. Trop Med Int Health 1996; 2:205–209.

3. Melbeye M, Poulsen AG, Gallo D, Pedersen JB, Biggar RJ, Larsen O, et al. HTLV-I infection in a population-based cohort of older person in Guinea-Bissau, West Africa: risk factors and impact on survival. Int J Cancer 1998; 76:293–298.

4. Larsen O, Andersson S, da Silva Z, Hedegaard K, Sandstrom A, Naucler A, et al. Prevalences of HTLV-1 infection and associated risk determinants in an urban population in Guinea-Bissau, West Africa. J Acquir Immune Defic Syndr 2000; 25:157–163.

5. da Silva ZJ, Oliveira I, Andersen A, Dias F, Rodrigues A, Holmgren B, et al. Changes in prevalence and incidence of HIV-1, HIV-2 and dual infections in urban area of Bissau, Guinea-Bissau: is HIV-2 disappearing? AIDS 2008; 22:1195–1202.

6. Holmgren B, Andersson S, Harding E, Schim van der Loeff M, Vastrup P, Aaby P, et al. Increased prevalence of HTLV-1 among HIV-2-infected women but not HIV-2-infected men in rural Guinea-Bissau. J Acquir Immune Defic Syndr 2002; 30:342–350.

7. Diop S, Calatini S, Abah-Dakou J, Thiam D, Diakhaté L, Gessain A. Seroprevalence and molecular epidemiology of human T-Cell leukemia virus type 1 (HTLV-1) and HTLV-2 in blood donors from Dakar, Senegal. J Clin Microbiol 2006; 4:1550–1554.

8. Andersson S, Dias F, Mendes PJ, Rodrigues A, Biberfeld G. HTLV-I and HTLV-II infections in a national survey of pregnant women in Guinea-Bissau, West Africa. J Acquir Immune Defic Syndr 1997; 15:320–322.

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