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Vol. 16. Issue 4.
Pages 335-338 (July - August 2012)
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Vol. 16. Issue 4.
Pages 335-338 (July - August 2012)
Original article
Open Access
Chlamydia trachomatis infection among HIV-infected women attending an AIDS clinic in the city of Manaus, Brazil
Leila Cristina Ferreira Silvaa,
Corresponding author

Corresponding author at: Fundação de Medicina Tropical do Amazonas, Rua Pedro Teixeira, 25, Dom Pedro, Manaus, Amazonas, 69040-000, Brazil.
, Angélica Espinosa Mirandab, Rosieny Santos Batalhaa, Carolina Sabinoa, Elizabeth Cristina Dantas Diba, Carolina Marinho da Costaa, Rajendranath Ramasawmya, Sinésio Talharic
a Fundação de Medicina Tropical do Amazonas, Manaus, AM, Brazil
b Infectious Diseases Division, Universidade Federal do Espírito Santo, Vitória, ES, Brazil
c Postgraduate Course in Tropical Medicine, Universidade Estadual Amazonas, Manaus, AM, Brazil
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Tables (2)
Table 1. Demographic and behavioral characteristics of the 329 participating HIV-infected women, attendees of the service of specialized care for AIDS in Manaus, Amazonas, Brazil.
Table 2. Clinical characteristics of the 329 participating HIV-infected women, attendees of the service of specialized care for AIDS in Manaus, Amazonas, Brazil.
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This was a cross-sectional study aimed to determine the prevalence of and to identify risk factors for Chlamydia trachomatis (CT) among human immunodeficiency virus (HIV)-infected women attending the acquired immunodeficiency syndrome (AIDS) clinic in the city of Manaus, Brazil, in 2009-2010. Participants answered a questionnaire containing demographic, epidemiological, and clinical data. A genital specimen was collected during examination to detect CT-DNA by hybrid capture, and blood samples were taken to determine CD4+T and HIV viral load. There were 329 women included in the study. Median age was 32 years (IQR=27-38) and median schooling was nine years (IQR=4-11). The prevalence of CT was 4.3% (95%CI: 2.1-6.5). Logistic regression analysis showed that age between 18-29 years [OR=4.1(95%CI: 1.2-13.4)] and complaint of pelvic pain [OR=3.7 (95%CI: 1.2-12.8)] were independently associated with CT. The use of condom was inversely associated with CT [OR=0.39 (95%CI: 0.1-0.9)]. The results showed that younger women who did not use condoms are at a higher risk for CT. Screening for sexually transmitted infections must be done routinely and safe sexual practices should be promoted among this population.

Chlamydia trachomatis
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Chlamydia trachomatis (CT) infection in the genitourinary tract is the most prevalent bacterial sexually transmitted disease (STD) worldwide.1 Genital chlamydial infection has a huge impact on sexual and reproductive health, and it is very common in developed and developing countries.2–4 In developed countries such as the United States and the United Kingdom, CT is the most commonly diagnosed bacterial sexually transmitted infection (STI) among adolescents and young adults.5,6 In Brazil, a high prevalence of CT is observed in the female population. Screening of CT in pregnant women in Brazil showed a prevalence of nearly 10%.7,8

In general, STIs increase the risk of HIV transmission and are associated with more severe and earlier symptoms in human immunodeficiency virus (HIV) infected patients. The control of these infections represents a unique opportunity to improve reproductive health of women living with HIV.9 Both ulcerative and non-ulcerative STIs increased the risk of HIV transmission by three to ten times, depending on the type and etiology of the STD.9 HIV-infected individuals affected by an STI have increased viral load in genital secretions,10,11 thereby increasing considerably their potential of infectiousness and transmission.

Some studies showed that the prevalence of CT among HIV-infected women ranges from 2% to 10%.12–15 In Brazil, a study conducted in Rio de Janeiro found a prevalence of 3% for CT among HIV-infected women.13 The aim of the current study was to determine the prevalence of and risk factors associated with CT among HIV-infected women attending a referral center for the care of AIDS patients.

Material and methods

This is a cross-sectional study conducted among HIV-infected women who attended the service for specialized care for AIDS at the Fundação de Medicina Tropical Dr. Heitor Vieira Dourado (FMT-DHVD), Manaus city, state of Amazonas, Brazil, from June 2009 to June 2010. HIV-infected women aged 18 to 49 years, not pregnant, and with no history of hysterectomy were invited to participate in the study after signing an informed consent. The Ethical Committee for Research of the FMT-DHVD approved all of the procedures used in the study, which was filed under the Registration No. 327-09, 06/04/2009. HIV-infected women diagnosed with CT during the study were provided treatment in accordance with the Manual of STI Control Program of the Ministry of Health of Brazil.

An individual interview for all of the participants of the study was conducted to complete a standardized questionnaire containing sociodemographical, epidemiological, and clinical data. Each participant also underwent a clinical and gynecological examination for genital specimen collection for bacterioscopy, cytology, and the detection of CT DNA by hybrid capture (QIAGEN Group Corporation). A 5mL blood sample was also collected for the determination of HIV viral load and CD4+ T-cell counts.

The sample size calculation was based on an average frequency of CT of 5% (95% CI, β=2%-8%).12–15 The required number of participants was 292. Considering a loss of 20%, the final sample size was estimated as 350.

A descriptive analysis was performed for the sociodemographic, sexual history, and behavioral covariates. The frequency distribution for qualitative variables and the median and interquartile range (IQR) for quantitative variables were calculated. The prevalence of CT was estimated along with the corresponding 95% confidence interval (CI). The chi-square test with Yates’ correction was used to assess possible associations between demographic variables and CT positivity. Fisher's exact test was applied when appropriate. Multivariate logistic regression analysis was applied to examine the independent effect of each demographic or risk variable for CT diagnosis. All variables that were moderately associated (p0.10) were considered for inclusion in the multivariate model. In the final analysis, variables with a non-significant association (p>0.05) were removed from the model.


A total of 329 (94%) HIV-infected women participated in the study. The median age was 32 years with an interquartile range (IQR) of 27 to 38. The median of years of schooling was nine years (IQR=4-11). The overall prevalence of CT was 4.3% (95% CI; 2.1%-6.5%).

The sociodemographic and behavioral characteristics of the women in the current study are shown in Table 1. HIV-infected women with positive hybrid capture for CT were younger (18–29 years) than those with a negative test (64.3 vs. 33.7%, p=0.049). The use of illicit drugs was also more common in CT-infected than non-infected women (35.7% vs. 14.3%, p=0.029).

Table 1.

Demographic and behavioral characteristics of the 329 participating HIV-infected women, attendees of the service of specialized care for AIDS in Manaus, Amazonas, Brazil.

Variables  CT positive  CT negative  p-value 
  n (%)  n (%)   
Age (years)       
18 to 29  9 (64.3)  106 (33.7)  0.049 
30 to 39  3 (21.4)  147 (46.7)   
40 or more  2 (14.3)  62 (19.7)   
Years of schooling       
≤ 4  2 (14.3)  84 (26.7)  0.771 
5 to 8  4 (28.6)  73 (23.2)   
9 or more  8 (57.1)  158 (50.2)   
Age first sexually active       
≤ 15 years  6 (42.9)  150 (47.6)  0.727 
>15 years  8 (57.1)  165 (95.4)   
Partner change in past 12 months       
12 (85.7)  275 (87.3)  0.696 
>2 (14.3)  40 (12.7)   
History of STI       
Yes  5 (35.7)  95 (30.2)  0.658 
No  9 (64.3)  220 (69.8)   
Sexual worker       
Yes  2 (14.3)  50 (15.9)  0.874 
No  12 (85.7)  265 (84.1)   
Condom use       
Yes  8 (57.1)  225 (71.4)  0.081 
No  6 (42.9)  90 (28.6)   
Illicit drug use       
Yes  5 (35.7)  45 (14.3)  0.029 
No  9 (64.3)  270 (85.7)   

The median CD4+T cell count and viral load were 338.5 (IQR=211.5 - 513.3) cells/mm3 and 497.5 (IQR=49-11,288) copies/mm3 respectively. The clinical data of the participants are described in Table 2. A total of 261 HIV-infected women (79.3%) were classified as AIDS patients. The report of pelvic pain was more prevalent among CT-infected than non-infected women (78.6% vs. 50.5%, p=0.040).

Table 2.

Clinical characteristics of the 329 participating HIV-infected women, attendees of the service of specialized care for AIDS in Manaus, Amazonas, Brazil.

Variables  CT positive  CT negative  p-value 
  n (%)  n (%)   
Pelvic pain       
Yes  11 (78.6)  159 (50.5)  0.040 
No  3 (21.4)  156 (49.5)   
Vaginal discharge       
Yes  10 (71.4)  172 (54.6)  0.215 
No  4 (28.6)  143 (45.4)   
Genital bleeding       
Yes  1 (7.1)  32 (10.2)  0.956 
No  13 (92.9)  283 (89.8)   
Burning micturition
Yes  4 (28.6)  72 (22.9)  0.620 
No  10 (71.4)  243 (77.1)   
Recent use of antibiotics
Yes  2 (14,3)  68 (21.6)  0.742 
No  12 (85,7)  247 (78.4)   
CD4 T cell count (cells/mm3)
≤ 200  2 (14.3)  68 (21.6)  0.724 
201 to 349  5 (35.7)  94 (29.8)   
350 to 500  3 (21.4)  69 (21.9)   
>500  4 (28.6)  84 (26.7)   
Viral load (copies/mL)
≤ 1000  6 (42.9)  176 (55.9)  0.098 
>1000  8 (57.1)  139 (44.1)   
Infection status       
HIV  12 (85.7)  249 (79.0)  0.547 
AIDS  2 (14.3)  66 (21.0)   

The final multivariate logistic regression model showed that age (18 to 29) [OR=4.1 (1.2 to 13.4)] and report of pelvic pain [OR=3.7 (1.2 to 12.8)] were independently associated with CT positivity. Condom use was inversely associated with CT [OR=0.39 (0.1-0.9)].


The prevalence of CT among HIV-infected women in the current study was 4.3%. This is in line with reports from Rio de Janeiro (Brazil) and Mombasa (Kenya) where a prevalence of CT of 3% and 3.2%, respectively, was observed among HIV-infected women.3,16 However, this prevalence is lower than that found among pregnant and parturient women in Brazil,7,8 and that observed (9.7%) among HIV-infected women in Thailand.15

An association of CT with younger age (18-29 years), with pelvic pain, and with unprotected sex (no condom use) was observed. Similar findings have been reported in other studies.6–8,17–19 Young women are the most heavily affected by CT. Early onset of sexual activity, having more than one partner, and practice of unprotected sex further intensify the risk of CT.20

Although cross-sectional studies are not ideal for determining risk factors, their application is justified for assessing the prevalence of and the associated factors for CT among HIV-infected women, especially at their age of highest fecundity. It is of utmost importance to demonstrate the vulnerability of this group of women to the complications of this infection in women's health. In this study, the possibility of response bias cannot be ruled out. There is always a general tendency to give socially acceptable answers. Moreover, the sensitivity of the hybrid capture test for CT is lower than the test based on nucleic acid amplification. This may lead to an underestimation of the prevalence. Conversely, the prevalence observed in the current study may be higher as HIV women seeking care at the clinics are potentially at higher risk for sexually transmitted infections.

Chlamydial infection is often asymptomatic. If CT is not detected by screening, it is unlikely to be reported. Due to the lack of specific symptoms, CT diagnosis is rarely considered. Approximately 70% to 80% of individuals with CT remain asymptomatic and undiagnosed.21 This renders the control of the spread of CT difficult as most of the asymptomatic patients are unaware of their status and do not seek treatment. The limited availability of laboratory tests for diagnosis of CT in Brazil further complicates the matter. CT can cause genitourinary infections, pelvic inflammatory disease, chronic pelvic pain, tubal-factor infertility, ectopic pregnancy and cervical cancer.19,22 Infection during pregnancy and childbirth can trigger preterm labor, ruptured membranes, and low birth weight.23,24 Infants born from mothers with CT can be infected during delivery through the birth canal and may present conjunctivitis and pneumonia.25 In patients with HIV, the co-infection with CT may prolong/or increase their potential of infectiousness, facilitating the transmission of HIV, and this epidemiological synergy may be responsible for the increased transmission of HIV in some populations.26

It is well known that when interventions in health services are effectively implemented, the quality of care is improved and consequently the condition of sexual and reproductive health, thereby avoiding complications and having positive effect in the control of the spread of STIs.27,28 The service of specialized care for HIV women must be aware of the need for STI screening in this vulnerable and high risk population.

Conflict of interest

All authors declare to have no conflict of interest.

Global strategy for intervention and control of sexually transmitted infections: 2006-2015.
World Health Organization, (2007),
K.A. Fenton, C.M. Lowndes.
Recent trends in the epidemiology of sexually transmitted infections in the Europe Union.
Sex Transm Infect, 80 (2004), pp. 255-263
D.S. LaMontagne, L.E. Patrick, D.N. Fine, J.M. Marrazzo.
Re-evaluating selective screening criteria for chlamydial infection among women in the US Pacific Northwest.
Sex Transm Dis, 31 (2004), pp. 283-289
C.T. Da Ros, C.S. Schmitt.
Global epidemiology of sexually transmitted diseases.
Asian J Androl, 10 (2008), pp. 110-114
CDC - Centers for Diseases Control and Prevention.
Chlamydia screening among sexually active young female enrollees of health plans - United States, 2000-2007.
MMWR Morb Mortal Wkly Rep, 58 (2009), pp. 362-365
E.J. Adams, A. Charlett, W.J. Edmunds, G. Hughes.
Chlamydia trachomatis in the UK: a systematic review and analysis of prevalence studies.
Sex Transm Infect, 80 (2004), pp. 354-362
E.M. Jalil, V.M. Pinto, A.S. Benzaken, et al.
Prevalência da infecção por clamídia e gonococo em gestantes de seis cidades brasileiras.
Rev Bras Ginecol Obstet, 30 (2008), pp. 614-619
V.M. Pinto, C.L. Szwarcwald, C. Baroni, L.L. Stringari, L.A. Inocêncio, A.E. Miranda.
Chlamydia trachomatis prevalence and risk behaviors in parturient women aged 15 to 24 in Brazil.
Sex Transm Dis, 38 (2011), pp. 957-961
J.N. Wasserheit.
Epidemiological synergy: Interrelationships between human immunodeficiency virus infection and other sexually transmitted diseases.
Sex Transm Dis, 19 (1992), pp. 61-77
R.H. Gray, M.J. Wawer, R. Brookmeyer, et al.
Probability of HIV-1 transmission per coital act in monogamous, heterosexual, HIV-1-discordant couples in Rakai, Uganda.
Lancet, 357 (2001), pp. 1149-1153
P.D. Ghys, K. Fransen, M.O. Diallo, et al.
The associations between cervicovaginal HIV shedding, sexually transmitted diseases and immunosuppression in female sex workers in Abidjan, Cote d’Ivoire.
AIDS, 11 (1997), pp. F85-F93
S. Scheer, P.L. Chu, J.D. Klausner, et al.
Effect of highly active antiretroviral therapy on diagnoses of sexually transmitted diseases in people with AIDS.
B. Grinsztejn, F.I. Bastos, V.G. Veloso, et al.
Assessing sexually transmitted infections in a cohort of women living with HIV/AIDS, in Rio de Janeiro, Brazil.
Int J STD AIDS, 17 (2006), pp. 473-478
S.E. Manning, M.R. Pfeiffer, D. Nash, et al.
Incident sexually transmitted infections among persons living with diagnosed HIV/AIDS in New York City, 2001e2002: a population-based assessment.
Sex Transm Dis, 34 (2007), pp. 1008-1015
S. Srifeungfung, A. Roongpisuthipong, S. Asavapiriyanont, et al.
Prevalence of Chlamydia trachomatis and Neisseria gonorrhoeae in HIV-seropositive patients and gonococcal antimicrobial susceptibility: an update in Thailand.
Jpn J Infect Dis, 62 (2009), pp. 467-470
R.W. Gitau, S.M. Graham, L.N. Masese, et al.
Effect of acquisition and treatment of cervical infections on HIV-1 shedding im women on antiretroviral therapy.
F.E. Skjeldestad, M.A. Marsico, H.L. Sings, A.S. Nordbo, G. Storvold.
Incidence and risk factors for genital Chlamydia trachomatis infection: a 4-year prospective cohort study.
Sex Transm Dis, 36 (2009), pp. 273-279
A.E. Miranda, C.L. Szwarcwald, R.L. Peres, K. Page-Shafer.
Prevalence and risk behaviors for chlamydial infection in a population-based study of female adolescents in Brazil.
Sex Transm Dis, 31 (2004), pp. 542-546
I.J. Bakken, S. Ghaderi.
Incidence of pelvic inflammatory disease in a large cohort of women tested for Chlamydia trachomatis: a historical follow-up study.
BMC Infect Dis, 9 (2009), pp. 130
C. Bébéar, B. de Barbeyrac.
Genital Chlamydia trachomatis infections.
Clin Microbiol Infect, 15 (2009), pp. 4-10
W.C. Miller, C.A. Ford, M. Morris, et al.
Prevalence of chlamydial and gonococcal infections among young adults in the United States.
JAMA, 291 (2004), pp. 2229-2236
K.L. Wallin, F. Wiklund, T. Luostarinen, et al.
A population-based prospective study of Chlamydia trachomatis infection and cervical carcinoma.
Int J Cancer, 101 (2002), pp. 371-374
W.W. Andrews, R.L. Goldenberg, B. Mercer, et al.
The preterm prediction study: association of second-trimester genitourinary Chlamydia infection with subsequent spontaneous preterm birth.
Am J Obstet Gynecol, 183 (2000), pp. 662-668
M. Wilkowska-Trojniel, B. Zdrodowska-Stefanow, I. Ostaszewska-Puchalska, et al.
The influence of Chlamydia trachomatis infection on spontaneous abortions.
Adv Med Sci, 28 (2009), pp. 1-5
J.F. Peipert.
Genital chlamydial infections.
N Engl J Med, 349 (2003), pp. 2424-2430
N. Chkhartishvili, N. Dvali, G. Khechiashvili.
High seroprevalence of Chlamydia trachomatis in newly diagnosed human immunodeficiency virus patients in Georgia.
Georgian Med News, (2010), pp. 12-16
J.E. Norman, O. Wu, S. Twaddle, et al.
An evaluation of economics and acceptability of screening for Chlamydia trachomatis infection, in women attending antenatal, abortion, colposcopy and family planning clinics in Scotland, UK.
P. Sangani, G. Rutherford, G.E. Kennedy.
Population-based interventions for reducing sexually transmitted infections, including HIV infection.
Cochrane Database Syst Rev, (2004), pp. CD001220
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The Brazilian Journal of Infectious Diseases

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