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Cervical Infection With Chlamydia trachomatis and Neisseria gonorrhoeae in Women From Ten Areas in Four Continents: A Cross-Sectional Study

Franceschi, Silvia MD*; Smith, Jennifer S. PhD†; van den Brule, Adriaan PhD‡; Herrero, Rolando MD§; Arslan, Annie BS*; Anh, Pham-thi-hoang MD∥; Bosch, F Xavier MD¶; Hieu, Nguyen-trong MD**; Matos, Elena MD††; Posso, Hector MD‡‡; Qiao, You-lin MD§§; Shin, Hai-rim MD∥∥; Sukvirach, Sukhon MS¶¶; Thomas, Jaiye O. MD***; Snijders, Peter J. F. PhD†††; Muñoz, Nubia MD§§; Meijer, Chris J. L. M. MD§

Sexually Transmitted Diseases: August 2007 - Volume 34 - Issue 8 - pp 563-569
doi: 10.1097/01.olq.0000258417.66619.0e

Objectives: Better information on the prevalence of Chlamydia trachomatis (CT) and Neisseria gonorrhoeae (NG) infection is needed in many world areas.

Study Design: Cross-sectional study of population-based samples of nonpregnant women aged 15 to 44 years in Nigeria, Colombia, Argentina, Vietnam (2 areas), China, Thailand (2 areas), Korea, and Spain. 5,328 consenting women aged 15 to 44 years participated. Exfoliated cervical cells were collected and testing for CT and NG and human papillomavirus (HPV) was done using PCR-based assays.

Results: Age-standardized CT prevalence ranged between 0.2% (95% confidence interval, CI: 0.0–0.7%) in Spain and 5.6% (95% CI: 3.4–7.8%) in Nigeria. NG ranged between 0% (with broad CIs) in several areas and 2.6% (95% CI: 1.0–4.2%) in Nigeria. Prevalence of CT in all areas combined was greater in women aged 15 to 24 (4.5; 95% CI: 3.4–5.8%) than 25 to 44 (2.6; 95% CI: 2.1–3.1%), whereas NG prevalence was similar in the 2 age groups (0.3%). The only significant risk factors were NG infection (for CT), CT infection (for NG) and infection with high-risk HPV types (for both).

Conclusions: The prevalence of CT and, most notably, NG was relatively low in a variety of countries. Our findings, however, do not apply to subsets of high-risk women who are likely to be underrepresented in our population-based samples.

This manuscript shows a Chlamydia trachomatis (CT) prevalence ranging between 0.2% in Spain and 5.6% in Nigeria and an NG prevalence between 0% in Argentina, Vietnam (Hanoi), China, Thailand (Lampang), Korea, and Spain; and 2.6% in Nigeria.

From the *International Agency for Research on Cancer, Lyon, France; †Department of Epidemiology, University of North Carolina at Chapel Hill, Chapel Hill, North Carolina; ‡Laboratory for Pathology and Medical Microbiology, PAMM Institute, Eindhoven, The Netherlands; §Fundación INCIENSA, San José, Costa Rica; ∥National Cancer Institute, Hanoi, Vietnam; ¶Institut Català d’Oncologia, Barcelona, Spain; **Neonatology Department, Hung Vuong Hospital, Ho Chi Minh, Vietnam; ††Facultad de Medicina, Instituto de Oncología ′Angel H. Roffo′, Buenos Aires, Argentina; ‡‡Instituto Nacional de Cancerología, Bogota, Colombia; §§Department of Cancer Epidemiology, Cancer Institute/Hospital, Chinese Academy of Medical Sciences, Beijing, People’s Republic of China; ∥∥National Cancer Center Research Institute, Busan, Republic of Korea; ¶¶National Cancer Institute, Bangkok, Thailand; ***College of Medicine, University of Ibadan, Ibadan, Nigeria; and †††Department of Pathology, VU Medical Center, Amsterdam, The Netherlands

We thank Stephan van Schaick, Rick van Andel, Debby Boon, and Marjolein Lettink for COBAS AMPLICOR testing and Ms. Karima Abdedayem for skillful technical assistance.

This research has received financial support from the UNPD/UNFPA/WHO/World Bank Special Program of Research, Development, and Research Training in Human Reproduction, Department of Reproductive Health and Research, WHO, Project No. A15238, and the Bill & Melinda Gates Foundation (grant number 35537).

Correspondence: Dr. Silvia Franceschi, International Agency for Research on Cancer, 150 cours Albert Thomas, 69372 Lyon, Cedex 08, France. E-mail:

Received for publication July 4, 2006, and accepted November 22, 2006.

CHLAMYDIA TRACHOMATIS (CT) INFECTION is the most common bacterial sexually transmitted infection (STI). The World Health Organization (WHO)1 estimated that 50 million women worldwide were newly infected with CT in 1999, of which 34 million were in sub-Saharan Africa and South/Southeast Asia. CT infection is relatively common in developed countries as well, especially in women younger than 25 years2 ( CT infection is asymptomatic in 70 to 75% of infected women, can be transmitted during vaginal, oral, or anal sexual contact, and can be passed by the mother to her newborn during delivery, with subsequent risk of neonatal eye infection or pneumonia. Pelvic inflammatory disease, a serious complication of CT infection, is a major cause of infertility in women.1

Gonorrhoea is caused by Neisseria gonorrhoeae (NG), and approximately 34 million new infections were estimated to have occurred among women in 1999, of which over 24 million in sub-Saharan Africa and South/Southeast Asia.1 Similar to CT, 80% of women (though only 10% of men) infected with NG are asymptomatic, and the most common and serious complications of the infection are also pelvic inflammatory disease, ectopic pregnancy, and infertility.1

The comparison of the prevalence of CT and NG infections in different parts of the world is difficult due to the variety of surveillance methods used (i.e., passive vs. report-based surveillance systems) and the lack of reliable information from many world areas. Furthermore, accurate diagnosis of CT and NG infection requires relatively sophisticated equipment, which is costly and not always available in laboratories of developing countries. The current study of CT and NG infection was done in the framework of the International Agency for Research on Cancer (IARC) human papillomavirus (HPV) Prevalence Surveys,3 and tried to remedy these problems by obtaining samples of women from population lists using a standardized protocol and performing PCR-based assays for bacteria detection in a central laboratory.

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Materials and Methods

Study Subjects

Population-based surveys, the main aim of which was to evaluate the prevalence of HPV, were carried out by IARC between 1993 and 2004. Similar protocols were developed at the IARC in different areas in 4 continents, chosen to represent regions at low, intermediate, and high risk for cervical cancer4 and hence, for HPV, the primary cause of cervical cancer.5 In 10 such areas it was also possible to evaluate the prevalence of CT and NG infection.

Complete population sampling methods have been previously described for the individual areas: Nigeria, Ibadan6; Colombia, Bogota7; Argentina, Concordia8; Vietnam, Hanoi and Ho Chi Minh9; China, Shanxi Province10; Thailand, Songkla, and Lampang11; Korea, Busan12; and Spain, Barcelona.13 Briefly, in each area available population lists (e.g., census, mandatory family planning clinic lists, etc.) were used to obtain a random, age-stratified sample that included approximately 100 women in each 5-year age group from 15 to 19 to 65 and over. Participation ranged from 48 to 70% in Spain, Argentina, Korea, Thailand, Songkla, China, and Nigeria; 70 to 90% in Thailand, Lampang; and Vietnam, Ho Chi Minh; and it was over 90% in Colombia, and Vietnam, Hanoi. Only women in the 15- to 44-year age range were included in the current study of CT and NG infection, as the prevalence of these infections and their complications are highest in women of reproductive age.1

Exclusion criteria, according to our study protocol, were pregnancy at time of recruitment, previous hysterectomy, and mental or physical incompetence. In addition, as very few self-reported virgins underwent a gynecological exam, the following analyses were further restricted to those women who reported being sexually active. The questionnaire included information on sociodemographic characteristics, sexual habits, reproductive factors, and use of contraceptive methods. A total of 6699 women were included in the current study. All participants signed informed consent forms according to the recommendations of the IARC Ethical Review Committee, which approved the study.

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Gynecological Examination and Specimen Collection

All study participants underwent a pelvic examination performed by a gynecologist or trained nurse. Samples of exfoliated cells were collected from the ectocervix using two wooden Ayre spatulas and from the endocervix with one or more cytobrushes. After preparation of a cytologic specimen, spatulas and cytobrushes were placed in phosphate-buffered saline and stored on ice, or, in China, in Cytorich transport media (Tripath Imaging, Burlington, NC). Cells were vortexed and subsequently centrifuged at 3000g for 10 minutes. Resulting cell pellets were diluted in buffer and frozen between −20°C and −80°C until they were shipped to IARC in dry ice.

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Detection of CT and NG

The DNA that remained after HPV testing3,14 was not sufficient for any further testing among 564 women. In addition, 807 women who had a β-globin-negative cervical sample by PCR with β-globin gene-specific primers were excluded. Women who were excluded were similar to those who had an adequate sample in respect to distribution by age, education level, and number of sexual partners.

For the initial detection of CT and NG DNA, the commercially available COBAS AMPLICOR CT/NG system (Roche Diagnostic Systems, Branchburg, NJ) was used. This involves a PCR assay in which CT and NG DNAs are amplified in a multiplex setting together with an internal control, and PCR products are subsequently detected in separate steps in an automated COBAS AMPLICOR device (Roche Diagnostic Systems15) according to the manufacturer’s protocol. One hundred microliters of crude exfoliated cell extract was diluted into an equal volume of lysis mix (CT/NG specimen preparation kit; Roche Diagnostic Systems) and used for PCR following the recommended incubation steps. PCR was performed using reagents in the CT/NG amplification kit (Roche Diagnostic Systems), and for each amplification round, CT- and NG-positive and -negative controls were included. The Detection Reagents Kit, Internal Control Detection Kit, CT Detection Kit, NG Detection Kit, and Conjugate Detection Reagent (Roche Diagnostic Systems) were used for establishing CT and NG positivity. In case the internal control appeared negative, the assay was repeated on the respective samples using a 1 to 5 dilution of sample (i.e., 20 μL) in lysis mix (i.e., 80 μL).

Because of known false-positive results for NG in COBAS AMPLICOR,15 NG-positive samples were subsequently subjected to confirmation assays as recently described.16 Briefly, purified DNA was subjected to 2 NG-specific real-time PCR assays targeting either the 16S ribosomal DNA or the cpp gene of the cryptic plasmid. Assays were performed using LightCycler (Roche Molecular Systems) as previously described.16 Only samples that revealed positivity in the confirmation PCR assays (17/37, 45.9% of initially positive samples) were ultimately scored positive for NG. In contrast, all samples that were CT-positive at the COBAS AMPLICOR were considered positive.15

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HPV Detection

HPV testing was performed using GP5+/GP6+ PCR-based enzyme immunoassay that detected 36 HPV types.14,17 HPV types considered high-risk for this study were HPV 16, 18, 31, 33, 35, 39, 45, 51, 52, 56, 58, 59, 68, 73, and 82.18

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Statistical Methods

The prevalence of CT and NG infection and corresponding 95% confidence intervals (CIs) were compared across study areas in 3 age groups (15–24; 25–34; and 35–44 years). On account of similar and relatively low prevalence of CT and NG, the age groups 25 to 34 and 35 to 44 were combined in Table 1 to increase precision. All-age prevalence was age-standardized to the 15 to 44-year-truncated world standard population.4 Unconditional logistic regression was used to calculate odds ratios (ORs) and corresponding 95% CIs of CT and NG infection by selected women’s characteristics, with adjustment for 5-year age group and study area.

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The crude prevalence of CT and NG infection among 5328 women was 3.0 and 0.3%, respectively (data not shown). The corresponding age-standardized prevalences were 3.0% (95% CI: 1.7–4.4) and 0.4% (95% CI: 0.0–0.8) (Table 1, Fig. 1). The highest age-standardized prevalence of CT infection was found in Nigeria (5.6; 95% CI: 3.4–7.8%) and the lowest in Spain (0.2; 95% CI: 0.0–0.7%). CT infection was also detected relatively frequently in Colombia (5.0, 95% CI: 3.6–6.4%) and Argentina (5.0; 95% CI: 2.8–7.2%). The prevalence of NG infection was 2.6% (95% CI: 1.0–4.2) in Nigeria but it was 0 in Argentina; Vietnam, Hanoi; China; Thailand, Lampang; Korea; and Spain, with broad corresponding 95% CIs (Table 1).

In respect to age group, the highest prevalence was found in women below 25 years of age for CT infection (4.5; 95% CI: 3.4–5.8 vs. 2.6; 95% CI: 2.1–3.1 at age 25–44) whereas for NG infection prevalence was similar at age 15 to 24 (0.3; 95% CI: 0.1–0.8%) and 25 to 44 (0.3; 95% CI: 0.2–0.5%, Table 1). The difference in the prevalence of CT infection between women aged 15 to 24 and those aged 25 to 44 was, however, 2-fold or more in Colombia; Vietnam, Ho Chi Minh; Thailand, Lampang; and Spain, but less strong elsewhere. Notably CT infection was similarly frequent in the 2 age groups considered in Nigeria; Vietnam, Hanoi; China; and Thailand, Songkla. In Nigeria, NG infection was more common at age 25 or more than among younger women.

Table 2 shows the association between CT or NG infection, age group and selected women’s characteristics. Only 4 study areas could be retained in the analyses of factors related to NG infection as the infection was not found elsewhere (Table 1). A significant inverse relationship was found between age group and CT (χ21, for trend = 9.41; P = 0.002) but not NG infection (χ21, for trend = 1.32; P = 0.25). Education level, marital status, lifetime number of sexual partners, partner’s extramarital sexual relationships, parity, and use of hormonal contraceptives, condom, and intrauterine device (IUD) were not significantly related to either CT or NG infection. Direct associations of borderline statistical significance were found, however, between CT infection and being divorced rather than married (OR = 1.9; 95% CI: 0.9–3.6) and reporting 2 (but not 3) lifetime sexual partners rather than 1 (OR = 1.5; 95% CI = 1.0–2.4).

Women with NG infection had a 9-fold (95% CI: 3.0–27.5) increased risk of being infected with CT and vice versa (95% CI: 2.9–26.6) (Table 3). Positivity to high-risk but not low-risk, HPV types was also a risk factor for CT (OR = 1.5; 95% CI: 1.0–2.4) and NG (OR = 6.4; 95% CI: 2.3–17.8) infection (Table 3).

Prevalences of CT and high-risk HPV types in different study areas were positively correlated (Pearson correlation coefficient = 0.75) (Fig. 2), but there were some exceptions. In Vietnam, Hanoi, the prevalence of HPV was as low as in Spain, but the age-standardized prevalence of CT was over 10-fold higher and similar to the one found in Vietnam, Ho Chi Minh, an area at much higher risk for high-risk HPV than Vietnam, Hanoi. In contrast, a relatively high prevalence of high-risk HPV types in women in Korea was accompanied by a low prevalence of CT infection. The correlation between the prevalence of high-risk HPV types and NG in study areas was weaker (Pearson correlation coefficient = 0.48, data not shown) than the correlation with CT.

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Our present population-based study confirmed that cervical CT infection is relatively common in Africa and Latin America (≥5.0% of women affected), but it was found in ≤2% of women in China, Thailand, and from the highest-income countries in our study (Korea and Spain). The prevalence of NG infection in all our study populations combined was 10-fold lower than CT infection: NG prevalence was ≤0.5% in all study areas except Nigeria and Thailand, Songkla. A similar difference between the prevalence of CT and NG was reported in the United Kingdom,2 the United States,19 and South Africa,20 but it may be partly due, in some countries,21 to greater screening efforts for CT than NG.

Our present findings on CT and NG infection are consistent with previous reviews of published and unpublished medical literature on the prevalence of STIs in low-risk women from 15 to 49 years of age, as well as WHO estimates.1,22 The review by Gerbase et al.22 was restricted to pregnant women, women attending family planning clinics, and blood donors, and showed, for instance, that the prevalence of CT infection was 7.1% in sub-Saharan Africa, 4.0% in Latin America, and 0.7% in East Asia and the Pacific. The corresponding prevalences for NG were 2.8, 1.1, and 0.1%, respectively.

A comparison of the prevalence of CT (2.7%) and NG (0.2%) infection in Western Europe22 with our findings is not possible as information was only available from Spain. A systematic review of 14 studies published between 1950 and 200023 showed that the prevalence of CT infection in European women varied between 1.0% in Spain to over 6.0% in France, the United Kingdom, and Bulgaria. Our findings from Thailand and Vietnam are lower than the prevalences of CT (4.9%) and NG (1.4%) infection shown for South/Southeast Asia in a WHO report, which included, however, areas at higher risk for STIs, such as India.1

We have also been able to evaluate the association of CT and NG prevalence with several women’s characteristics and the prevalence of HPV, the most common viral STI.5 An association with age below 25 years was found for CT but not NG. It is, however, worth noting that the marked excess of CT infection in adolescent and young women that is typically found in developed countries24 ( did not clearly emerge in many of our study areas (e.g., Nigeria, Vietnam, Hanoi, China, Thailand, Songkla). We have already reported that also for HPV prevalence age-specific curves vary from one population to another.3 Thus, age-specific patterns of sexual behavior of women and their sexual partners may vary substantially and, in some parts of the world, women 25 to 44 years old may not be exposed less often to CT infection than women below age 25.

The lack of significant association between current CT and NG infection and available indicators of sexual behavior may be due in part to inaccuracies in the self-reported number of sexual partners and male partner’s extramarital relationships and the absence of some relevant information (e.g., history of recent sexual partners). Other studies,24 however, have shown that sexual risk factors contributed little to predicting CT infection, and our current study had low statistical power to detect weak and moderate associations.

In light of some concerns that have been expressed on the topic25–27 it is reassuring that our study did not disclose any unfavorable effect of use of hormonal contraceptives or IUD on the prevalence of either CT or NG infection. About condom use, there was a hint of an inverse association between ever-use and CT and, more clearly, NG infection. Although the 95% CIs of the ORs were broad and condom use was not reported in detail, our findings are thus compatible with the significant protection against CT or NG infection reported for consistent condom use.28,29

Infection with high-risk HPV types, although not with low-risk types, was a risk factor for CT and NG infection risk: Approximately one-fifth of CT-infected women and half of NG-infected women were positive for high-risk HPV types. Previous studies showed that concurrent CT infection is associated with 6-month persistence of high-risk HPV types30 and past CT infection is associated with cervical cancer risk after adjustment for HPV infection31 or restriction to HPV-positive women.32 However, when the prevalence of CT and high-risk HPV types in each study area were compared it was clear that, at a population level, there were areas (e.g., Vietnam Hanoi) where CT is relatively common but high-risk HPV types are rarely detected and others (e.g., Korea) where CT infection is rare but high-risk HPV types are frequently found. These findings are exemplars of the fact that STIs may have distinct epidemic patterns across populations.

The current study has strengths as well as weaknesses. Many hundreds of women were examined in every location and all cervical samples were tested for CT and NG infection using a sensitive validated PCR-based system that included confirmatory testing for NG and was performed in a centralized laboratory. A systematic review of diagnostic tests for the detection of CT showed that DNA amplification techniques have higher sensitivity than conventional tests (e.g., enzyme immunoassays33). Falsely positive findings for NG infection were ruled out by means of a confirmation assay.16

More importantly, our study did not rely on opportunistic samples of women self-referred to various types of clinic but instead identified them using population-based lists. The main cause for lack of participation was not women’s refusal but the impossibility of finding women due to the inaccuracies of population lists available, which were not up-to-date in many study areas.3 The use of cytobrushes in our study was dictated by the need to obtain cytologic smears14 and is not currently considered practical in broad-based population surveys of CT and NG infection, as it requires a pelvic examination. Cervical cytobrushes allow to achieve levels of sensitivity for CT detection that were equivalent to vaginal swabs and superior to cervical swabs34,35 and first-catch urine samples.36

Weaknesses of our study include the limited number of geographic areas available and, on account of the relatively low prevalence of CT and NG infection detected, the relatively small number of infected women available in each center. Thus the prevalence of infection and the ORs for possible risk factors, most notably for NG infection, have broad 95% CIs.

In conclusion, whereas our findings can be considered a reliable estimate of the prevalence of CT and NG in the general female population of the areas under study, it should be born in mind that they may not apply to subsets of the populations that could not be included in our surveys (e.g., pregnant women, women who did not have a permanent address or were unwilling to admit to be sexually active or to undergo gynecological examination). Hence our findings do not undermine the necessity of programs of prevention and control of STIs in the countries under study.

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