Sexually Transmitted Diseases:
Chlamydia in the Pacific Region, the Silent Epidemic
Cliffe, Susan J. PhD*; Tabrizi, Sepehr PhD†‡; Sullivan, Elizabeth A. MPH*; on behalf of the Pacific Islands Second Generation HIV Surveillance Group
From the *Perinatal and Reproductive Epidemiology and Research Unit, School Women’s and Children’s Health at the University of New South Wales, Randwick, New South Wales; †Department of Microbiology and Infectious Diseases, The Royal Women’s Hospital, Carlton; and ‡Department of Obstetrics and Gynaecology, University of Melbourne, Parkville, Victoria, Australia
The following individuals contributed to the surveys in Pacific Island Countries. Fiji: Timaima Tuiketei, Sophaganine Ty Ali, Eseroma Rausuvanua, Litiana Raikuna, Aliote, Galuvakadua, Leone Tupua, Sereima Lala and Apaitia Seru. Kiribati: Kabwea Tiban, Mamao Robate, Lauren Kandt, Tebuka Toatu, Rosemary Tekoaua, Andrew Tekanene, Barieti Itaaken, Bernard P. Tatireta, Benina Tauman, Tekaibeti Tarataake, Takeieta B. Kienene, Tekaniuea Uriam, Brown Nataua, Angibwebwe Toromon, Tooreka Etuati, Komera Otea, Kabunateiti Teabo, and Tinai I Metai. Samoa: Leuluaialii Perive Lelevaga, Vaialia Iosua, Doris Kwan, Sera Vaafuti, Sione Tamalii, Faafouina Mafua, Valeliano Levi, Kaisarina Poloa, Lusi Aiolupo, Sara Filemu, ALpati Anoia, Mariana Penitito, Iakopo Vito, Vaomalo Ulu Kini, Puipuia Alaelua, Leofao Lafoga, Fiapaipai Tanea, Saine Alo Vaai, Asaua Faasino, Elisapeta Pasa-Anesone, and Namulauulu Nuualofa Tuuau Potoi. Solomon Islands: George Malefoasi, Amos Lapo, Nancy Kwalea, John Paulsen, Elliot Puiahi, Jeffrey Hii, Salesi Katoanga, Glenda Lapo, and Ricky Eddie. Tonga: Seini Kupu, Reynold ‘Ofanoa, Lesieli Halai, Makelesi Pole, Mafi ‘Ealelei, Taina Palaki, Vika Finau, Iunisi Uhi, Lesieli ‘Uluheua, Saia Penitani, Naomi Fakauka, Telesia Talia’uli, Taukei Halauafu, Nukonuka Mafile’o, Meleane Kava, Lesieli Vanisi, Semisi Latu, Aivi Puloka, and Niklas Danielsson. Vanuatu: Marina Laklotal, Timothy Phatu, George Taleo and Ross Seya.
The Global Fund to Fight AIDS, Tuberculosis and Malaria funded the Second Generation Surveillance Surveys of HIV, other STIs, and risk behaviors in 6 Pacific Islands Countries. The World Health Organization Western Pacific Regional Office funded technical support provided by the University of New South Wales supporting the implementation of the Second Generation Surveillance Surveys of HIV, other STIs, and risk behaviors in 6 Pacific Islands Countries.
This project was part of a regional proposal for HIV/STI surveillance covering 6 PICTs which received money from the Global Fund to Fight AIDS Tuberculosis & Malaria (GFATM).
E.A.S. contributed to the design of the survey and oversaw analysis of results. S.C. performed the statistical analyses and was lead author of the article. S.T. contributed to survey design and was responsible for laboratory analyses. All authors contributed to interpretation of results and the write up of the article.
Correspondence: Dr. Elizabeth A. Sullivan, MPH, Perinatal and Reproductive Epidemiology and Research Unit at the University of New South Wales, Level 2, McNevin Dickson Building, Gate 6, Avoca Street, Randwick Hospitals Campus, Randwick, NSW 2031, Australia. E-mail: firstname.lastname@example.org.
Received for publication December 8, 2007, and accepted March 18, 2008.
Background: Second generation surveillance of HIV infection and sexually transmitted infections (STIs) among pregnant women in 6 Pacific Island Countries and Territories were undertaken to improve knowledge and to make recommendations on future prevention and management of STIs.
Methods: Cross-sectional studies, using standardized questionnaire, laboratory tests, and protocols were undertaken in Fiji, Kiribati, Samoa, Solomon Islands, Tonga, and Vanuatu between 2004 and 2005. For each country, between 200 and 350 pregnant women aged 15 to 44 years were consecutively recruited from antenatal clinics located in the main hospital of the major urban centre of each Pacific Island Countries and Territories. Consenting participants were interviewed about their socio-demographic characteristics and their sexual behavior, and were tested for HIV, chlamydia, syphilis (Treponema pallidum antibody seroactivity), and gonorrhoea.
Results: Amongst the 1618 pregnant women studied, the most prevalent STI was chlamydia with 26.1% of women under 25 and 11.9% of women aged 25 years and over being positive. Highest infection was detected in single teenage women with 38.1% positive for chlamydia. The overall prevalence of gonorrhoea and syphilis was 1.7% and 3.4%, respectively. No case of HIV was detected. Chlamydia infection was independently associated with younger age, being nulliparous, single status, multiple lifetime sexual partners, and commercial sex activity.
Conclusion: In a population of young women, chlamydia infection was endemic. Regional leadership is needed to implement strategies to prevent the spread of chlamydia and to implement HIV and STI prevention and management.
RECENT SURVEYS HAVE CONFIRMED THAT sexually transmitted infections (STIs) in the Pacific are particularly prevalent. Previous surveys in Fiji, Vanuatu, and Samoa have found between 1 in 5 and 1 in 3 women to be infected with an STI,1–3 and rates were highest in young women. In contrast, reported HIV prevalence is low.1,2,4–6 Following years of neglect, the importance of STIs as a public health problem in the region needs to be acknowledged.
The emergence of HIV/AIDS has resulted in increasing focus on STIs and their control as an effective intervention to limit the spread of an HIV epidemic.7 However, STIs are a major cause of morbidity in their own right. Chlamydia is one of the most commonly reported STIs8 and most infections in women are asymptomatic. In women the infection has been associated with severe complications of the reproductive tract and adverse pregnancy outcomes, including pelvic inflammatory disease, ectopic pregnancy, preterm delivery, spontaneous abortion, low birth weight, infertility, and chronic pelvic pain.9–16 A link between chlamydia infection and cervical cancer has also been reported.17 Maternal infections may also affect the neonate and associations with pneumonia and opthalmia neonatorum have been documented.18,19 Because the majority of infections in women are asymptomatic, some countries, particularly in the developed world, have implemented screening programs in selected healthcare settings.20–22 In particular, routine chlamydial screening for sexually active women aged under 25 years is recommended by several organizations.23 The United Nations agencies have recently identified a number of priority areas to address the increase in STIs worldwide.24
To improve knowledge about risk behaviors and STI prevalence in Pacific Island Countries and Territories (PICTs), 6 PICTs participated in a regional project that included cross-sectional STI/HIV prevalence surveys of young pregnant women. The surveys targeted women 15 to 44 years of age. A stratified analysis was undertaken to compare women younger than 25 with those 25 years of age and older as women under 25 years are considered at higher risk for chlamydia and have been targeted for prevention efforts.23
Materials and Methods
Cross-sectional surveys of pregnant women aged 15 to 44 years attending their first antenatal clinic visit were conducted in 6 PICTs (Fiji, Kiribati, Samoa, Solomon Islands, Tonga, and Vanuatu) between October 2004 and July 2005. Ethical clearance for the surveys was obtained from the Ministries of Health and/or national ethics committees for participating countries, and the Human Research Ethics Committee University of New South Wales (UNSW).
Potential participants were informed about the survey via information leaflets and/or group information sessions before obtaining consent to participate in the survey. In each participating country 200 to 350 participants were consecutively recruited from the antenatal clinic located in the main hospital of each country and asked to provide a blood and urine specimen. Participants also completed a confidential standard questionnaire administered by trained interviewers capturing socio-demographic, obstetric, sexual history, and HIV knowledge. The questionnaire was adapted for local use, translated into the local languages, and piloted before the surveys commenced. Data and sample collection was on average 4 months per country. Survey design included confidential linked testing or linked anonymous testing depending on the country. Number of sites per country ranged from 1 to 4. Further information of the study design and methods has been described previously.25
Specimen Collection and Laboratory Procedures
Participants provided a 10 to 15 mL first-catch urine sample. Urine samples were stored at −20°C and shipped frozen to the Molecular Microbiology Laboratory, at the Royal Women’s Hospital, Melbourne, Australia, where they were tested for chlamydia and gonorrhoea. Amplification of Chlamydia trachomatis and Neisseria gonorrhoeae sequences were performed using ROCHE COBAS Amplicor (Roche Diagnostics, Branchburg, NJ) according to manufacturer’s recommendation. All positive N. gonorrhoeae specimens were confirmed by an alternate polymerase chain reaction assay using primers and probes directed at a 90 base pair region of opa gene as previously described.26
In addition to providing a urine sample, a 10-mL blood sample was collected from participants and the serum was separated by centrifugation at 1200 to 1500 rpm for 10 minutes and tested for HIV at local laboratories using Determine and Serodia HIV test kits (Fujirebio, Tokyo, Japan). Where tests were reactive, they were retested in the National Research Laboratory, Melbourne, Australia, using an ELISA test with confirmatory Western Blot. The selection of the HIV testing approach (linked or unlinked anonymous testing) was dependent upon local factors such as policy, laboratory capacity and infrastructure, and existing testing practices.
Sera were also tested for syphilis infection using Determine Syphilis TP test (Abbott Laboratories, Tokyo, Japan), and reactive sera were confirmed by TPPA and FTA tests or VDRL (VDRL-Cardiolipin Antigen, Dade Behring, Marburg, Germany) and a treponema-specific test, the Treponema pallidum particle agglutination test (Serodia-TPPA, Fujirebio). Any specimen found reactive in the VDRL test was titred in serial dilution. The fluorescent treponemal antibody absorption test (sorbent from Zeus Scientific, Raritan, NJ; IgG conjugate from Dako Corp, Glostrup, Denmark) was used as a confirmatory treponemal test for any specimens found reactive in the TPPA test. All tests were performed according to standard methods. The syphilis serology measures the prevalence of lifetime treponemal exposure and does not necessarily reflect on detection of an active infection.
During the survey, participants received counseling on STI and HIV prevention as clinically indicated and case-management was provided to all participants with a laboratory-confirmed diagnosis of an STI. Treatment protocols were compliant with World Health Organization STI Syndromic Case Management Guidelines.27 These guidelines had been modified by Ministries of Health to suit local conditions and be sustainable subsequent to completion of the survey. Pregnant women, if symptomatic, were treated at the time of their routine antenatal examination according to the standard syndromic approach or at the follow-up visit when test results were available.28 Patients were informed verbally of the potential side effect(s) of medications to be used. All medications selected are routinely used to treat these infections. Partners were followed-up with the consent of the survey participants and offered counseling and treatment according to existing country guidelines. Treatment was provided free to the named contacts of the survey cases.
Data Preparation and Analysis
Data were entered on a secure Microsoft Access file and computer. Preliminary data checking was undertaken locally before electronic transfer to the National Perinatal Statistics Unit at the UNSW as a password-protected file. Further checking of the data were then undertaken at the UNSW to examine inclusion criteria, distributions, range checks, consistency checks, and summary measures.
Data were analyzed using logistic regression analysis in SPSS (SPSS Incorporated, Chicago, IL).29 Women who failed to meet the inclusion criteria of age 15 to 44 years were excluded from analyses. A stratified analysis of pregnant women aged less than 25 years and greater than or equal to 25 years was conducted as women under 25 years are considered the target group for prevention and surveillance. For assessment of risk factors for infection with C. trachomatis, univariate logistic regression analyses were first conducted. Factors found to be significant on univariate testing were then used in a multivariate logistic regression analysis.
Of the 1745 pregnant women in the study, 67 were excluded from the final analysis because of nonstatement of age or not satisfying the 15 to 44 years age criteria, 5 women declined to participate, leaving a final survey population of 1673 women (range, 199–348 women per country). Blood and urine samples were obtained from 1618 women (96.7%).
Population and Sexual Behavior Characteristics
Table 1 shows selected demographic characteristics of the women studied. The mean age was 26.6 years (SD 5.9 years), with 42.6% aged less than 25 years and 9.8% were 15 to 19 years of age. Overall 18.9% of the women were resident in the capital city, 38.4% resident in urban, and 38.9% resident in rural villages. The majority of the women (84.6%) in the study were married or cohabiting and this ranged from 53.9% in the Solomon Islands to 97.5% in Kiribati. Most (63.5%) of the women had post primary including tertiary education. The majority of women were multiparous (71.2%) and had presented to the clinic in their second trimester. The occupations of the babies’ fathers differed across countries, where in Fiji, Samoa, Solomon Islands, and Vanuatu many fathers were company workers whereas in Kiribati and Vanuatu a high proportion of fathers were either seafarers/fishermen or unemployed.
Table 2 shows selected sexual behavior characteristics of pregnant women aged under 25 years. The median age at first sex for younger women was 18 years (range, 11–24 years) with 34.7% having had their sexual debut under the age of 18 years and 9.8% under the age of 15 years. Overall 42% reported a history of more than 1 sexual partner in their life, 19.2% had had 2 lifetime partners whereas 23.0% had 3 or more. Few women reported having had either commercial sex (1.5%) or concurrent partners (5.5%) in the previous 12 months. Use of condoms was low with 28.6% of the women had ever used a condom and of these 8.3% had used 1 either every time or almost every time and 77.1% had used a condom sometimes. Most (87.0%) women had heard of STIs and few (2.5%) reported having been diagnosed with an STI in the last 12 months.
Variation in sexual behavior amongst women aged under 25 years was apparent across country. In the Solomon Islands, 23.5% of women reported having had sex under the age of 15 years compared with 4.9% in Fiji and 2.7% in Tonga. Women in Kiribati and Tonga were more likely to have reported only 1 lifetime sexual partner and to have never used a condom (Table 2).
The most prevalent STI was chlamydia (26.1% amongst women under 25 and 11.9% amongst women aged 25 years and over). Amongst younger women, chlamydia prevalence varied by country and ranged from 7.3% in the Solomon Islands to 40.7% in Samoa (Table 3). A low prevalence of gonorrhoeal infection and no cases of HIV were detected. Overall, nearly a third (30.1%) of women less than 25 years had evidence of a current STI.
Risk factor analyses for chlamydia infection were undertaken. In women in all 6 countries, the prevalence was highest in the age group 15 to 19 years (31.4%) and decreased with increasing age (test for trend, P <0.05). Univariate analyses showed that amongst women aged less than 25 years, the prevalence of chlamydia was significantly higher among nulliparous women, women who were not married/cohabiting, were educated post primary school level, had reported 2 or more sexual partners in their lifetime and had reported sex for money or gifts in the last year (Table 4). Over a third (38.1%, 37 of 97) of women aged 15 to 19 who were not married/cohabitating had evidence of chlamydial infection.
Marital status, parity, number of lifetime sexual partners, and commercial sex remained significant in multivariate analysis (Table 5). Younger women who were not married or living with anyone were nearly twice as likely to be infected with chlamydia than married women (AOR, 1.78; 95% CI, 1.08–2.92). Although few women reported having had commercial sex (1.5%), these women were 6 times more likely to be infected with chlamydia than other women (AOR, 6.19; 95% CI, 1.39–27.54).
The majority (63%) of the women surveyed were considered low risk for STI infection, i.e., women who were married and had only 1 sexual partner in the previous 12 months. However, of these women, a significant proportion [13% (97 of 722)] were infected with chlamydia.
This is the first study of the prevalence of STIs amongst women throughout the Pacific. Nearly 1 in 5 pregnant women, traditionally a low-risk population of women who are largely representative of the general population, were found to be infected with chlamydia, indicating a high prevalence of risk-taking behaviors and low use of condoms. We did find statistically significant differences between the 6 countries in terms of chlamydia prevalence. This level of infection is alarming not just for the implications for HIV transmission, but because chlamydia infection is a significant cause of morbidity and can often lead to infertility or neonatal complications. These high rates of treatable infections indicate that STI control programs should be strengthened in the Pacific.
Our analysis has some limitations. Although acceptance rates to participate in the survey were high, the nonprobability sampling techniques, limited sample size, and sensitive nature of the behavioral data collected may have caused biases to the results. In addition, all data were obtained from selected sites in each participating country limiting the generalizability of results to the major urban centers of the country. However, for a number of countries the survey captured up to 20% of second and third trimester pregnancies for the country population for the year.
Our finding of high chlamydia positivity is consistent with previous studies amongst pregnant women in the Pacific and these results clearly indicate the need to reduce the incidence of chlamydial infection. Previous studies in Vanuatu and Samoa found rates of chlamydia of 22.4% and 29.7%, respectively, in pregnant women.1,2 Particularly worrying, was the high prevalence of chlamydia infection in younger women found in this study (ranging from 7.3% in the Solomon Islands to 40.7% in Samoa). The reasons for the comparatively low prevalence of chlamydia infection in the Solomon Islands is uncertain, although this may be attributed to those persons resident in the Solomon Islands having reduced travel to high prevalence areas.
Risk factor analyses also indicated that rates were high for single unmarried women, particularly teenagers who had a prevalence of 38%. The immediate and long-term morbidity to these women including potential loss of fertility is a public health emergency that requires intervention. Possible interventions include STI prevention and fertility preservation education programs targeted at youths attending secondary schools and tertiary centers; improvement in screening programs for young women attending family planning and antenatal clinics; and targeted social marketing campaigns promoting condom use and serial rather than concurrent sexual partners.
It is recognized in the literature that knowledge in itself is insufficient and that people also require access to family planning and sexual health services to take action to protect themselves from acquiring an STI. The need for such measures in the Pacific are pressing and the community recently published a Pacific Regional Strategy on HIV/AIDS that has been developed to assist countries in their fight against HIV/AIDS.4 The strategy is framed within 11 principles that acknowledge the traditional, cultural, and religious values of the Pacific communities.
Despite the surveys finding a HIV seroprevalence of zero, the STI picture indicates a population vulnerable to the introduction and rapid spread of HIV infection. The prevalence of STIs found in the Pacific are of a similar magnitude to those found in countries in Africa and Asia that are now experiencing HIV epidemics.30,31 One of the greatest problems with HIV is the long period between infection and development of symptoms. In the Pacific this is compounded with a health infrastructure that has limited private and confidential HIV testing capacity and little exposure or experience to diagnosing and treating HIV.
Chlamydia is a curable disease. The approach to its diagnosis and management is likely to differ from country to country depending on available resources. STI syndromic case management was introduced in the Pacific in 1994. However, as many chlamydial infections are asymptomatic this approach should be enhanced by using customized clinical and socio-demographic risk assessment tools based on local disease conditions. Screening “at risk” women for chlamydia is unlikely to discover the majority of infections as it is highly likely that many women are infected by their partners, based on the number of low risk women found to have infection. The successful management of STIs is also difficult for a number of other reasons, including the sensitive nature of sexual activity and the potential stigmatization of those with the diseases. Nonetheless, given the serious nature of these infections, it is vital these problems are addressed urgently. At the time of these surveys, there was no policy of prenatal screening for chlamydia. These findings suggest that for pregnant women, the utility of either screening or a form of presumptive treatment needs to be investigated as potential strategies to combat the endemic rates of chlamydia. It is critical that women have the opportunity to be diagnosed with chlamydial infection and treated antenatally to prevent known complications of pregnancy. Barriers to successful screening programs in the Pacific include lack of funding and the lack of inexpensive, reliable field diagnostic tests.
In conclusion, these findings show that chlamydia is endemic in young women in the Pacific, and that a generation of young women are at risk of infertility and chronic sequelae from undetected and untreated chlamydia infection. Regional leadership is needed to implement strategies to prevent the spread of HIV including STI prevention and management. However, regional leadership is also needed to halt the chlamydia epidemic which is a major public health problem in its own right that can be addressed with targeted funding, prevention and treatment strategies, and investment in adequate laboratory services.
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The Pacific Islands Second Generation Surveillance group consists of the following persons and organizations who contributed to the development, implementation and execution of the surveys. Sophaganine Ty Ali, Litiana Raikuna, Ministry of Health, Fiji; Mamao Robate, Tebuka Toatu, Ministry of Health, Kiribati; Saine Alo Vaai, Elisapeta Pasa-Anesone, Ministry of Health, Samoa; John Paulsen, Elliot Puiahi, Ministry of Health, Solomon Islands; Seini Kupu, Saia Penitani, Ministry of Health, Tonga; Marina Laklotal, Timothy Phatu, Ministry of Health, Vanuatu; Sepehr Tabrizi, Royal Women’s Hospital, Melbourne; Tim Sladden, Secretariat of the Pacific Community; Debbie black, Susan Cliffe, Jishan Dean, Lisa Maher, Elizabeth Sullivan, and Yueping Alex Wang, University of New South Wales; and Niklas Danielsson (Tonga), Asaua Faasino (Samoa), Jeffrey Hii (Solomon Islands), Ross Seya (Vanuatu), Seng Sopheap (South Pacific), and Nguyen Thi Thanh Thuy (Western Pacific Regional Office), World Health Organization.
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