Prevalence assessment of sexually transmitted infections among pregnant women visiting an antenatal care center of Nepal: Pilot of the World Health Organization’s standard protocol for conducting STI prevalence surveys among pregnant women

Rubee Dev; Shambhu P Adhikari; Anjana Dongol; Surendra K Madhup; Pooja Pradhan; Sunila Shakya; Shrinkhala Shrestha; Sneha Maskey; Melanie M Taylor

doi:10.1371/journal.pone.0250361

. 2021 Apr 23;16(4):e0250361. doi: 10.1371/journal.pone.0250361

Prevalence assessment of sexually transmitted infections among pregnant women visiting an antenatal care center of Nepal: Pilot of the World Health Organization’s standard protocol for conducting STI prevalence surveys among pregnant women

Rubee Dev ^1,^*, Shambhu P Adhikari ², Anjana Dongol ³, Surendra K Madhup ⁴, Pooja Pradhan ⁵, Sunila Shakya ⁶, Shrinkhala Shrestha ⁷, Sneha Maskey ⁸, Melanie M Taylor ^9,¹⁰

Editor: R Matthew Chico¹¹

¹Faculty of Nursing, University of Alberta, Edmonton, Alberta, Canada

²Department of Physiotherapy, Kathmandu University School of Medical Sciences, Dhulikhel, Kavre, Nepal

³Department of Obstetrics and Gynecology, Kathmandu University School of Medical Sciences, Dhulikhel, Kavre, Nepal

⁴Department of Microbiology, Kathmandu University School of Medical Sciences, Dhulikhel, Kavre, Nepal

⁵World Health Organization- Country Office, Lalitpur, Nepal

⁶Department of Obstetrics and Gynecology, Kathmandu University School of Medical Sciences, Dhulikhel, Kavre, Nepal

⁷Department of Community Programs, Kathmandu University School of Medical Sciences, Dhulikhel, Kavre, Nepal

⁸Department of Community Programs, Kathmandu University School of Medical Sciences, Dhulikhel, Kavre, Nepal

⁹Department of Global Programmes of HIV, Hepatitis, STI, World Health Organization, Geneva, Switzerland

¹⁰Centers for Disease Control and Prevention, Division of STD Prevention, Atlanta, Georgia, United States of America

¹¹London School of Hygiene and Tropical Medicine, UNITED KINGDOM

Competing Interests: The authors have declared that no competing interests exist.

^✉

* E-mail: rubee@ualberta.ca

Roles

Rubee Dev: Conceptualization, Formal analysis, Funding acquisition, Investigation, Methodology, Writing – original draft, Writing – review & editing

Shambhu P Adhikari: Data curation, Project administration, Supervision, Writing – review & editing

Anjana Dongol: Investigation, Project administration, Resources, Supervision, Validation, Writing – review & editing

Surendra K Madhup: Investigation, Project administration, Resources, Validation, Visualization

Pooja Pradhan: Methodology, Project administration, Resources, Supervision

Sunila Shakya: Conceptualization, Data curation, Investigation, Methodology, Project administration, Supervision, Writing – review & editing

Shrinkhala Shrestha: Investigation, Project administration, Resources, Validation, Writing – review & editing

Sneha Maskey: Data curation, Investigation, Project administration, Software

Melanie M Taylor: Conceptualization, Funding acquisition, Methodology, Supervision, Writing – original draft, Writing – review & editing

R Matthew Chico: Editor

PMCID: PMC8064610 PMID: 33891652

Abstract

Introduction

Sexually transmitted infections (STIs) are common during pregnancy and can result in adverse delivery and birth outcomes. The purpose of this study was to estimate the prevalence of STIs; Chlamydia trachomatis (CT), Neisseria gonorrhoeae (NG), Treponema pallidum (syphilis), Trichomonas vaginalis (trichomoniasis), and Human Immunodeficiency Virus (HIV) among pregnant women visiting an antenatal care center in Nepal.

Materials and methods

We adapted and piloted the WHO standard protocol for conducting a prevalence survey of STIs among pregnant women visiting antenatal care center of Dhulikhel Hospital, Nepal. Patient recruitment, data collection, and specimen testing took place between November 2019-March 2020. First catch urine sample was collected from each eligible woman. GeneXpert platform was used for CT and NG testing. Wet-mount microscopy of urine sample was used for detection of trichomoniasis. Serological test for HIV was done by rapid and enzyme-linked immunosorbent assay tests. Serological test for syphilis was done using “nonspecific non-treponemal” and “specific treponemal” antibody tests. Tests for CT, NG and trichomoniasis were done as part of the prevalence study while tests for syphilis and HIV were done as part of the routine antenatal testing.

Results

672 women were approached to participate in the study, out of which 591 (87.9%) met the eligibility criteria and consented to participate. The overall prevalence of any STIs was 8.6% (51/591, 95% CI: 6.3–10.8); 1.5% (95% CI: 0.5–2.5) for CT and 7.1% (95% CI: 5.0–9.2) for trichomoniasis infection. None of the samples tested positive for NG, HIV or syphilis. Prevalence of any STI was not significantly different among women, age ≤ 24 years (10%, 25/229) compared to women age ≥25 years (7.1%, 26/362) (p = 0.08).

Conclusions

The prevalence of trichomoniasis among pregnant women in this sub-urban population of Nepal was high compared to few cases of CT and no cases of NG, syphilis, and HIV. The WHO standard protocol provided a valuable framework for conducting STI surveillance that can be adapted for other countries and populations.

Introduction

Every day around the world, more than one million people acquire a sexually transmitted infection (STI) [1]. Some viral STIs, like human papillomavirus (HPV) and human immunodeficiency virus (HIV), are still incurable and can be deadly, but some bacterial and protozoal STIs–like Chlamydia trachomatis (CT), Neisseria gonorrhoeae (NG), Treponema pallidum (syphilis) and Trichomonas vaginalis (trichomoniasis)–are curable and detectable with widely available but underutilized diagnostic platforms [2].

Most CT and NG infections in women are asymptomatic, but if left untreated can lead to serious complications, including pelvic inflammatory disease (PID), infertility, chronic pelvic pain and infant infection [3]. Women with trichomoniasis may be asymptomatic and may experience negative pregnancy outcomes such as preterm birth and an increased risk of PID among HIV-infected women [4]. Trichomoniasis has also been independently associated with increased risk for HIV acquisition and transmission [5]. Maternal HIV infection is associated with low-birth weight and increased susceptibility to infections in HIV-exposed uninfected infants [6]. Vertical transmission of syphilis (congenital syphilis) is the second leading global cause of stillbirth (malaria being the first) [7]. Screening for early detection followed by appropriate management of these infections could reduce the sequelae of complications and transmission.

To address this global and critical issue and to enable countries to reach targets set by the Sustainable Development Goals, the World Health Organization (WHO) developed the Global Health Sector Strategy on Sexually Transmitted Infections 2016–2021 [8]. The strategy positions the health sector response to STI epidemics as critical to the achievement of universal health coverage–one of the key health targets of the SDGs identified in the 2030 agenda for sustainable development. A key pillar of this strategy is STI surveillance. WHO recommends routine STI prevalence assessments among general populations of women and men to assess STI burden and guide programming [9]. To guide countries in implementing routine STI prevalence surveys, WHO released a standard protocol to assess prevalence of STIs among pregnant women in 2018 [10]. Nepal was chosen as the first pilot site for implementation of this protocol.

WHO global estimates of STIs among general populations are based on STI prevalence assessments in the peer-reviewed literature. Unfortunately, few of such STI prevalence surveys are published each year and studies are even fewer from the South East Asia region. The limited availability of STI prevalence surveys results in limited representativeness of global estimates. To address this surveillance priority, WHO developed a standard protocol for STI prevalence surveys [10] to encourage countries, regions, and academic institutions to perform STI prevalence surveys to improve STI surveillance and program response at national, regional and global levels. Herein we describe the pilot of the WHO protocol and comment on the benefits of generating STI prevalence data for program response.

Information on the burden of STIs among general populations and among pregnant women in Nepal is limited. Available data are in the form of STI case reports which are known to drastically under-estimate STI burden due to limited access to STI diagnostic services. Various studies have been conducted to examine STI prevalence, mainly HIV and syphilis; however, most of them are conducted among high-risk populations such as sex workers (1.7% HIV and 3.9% syphilis), truck drivers (1.5% HIV and 5.3% syphilis), and male labor migrant workers (8% HIV and 22% syphilis) [11–13]. STI prevalence among such high-risk populations is reported to be high [9]. HIV is reported to be concentrated among key populations, with HIV prevalence at 5% among male sex-workers, 8.5% among transgender people, and 8.8% among males who inject drugs [14]. Information about assessment and trends in STI prevalence—whether, and by how much, the prevalence is increasing or decreasing, and which populations are affected—can help Nepal monitor its STI trends and provide information on the effectiveness of prevention and control measures.

This study aims to fill an existing gap in the collection of STI strategic information among pregnant women in Nepal. Studies to determine the prevalence of STIs can support program actions by providing information on population burden and supporting prevalence and incidence estimates. Hence, the main purpose of this study was to epidemiologically determine the prevalence of CT, NG, syphilis, trichomoniasis and HIV among pregnant women attending an antenatal care (ANC) center in Nepal by adapting the WHO standard protocol for STI prevalence surveillance.

Materials and methods

Study design

This was a prevalence survey of STIs among pregnant women. The survey was conducted between November 2019 –March 2020 at the antenatal care center of Kathmandu University Hospital (KUH)/Dhulikhel Hospital (DH), Kavre, Nepal. The Strengthening the Reporting of Observational Studies in Epidemiology (STROBE) checklist was utilized to ensure quality reporting during this cross-sectional study [15] (see S1 Checklist).

Study site and population

Pregnant women attending antenatal care clinic at KUH/DH were enrolled in the study. DH is a not-for-profit community and university hospital that covers the rural, urban, and sub-urban population from Kavrepalanchowk, Sindhupalchowk, Dolakha, Sindhuli, Ramechhap, Bhaktapur and other surrounding districts. DH is also a tertiary care hospital where on an average, 60–70 pregnant women visit the antenatal clinic every day.

Sample size and sampling technique

The sample size was determined based on the estimated prevalence of CT in Dhulikhel and prevalence of trichomoniasis in Kathmandu and surrounding geographical areas. CT infection was prevalent in 0.8% (95% CI: 0.5–1.5) of the women in a STI prevalence study conducted among married women in the rural Kavre district of Nepal [16]. Trichomoniasis was prevalent in 1.3% of the pregnant women attending Paropakar Maternity and Women’s Hospital in urban Kathmandu [17]. As recommended for prevalence studies, we used n = Z²P(1-P)/d² formula to calculate the sample size; where n is the sample size, Z is the statistic corresponding to 95% level of confidence, P is expected prevalence (obtained from similar studies), and d is precision (estimated not to exceed 1%) [18]. For a given level of observed CT and trichomoniasis prevalence, the minimum sample size needed for a survey was estimated to be 305 and 493 pregnant women. Using the given estimated sample size, we sampled 591 pregnant women for this prevalence survey.

We used convenience sampling technique to sample pregnant women. All women attending antenatal clinic at DH were approached by a trained research assistant (RA) who screened them for their eligibility and sequentially enrolled all eligible women who were interested to participate in the study.

Eligibility criteria for the enrolment site and pregnant woman

ANC center at DH was purposively selected as: (i) it was the first entry point for all the pregnant women visiting for antenatal check-up; (ii) the site provided services to a sufficiently large number of clients; (iii) there was a presence of a reliable laboratory for processing of specimens and transport to the laboratory; (iv) there was an availability of treatment for infected pregnant women; (v) the site was accessible to surveillance staff; and (vi) their on-site staff members were willing to cooperate and were trained to conduct the survey.

Pregnant women were eligible for inclusion if they: (i) attended the clinic irrespective of their gestational age; (ii) were aged 18–49 years or were emancipated minors by marriage; and (iii) were candidates for routine laboratory examinations. Women were excluded if they had previously visited the clinic during the survey period to avoid duplication, had received treatment for any of the STIs within two weeks, and if they did not give informed consent to participate in the study.

Study procedures

Enrollment, consenting, counseling, and follow-up of participants

The study team organized a one-day training on nature of the study, study protocol and study procedures for the RA and co-investigators (gynecologists, laboratory personnel, site coordinator) before initiation of the study. All team members received training on interviewing clients for determining eligibility, obtaining informed consent, sample collection, sample transportation, research confidentiality and participants’ rights, and data collection and storage procedures.

Women attending ANC clinic were approached by an RA to screen for the eligibility and enroll in the study. Participating women were notified about the occurrence of the study and the opportunity to undergo tests for CT, NG and trichomoniasis as part of the prevalence study in addition to the routine antenatal testing done for syphilis and HIV. Women were informed that the results of syphilis and HIV tests will be extracted from the electronic health record (EHR) at the laboratory. A written informed consent was obtained from each woman. Minors emancipated by marriage were allowed to consent independently as adults.

Women were counseled on participation and testing for the STIs. Women received counseling and assurance that the results of testing would be confidential and would not be shared outside of the prevalence survey or clinic setting. Counseling was specifically on: (i) the benefits of early detection and provision of treatment to prevent manifestations of untreated infection, (ii) potential risks associated with untreated STIs during pregnancy on both the mother and newborns; (iii) potential emotional stress of being diagnosed with a STI; (iv) the importance of treatment of sexual partners to avoid re-infection during pregnancy; and (v) the risk of disclosure to sexual partners of exposure to an STI. Participants with positive test results for any STIs were followed-up for the treatment. Three attempts were made to contact each patient. The follow-up required that the patients are confidentially notified of their positive test results and asked to return to the clinic for the treatment and post-test counseling. Women with negative test results were not followed-up and were asked to come to the clinic on their regular ANC visit.

Laboratory tests

Laboratory testing for CT, NG, and trichomoniasis was undertaken through collection of first catch urine sample, while serological testing for syphilis and HIV was performed on blood sample as per routine care at DH [4]. CT and NG tests were performed using GeneXpert kits donated to the hospital by Cepheid, USA (donation company); hence, the tests were performed free of cost for the study participants. In Nepal, the GeneXpert (Cepheid, USA) testing platform is available for tuberculosis testing but not for routine testing for CT/NG. As part of a collaborative and integrated program effort between the WHO country office in Nepal, the National Tuberculosis Center, and DH, the GeneXpert platform available at DH was used for all CT/NG tests in the current prevalence survey.

The same urine sample collected for CT and NG tests was also used for the test of trichomoniasis using wet mount preparation method of microscopic examination of motile protozoa. Serological testing for syphilis was done using non-treponemal antibody screening test i.e., Rapid Plasma Reagin (RPR- RFCL Diagnova Trepostat, Ranbaxy, Gurgaon, India), and specific treponemal antibody tests (Treponema pallidum haemagglutination- Fujirebio, Europe, N.V., Gent, Belgium) to confirm positive screening tests. Serological HIV test was done by AccuDiag^TM HIV enzyme-linked immunosorbent assay (HIV- ELISA, Diagnostic Automation/Cotez Diagnostics, Inc., CA, USA) method that detects HIV antibodies and antigens in the blood. In case of a positive result, the ELISA test was followed by a Western Blot test to confirm the diagnosis. These tests were performed following the national algorithm of Nepal [4]. Specimens for serological testing of syphilis and HIV were collected as part of the routine ANC package (including hemoglobin, glucose, blood grouping, HBsAg, HIV and syphilis testing) at DH during the first ANC visit according to the hospital ANC protocol.

Samples obtained from pregnant women were collected and transported in an icebox to the microbiology laboratory of DH where the tests for CT, NG and trichomoniasis were performed. Most of the samples were analyzed on the same day of collection, and samples left for analysis were stored in a refrigerator at -20°C until further analyses. The results of syphilis and HIV was extracted from the EHR. Test results were dispatched within a week. Women with positive test results were contacted by the RA using personal phone numbers and asked to return for treatment.

Treatment

Women with positive test results who came back to the clinic for follow-up were referred to the gynecologists, who explained the STI test result, discussed their concerns and the need for treatment, prescribed them medicine following national treatment guidelines [19], and discussed the need for partner testing. Women with positive test results for any of the tested STIs received treatment free of cost according to the study protocol.

Statistical analysis

Descriptive analyses were used to describe the socio-demographic and reproductive characteristics of pregnant women. The results of continuous variables were expressed as the mean (standard deviation [SD]), and the results of categorical variables were expressed as counts (percentages). The prevalence of overall and individual STIs were calculated and summarized as percent with 95% confidence intervals (CIs). To measure the overall prevalence of at least one of the five STIs, we defined a composite STI variable as “any STI”, as a positive test for CT or NG or trichomoniasis or syphilis or HIV infection. Bivariate analyses were conducted to examine the association between the participant characteristics and CT and trichomoniasis infections, using Pearson’s chi-square test (χ² test) and the Fisher’s Exact test where expected cell counts for exposure and outcome were less than five [20]. A p-value less than 0.05 was considered statistically significant. All analyses were done using Stata version 15 (Stata Corporation, College Station, TX, USA).

Ethical approval

This study was approved by the World Health Organization Research Ethics Review Committee (WHO ERC.0003182), Nepal Health Research Council (NHRC 78/2019), and Kathmandu University School of Medical Sciences-Ethical Review Committee (KUSMS-IRC 37/19), Nepal. Women enrolled in the study provided written informed consent to participate. All methods were carried out in accordance with relevant guidelines and regulations.

Results

Socio-demographic characteristics

In total, 591 (87.9%) of 672 approached women met the eligibility criteria and were recruited in the study. The mean age of the women attending the clinic was 26 years (SD = 4.2). A majority (46.4%) of the women were primigravida. The mean age at marriage was 22 years (SD = 3.6) and 62.4% of the women reported to be either a housewife or unemployed. Majority (84.8%) of the women reported being tested for STIs in the past of which 84.9% reported having negative result for any of the STIs, while 15.1% did not know their test result (Table 1).

Table 1. Characteristics of pregnant women visiting antenatal care clinic in Dhulikhel Hospital, Nepal (N = 591).

	n (%) or mean (SD)
Sociodemographic characteristics
Age (years)	26 (4.2)
Age category (years)
< 20	29 (4.9%)
20–24	200 (33.8%)
25–29	235 (39.8%)
30–34	107 (18.1%)
≥ 35	20 (3.4%)
Age of marriage	22 (3.6)
Place of residence
Urban	332 (56.2%)
Rural	259 (43.8%)
Education level of women
No education	21 (3.6%)
Primary	234 (39.6%)
Some college or university	202 (34.2%)
Completed university	134 (22.7%)
Education level of husband
No education	17 (3.3%)
Primary	207 (40.7%)
Some college or university	170 (33.4%)
Completed university	115 (22.6%)
Occupation of women
Housewife	369 (62.4%)
Self-employed	100 (16.9%)
Salaried	122 (20.6%)
Occupation of husband
Unemployed	20 (3.4%)
Self-employed	268 (45.4%)
Salaried	303 (51.3%)
Reproductive characteristics
Gestational week	25.6 (9.1)
Gravidity
1	274 (46.4%)
2	203 (34.4%)
≥ 3	114 (19.3%)
Number of live births	1 (1)
Number of abortion/miscarriages
No abortion/miscarriages	471 (79.7%)
1	99 (16.6%)
>1	21 (3.6%)
STI test history
Ever tested for STIs in the past
Yes	501 (84.8%)
No	90 (15.2%)
Past test result for STIs
Unknown	76 (15.1%)
Negative	425 (84.9%)

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N (number of complete observations), SD (standard deviation), STI (sexually transmitted infection)

Prevalence of STIs

The overall prevalence of any STIs among women attending antenatal clinic at DH was 8.6% (51/591, 95% CI: 6.3–10.8); with 1.5% prevalence of CT (9/591, 95% CI: 0.5–2.5), 7.1% (42/591, 95% CI: 5.0–9.2) trichomoniasis, and zero prevalence of NG, syphilis, and HIV respectively (Table 2). Trichomoniasis was the most commonly occurring infection. Only one woman (0.2%) had both CT and trichomoniasis infections. Prevalence of any STI was not significantly different among women, age ≤ 24 years (10%, 25/229) compared to women age ≥25 years (7.1%, 26/362) (p = 0.08). Prevalence of any STI was common among women who reported being a housewife (32 /369, 8.7%) and among the primigravida (24/274, 8.8%). However, none of the demographic variables collected were statistically associated with having CT or trichomoniasis (Table 3).

Table 2. Prevalence of STIs among pregnant women visiting antenatal care clinic in Dhulikhel Hospital, Nepal (N = 591).

	Number positive	% (95% CI)
Types of STI
Chlamydia	9	1.5 (0.5–2.5)
Gonorrhea	-	-
Syphilis	-	-
Trichomoniasis	42	7.1 (5.0–9.2)
HIV	-	-
Any STI	51	8.6 (6.3–10.8)

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CI (Confidence interval), HIV (Human Immunodeficiency Virus), STI (sexually transmitted infection)

Table 3. Characteristics of study participants by types of STI (N = 591).

	Chlamydia (n = 9)		Trichomoniasis (n = 42)		Any STI (n = 51)
	% (95% CI)	p-value	% (95% CI)	p-value	% (95% CI)	p-value
Sociodemographic characteristics
Age category (years) <20 20–24 25–29 30–34 ≥35	- 55.6 (21.1–90.1) 22.2 (-6.6–51.1) 11.1 (-10.7–32.9) 11.1 (-10.7–32.9)	0.312	4.8 (-1.8–11.3) 42.9 (27.7–58.0) 38.1 (23.2–52.9) 11.9 (1.9–21.8) 2.4 (-2.3–7.1)	0.729	4.0 (-1.5–9.5) 46.0 (32.0–59.9) 36.0 (22.5–49.5) 10.0 (15.8–18.4) 4.0 (-1.5–9.5)	0.296
Age category (dichotomous) ≤24 years ≥25 years	55.6 (21.1–90.1) 44.4 (9.9–78.9)	0.297	47.6 (32.3–62.9) 52.4 (37.1–67.7)	0.221	50.0 (35.9–64.0) 50.0 (35.9–64.0)	0.088
Place of residence Urban Rural	33.3 (0.6–66.1) 66.6 (33.9–99.4)	0.19	69.0 (54.9–83.2) 30.9 (40.6–48.9)	0.081	62.0 (48.4–75.6) 38.0 (24.4–51.6)	0.386
Education level of women No education Primary Some college/university Completed university	22.2 (-6.6–51.1) 44.4 (9.9–78.9) 11.1 (-10.7–32.9) 22.2 (-6.6–51.1)	0.051	4.8 (-1.8–11.3) 33.3 (18.9–47.8) 38.1 (23.2–52.9) 23.8 (10.7–36.9)	0.749	8.0 (0.4–15.6) 36.0 (22.5–49.5) 34.0 (20.7–47.3) 22.0 (10.4–33.6)	0.351
Occupation of women Housewife Self-employed Salaried	66.7 (33.9–99.4) 22.2 (-6.6–51.1) 11.1 (-10.7–32.9)	0.798	61.9 (47.0–76.8) 26.2 (12.7–39.7) 11.9 (1.9–21.8)	0.137	64.0 (50.5–77.5) 24.0 (12.0–35.9) 12.0 (2.9–21.1)	0.164
Reproductive characteristic
Gravidity 1 2 ≥3	22.2 (-6.6–51.1) 44.4 (9.9–78.9) 33.3 (6.0–66.1)	0.308	52.4 (37.1–67.7) 35.7 (21.0–50.4) 11.9 (1.9–21.8)	0.437	48.0 (33.9–62.0) 36.0 (22.5–49.5) 16.0 (5.7–26.3)	0.826

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N (number of complete observations), CI (confidence interval), CT (Chlamydia trachomatis), STI (sexually transmitted infection)

p-values were obtained using Chi-square or Fishers exact tests.

Treatment of participants

A total of 42 women (82.4%) who tested positive for any of the STIs were called for follow-up. Of those, 19 women (2 CT and 17 trichomoniasis positive cases) came and received treatment, while 23 women refused to come for the treatment. Among women who refused, one woman had already delivered a baby, and the remaining either refused to come as they lived far from the hospital and did not want to return to clinic only to receive treatment or said they will come but did not come. Despite of multiple attempts to call, we could not follow-up with 9 women as their phones were unreachable.

Discussion

This first pilot application of the WHO standard protocol for assessing the prevalence of CT and NG among pregnant women established a standard method for conducting STI prevalence surveys in Nepal. We identified a lower than expected prevalence of STIs among this group of pregnant women attending a sub-urban ANC center in Kavre, Nepal. The prevalence of trichomoniasis was comparatively higher among the women followed by CT.

Trichomonas vaginalis was identified in 7.1% of women using a non-sensitive method of microscopic detection and CT was prevalent among 1.5% of women using a GeneXpert platform. These prevalence values are higher compared to 5.4% prevalence of trichomoniasis and 0.8% prevalence of CT ascertained in a previous study among married women in rural Nepal [16], likely due to the fact that the study was conducted among non-pregnant women that may not have been sexually active. Other studies in high and low-middle income countries have found varying prevalence of TV in pregnant women [21–24]. Based on the low sensitivity of the TV wet mount, we expect the prevalence of trichomoniasis in our study population to be higher than what we report.

Though the prevalence of CT was low in this study, it is alarming as a recent studies have reported a significant association of CT with preterm birth and term preeclampsia mainly among the women aged <25 years [25, 26]. Several studies have also suggested the association between trichomoniasis and preterm delivery as well as low-birth weight infants [27, 28]. These findings demonstrate the importance of considering integration of routine screening and treatment of STIs during antenatal care in Nepal.

Despite the low prevalence of STIs among this population of pregnant women, these data provide valuable STI prevalence points for CT and trichomoniasis that can be used to generate estimates of prevalence and incidence of these infections using STI modeling tools [29]. The participation of the WHO country office in Nepal as well as the research collaborators at DH, formed a system and partnership that could be replicated for repeat STI prevalence surveys among pregnant women and other populations such as men. Further, the collaboration with the national center for tuberculosis program for the shared use of the GeneXpert platform for CT/NG along with tuberculosis demonstrated the availability and the importance of expanding the STI diagnostic capabilities of this and other multiplex testing systems.

Regardless of the stigma associated with STI testing, nearly all pregnant women who were approached participated in screening. However, the findings of this prevalence survey should be interpreted with the following limitations. First, this is not a national representative sample as data were only collected from one clinical setting and thus these results cannot be generalized for the entire country. Second, the zero prevalence of NG, HIV and syphilis suggests that increasing our sample size could have estimated more accurate prevalence of these infections by providing more accurate information on prevalence, narrowing margin of error, and identifying correlates of infection; however, resources and contextual factors for this pilot application limited our ability to increase the sample size. Future prevalence studies could determine the correlates of STIs using multivariate analysis and a larger sample size. In April 2020, the study was suspended due to the outbreak of SARs-CoV-2 in the country. On June 25, 2020, due to the worsening COVID-19 epidemic, the ongoing closure of the outpatient ANC recruitment site, the reorganization of the laboratory services to support the COVID-19 response, and the obtainment of the required sample size needed, the study was stopped. It must be pointed out that the aim of this study was to enhance STI surveillance and not to provide clinical care. However, contacting women within a week (from sample collection to results dispatch) to refer them for treatment was valuable to our understanding of the challenges of STI treatment when patients must return for results. Further, refusal of more than half of the women to re-visit clinic just for the treatment of STI was alarming. Strategies to improve testing and point of care treatment on the same visit should be prioritized.

The global burden of curable STIs is high and has shown no decline based on the most recent WHO estimates [1]. National-level prioritization of STI control has fallen behind that of other infections such as HIV and hepatitis [30]. Better STI surveillance data can be used to guide clinical systems in enhancing STI testing services for pregnant women as well as other populations. Moving forward, further studies will be needed to explore the most cost-effective STI screening and treatment strategies among pregnant women at national and local levels.

Conclusions

In this prevalence survey, we found an overall low prevalence of STIs among pregnant women attending an antenatal clinic in Kavre, Nepal. Trichomoniasis was the most commonly detected STI followed by CT. Adoption of WHO’s STI surveillance protocol at the country level will help to examine the prevalence and trend of STIs among pregnant women and other populations and prioritize infection control strategies accordingly.

Supporting information

S1 Checklist. STROBE statement—Checklist of items that should be included in reports of cross-sectional studies.

(DOC)

Click here for additional data file.^{(90KB, doc)}

Acknowledgments

The authors would like to express their gratitude to the Department of Obstetrics and Gynecology and the Department of Microbiology at the Dhulikhel Hospital, and all the participants of the study.

Disclaimer: The views expressed in this manuscript are those of the authors and do not necessarily represent the official position of the World Health Organization, the United States of America Centers for Disease Control and Prevention, or other affiliated organizations.

Data Availability

All data relevant to the study are included within the article. Raw data cannot be shared publicly because of the confidentiality issues as it includes the personal identifying information of the women. Deidentified data could be available from the Kathmandu University Institutional Data Access / Ethics Committee (contact via email at irc@kusms.edu.np) for researchers who meet the criteria for access to confidential data.

Funding Statement

This study was made possible by support from the UNDP/UNFPA/UNICEF/WHO/World Bank Special Programme of Research, Development and Research Training in Human Reproduction (HRP), Department of Sexual and Reproductive Health and Research, World Health Organization, Geneva, Switzerland.

References

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PLoS One. doi: 10.1371/journal.pone.0250361.r001

Decision Letter 0

R Matthew Chico

2 Mar 2021

PONE-D-21-02130

Prevalence assessment of sexually transmitted infections among pregnant women visiting an antenatal care center of Nepal: Pilot of the World Health Organization’s standard protocol for conducting STI prevalence surveys among pregnant women

PLOS ONE

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Reviewer #1: The Dev et al. manuscript describes a cross-sectional study of STI prevalence in Nepal. The authors report a relatively high prevalence of trichomoniasis (TV) compared to other STI. The work presented in this manuscript is well described and provides a valuable contribution to global health literature.

I am pleased to see the sound logically structure and concise writing style found in this manuscript, along with the solid methodology. I have a few questions and a few minor comments.

Questions:

1. Would the authors please clarify why the sampling is purposive as opposed to convenience? My understanding is that the authors did not target a specific subset of the ANC population in order to develop a specific sample population profile or have a specific goal needing a specific population, but instead sampled a general ANC population, so this seems to be convenience sampling?

2. As the authors acknowledged, the sensitivity of wet mount for TV (averaging around 50%) and PCR for CT (98.7%) is different. Although PCR for CT and TV is similar, sensitivity of wet mount for TV can be as low as 38%. The STI prevalence data in this manuscript is valuable, but I think the comparison might be problematic given the difference in sensitivity of the diagnostic tests. Perhaps decreasing the language that suggests a comparison might be more accurate?

3. The number of women in the sample that report STI testing history is reported as 84.7%. This seems high? And makes me wonder if there is something unique about this population?

Minor comments:

Line 92-93: Is there a specific reason that Nepal was chosen as the first pilot site for implementation of the new WHO protocol?

Line 201: This seems to be a repeat of line 199?

Line 211: I don’t think Wet should be capitalized?

Line 212 and Line 214: I don’t think the nonspecific/specific and the quotation marks around non-treponemal and treponemal are needed?

Line 221: HBsAg not HBsAG

Line 300 to 303: I am unsure about this argument as the prevalence of STIs is generally higher in Brazil than Nepal?

Reviewer #2: This is an important manuscript about the prevalence of STIs including HIV in pregnant women in Nepal. There are some areas of the manuscript that could be improved upon prior to publication listed below.

1. Abstract: introduction should include harmful effects on pregnancy outcomes and infants. Can you add that the syphilis and HIV testing were part of standard of care, but other STIs were part of the study (otherwise it appears that 12% of the sample were not tested for HIV/RPR).

2. Introduction: Line 75 "may be asymptomatic OR may experience" - should this be and as these are not mutually exclusive categories (symptoms and outcomes).

- It would be helpful to add in the prevalence reported in other studies in the introduction even in high risk populations or the study of married women in Nepal. Also please cite the HIV prevalence from UNAIDS for Nepal to give context to the study.

3. Methods: were partners informed about the partner's STI diagnosis? Were they referred for treatment or testing? how long did it take to test and contact participants?

For statistical analysis, it may be better to conduct a mutlivariate analysis that controls for other covariates like age, gestational age, education, etc if you want to test hypotheses of associations between STI diagnosis and age, education, etc. using a multivariate logistic regression model. Otherwise, I would avoid making hypotheses and presenting statistics from statistical tests as presented.

4. Results:

Table 1. Did you record what kind of STI tests women had had in past as the % seems high. Was that for HIV or syphilis in prior pregnancies? And why do the # differ in ever testing and unknown STI test results (90 vs 89 and 501 vs 502)?

Please include abortion/miscarriage in the line "no abortion" as they were combined in the question.

The analysis in table 3 presents simple chi-square stats and the p-value is almost significant for education and CT and TV and place of residence, and age and any STI (can update this with the %s in line 269-271). If the authors could conduct a multivariate analysis testing some of these hypotheses, the results would be more interesting/valid.

5. Discussion: please include what (if anything) was done for male partners? How long did it take to give feedback on the results? Why did only 1/2 of women return for treatment? What can be done to improve this (point of care testing, earlier feedback, partner engagement?).

Please add this outcome about limited treatment uptake to the abstract and conclusions/recommendations if there is space.

**********

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Reviewer #1: No

Reviewer #2: No

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PLoS One. 2021 Apr 23;16(4):e0250361. doi: 10.1371/journal.pone.0250361.r002

Author response to Decision Letter 0

21 Mar 2021

Manuscript reference number: PONE-D-21-02130

Title: Prevalence assessment of sexually transmitted infections among pregnant women visiting an antenatal care center of Nepal: Pilot of the World Health Organization’s standard protocol for conducting STI prevalence surveys among pregnant women

Dear Editor/Reviewers,

Thank you for your careful review of our manuscript entitled “Prevalence assessment of sexually transmitted infections among pregnant women visiting an antenatal care center of Nepal: Pilot of the World Health Organization’s standard protocol for conducting STI prevalence surveys among pregnant women” (PONE-D-21-02130).

We greatly appreciate your comments and have revised the manuscript and have detailed responses to each of the points below.

Journal Requirements

1. Please ensure that your manuscript meets PLOS ONE's style requirements, including those for file naming.

We carefully checked the PLOS ONE’s style requirements and have revised our manuscript accordingly.

In your revised cover letter, please address the following prompts:

We will update your Data Availability statement on your behalf to reflect the information you provide.

Thank you for this suggestion. In our revised cover letter, we have addressed the suggested points related to the data availability.

3. Please upload a copy of Supplementary File which you refer to in your text on page 7.

The Supplementary File that we are referring to is STROBE Research Checklist. Revised version of the checklist now has been uploaded.

Thank you for this suggestion. We have now omitted the ethics statement from the declaration section and added it under the Methods section on page 13 of the revised manuscript.

Reviewer 1

Questions

We would like to thank the reviewer for pointing this out. We agree with the reviewer’s comment and have now replaced the sampling technique from “purposive” to “convenience” on page 8, line 174 of the revised manuscript.

Thank you for the comment. We agree with this description regarding the large difference in sensitivity of the tests.

In response, we have removed this statement in the discussion: A study conducted in Brazil reported similar prevalence of trichomoniasis (7.7%) among young pregnant women using a highly sensitive nucleic acid amplification test [21], supporting the sensitivity of detection in our study.

We have replaced the statement on page 17 with: Other studies in high and low-middle income countries have found varying prevalence of TV in pregnant women (21-24). Based on the low sensitivity of the TV wet mount, we expect the prevalence of trichomoniasis in our study population to be higher than what we report.

3. The number of women in the sample that report STI testing history is reported as 84.7%. This seems high? And makes me wonder if there is something unique about this population?

Thank you for this comment. As part of the antenatal care in Nepal, every pregnant woman has to undergo general screening for STIs including HIV and syphilis during their first visit to the antenatal care clinic. However, the screening does not include a test for CT, NG, and trichomoniasis. More than half of the women (53.7%) in the sample were either 2nd or 3rd gravida, which indicates they might have undergone screening tests during their initial pregnancies. Even for the prima gravida, we recruited women, irrespective of their gestational age, which means most of them might already have undergone general screening for STIs. This could be the reason behind the high percentage of women reporting STI testing history.

Minor comments

Line 92-93: Is there a specific reason that Nepal was chosen as the first pilot site for implementation of the new WHO protocol?

Thank you for this comment. Nepal was selected as the first pilot site for implementation of the new WHO protocol because of the following reasons: (i) information on the burden of STIs among pregnant women in Nepal and in South East Asia was lacking, (ii) we were able to identify a setting with well-established laboratory setting that was already using GeneXpert platform for screening tuberculosis, and (iii) Two of the on-site researchers/clinicians involved in this study had conducted a similar study among married non-pregnant women in Nepal (Shakya et al., 2018). We believed that our proposed study would benefit from their experiences and expertise in conducting a similar study.

Reference:

Shakya S, Thingulstad S, Syversen U, Nordbø SA, Madhup S, Vaidya K, et al. Prevalence of Sexually Transmitted Infections among Married Women in Rural Nepal. Infectious diseases in obstetrics and gynecology. 2018;2018.

Line 201: This seems to be a repeat of line 199?

Thank you for pointing this out. We have now deleted the repetitive line from the manuscript.

Line 211: I don’t think Wet should be capitalized?

We have now replaced “Wet” with “wet”.

Line 212 and Line 214: I don’t think the nonspecific/specific and the quotation marks around non-treponemal and treponemal are needed?

We have now omitted the quotation marks.

Line 221: HBsAg not HBsAG

We have now replaced “HBsAG” with “HBsAg”.

Line 300 to 303: I am unsure about this argument as the prevalence of STIs is generally higher in Brazil than Nepal?

We agree with the reviewer’s comment regarding the higher prevalence of STIs in Brazil compared to Nepal.

Based on this comment we have edited the following statements in the discussion as noted above:

We have removed this statement in the discussion: A study conducted in Brazil reported similar prevalence of trichomoniasis (7.7%) among young pregnant women using a highly sensitive nucleic acid amplification test [21], supporting the sensitivity of detection in our study.

Reviewer 2

Thank you for this suggestion. We have now paraphrased the introduction section of the abstract to specify harmful effects of STIs on pregnancy outcomes and infants. As suggested, we have also added the following sentence under the methods section on page 3, line 48-50 of the revised manuscript:

“Tests for CT, NG and trichomoniasis were done as part of the prevalence study while tests for syphilis and HIV were done as part of the routine antenatal testing.”

2. Introduction: Line 75 "may be asymptomatic OR may experience" - should this be and as these are not mutually exclusive categories (symptoms and outcomes).

Thank you for pointing this out. We agree with the reviewer’s comment regarding the categories not being mutually exclusive. We have now replaced ‘or’ with ‘and’.

- It would be helpful to add in the prevalence reported in other studies in the introduction even in high-risk populations or the study of married women in Nepal. Also please cite the HIV prevalence from UNAIDS for Nepal to give context to the study.

Thank you for this suggestion. We have now added the prevalence of STIs for the high-risk populations. We have also added the HIV prevalence from UNAIDS for Nepal and cited the given below reference:

Reference:

UNAIDS. Country Progress Report Nepal. To contribute to global AIDS monitoring report 2017. Accessed on 15 March 2021 at https://www.unaids.org/sites/default/files/country/documents/NPL_2018_countryreport.pdf.

3. Methods: were partners informed about the partner's STI diagnosis? Were they referred for treatment or testing? how long did it take to test and contact participants?

Thank you for these questions. The study team did not inform about the women’s STI diagnosis to their partners. Only women were informed about their diagnosis who were then called for a follow-up counseling and treatment. During the counseling, the gynecologists also discussed about the need for partner testing with women. We have specified this under the treatment section. Test results were ready within a week. Women with positive test results were then contacted by RA by calling in their personal phone numbers to come to the clinic for a follow-up visit for the treatment. We have added the following sentence on page 12, line 261-262:

“Test results were dispatched within a week. Women with positive test results were contacted by the RA using personal phone numbers and asked to return for treatment.”

For statistical analysis, it may be better to conduct a multivariate analysis that controls for other covariates like age, gestational age, education, etc. if you want to test hypotheses of associations between STI diagnosis and age, education, etc. using a multivariate logistic regression model. Otherwise, I would avoid making hypotheses and presenting statistics from statistical tests as presented.

We understand the reviewer’s concern regarding the conduct of multivariate analysis controlling for other covariates; however, it was beyond the scope of our study. To address the issue, we have omitted the given below paragraph from the manuscript:

The high rate of CT and trichomoniasis infection in this study was observed among younger women ≤29 years (86%, 95% CI: 76.3-95.7), which is similar to the findings of a study conducted among pregnant women in Egypt where the high rate of infection was reported in age group of 20–30 years (29). Younger women are at higher risk of acquiring infection because of a combination of behavioral, biological, and cultural reasons. For some STDs, such as CT, young women may have increased susceptibility to infection because of increased cervical ectopy, which although is a normal finding in young women, make them more susceptible to infection (30). This study further highlights the need to strengthen the efforts to screen and treat STIs during antenatal care, mainly among the younger age group women.

Further, we added the given below statement under the limitations section:

“Future prevalence studies could determine the correlates of STIs using multivariate analysis and a larger sample size.”

4. Results:

Table 1. Did you record what kind of STI tests women had had in past as the % seems high. Was that for HIV or syphilis in prior pregnancies?

The investigators were not able to record what kind of STI tests women had had in the past, as the women did not remember the name of the test nor did they have any record of the test. It was completely based on women’s memory of the past that might have led to the high percentage of STI test reporting. Women did not specify whether the test was done for HIV or syphilis in prior pregnancies as they were not informed, thus, highlighting the lack of proper counseling during the antenatal care.

And why do the # differ in ever testing and unknown STI test results (90 vs 89 and 501 vs 502)?

We would like to thank the reviewer for pointing this issue out. Past test result for STIs should have been among the women who had ever tested for STIs in the past, i.e., 501. We have now updated the numbers in Table 1.

Please include abortion/miscarriage in the line "no abortion" as they were combined in the question.

As suggested, we have now included abortion/miscarriages in the line “no abortion” of Table 1.

In this study, a p-value less than 0.05 was considered statistically significant, hence, we did not include the borderline significance (p=0.08) as statistically significant result. We have added the following statement under the statistical analysis section on page 13, line 293-294:

“A p-value less than 0.05 was considered statistically significant.”

While we understand the reviewer’s concern regarding the conduct of multivariate analysis, it was beyond the scope of our study. Future prevalence studies could determine the correlates of STIs using multivariate analysis.

We have added the following acknowledgement of this limitation in the discussion section:

“Future prevalence studies could determine the correlates of STIs using multivariate analysis and a larger sample size.”

Please add this outcome about limited treatment uptake to the abstract and conclusions/recommendations if there is space.

Thank you for this valuable suggestion. Due to the stigma associated with STIs, male partners were not directly informed about the women’s STI results. Women were informed about their result directly over a phone call and asked to come for the treatment. Women who came back for the treatment were then referred to the gynecologists who along with the treatment discussed about the need of partner testing with the women. This information has been included under the treatment section of the manuscript.

For the duration it took to give feedback on the results, we added “contacting women within a week (from sample collection to results dispatch)” on page 19, line 430-431.

Regarding the refusal of treatment and what can be done to improve it, we have included the following sentence under the discussion section on page 19, line 432-434:

“Further, refusal of more than half of the women to re-visit clinic just for the treatment of STI was alarming. Strategies to improve testing and point of care treatment on the same visit should be prioritized.”

Since the main aim of the pilot study was to enhance STI surveillance and not to provide clinical care, the authors did not highlight about the limited treatment uptake in the abstract.

The thoughtful comments and guidance of the PLOS ONE reviewer is greatly appreciated. The authors feel that the reviewers’ revisions as well as other small clarifications have strengthened the focus and content of this manuscript submission. We look forward to the PLOS ONE decision.

Kind regards,

Rubee Dev, PhD, MPH

University of Alberta

Faculty of Nursing

Edmonton, Canada

Email: rubee@ualberta.ca

Phone: +1 778-821-2375

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PLoS One. doi: 10.1371/journal.pone.0250361.r003

Decision Letter 1

R Matthew Chico

6 Apr 2021

PONE-D-21-02130R1

Dear Dr. Dev,

We’re pleased to inform you that your manuscript has been judged scientifically suitable for publication and will be formally accepted for publication once it meets all outstanding technical requirements.

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Academic Editor

PLOS ONE

Additional Editor Comments (optional):

Reviewers' comments:

PLoS One. doi: 10.1371/journal.pone.0250361.r004

Acceptance letter

R Matthew Chico

14 Apr 2021

PONE-D-21-02130R1

Dear Dr. Dev:

I'm pleased to inform you that your manuscript has been deemed suitable for publication in PLOS ONE. Congratulations! Your manuscript is now with our production department.

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on behalf of

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Associated Data

This section collects any data citations, data availability statements, or supplementary materials included in this article.

Supplementary Materials

S1 Checklist. STROBE statement—Checklist of items that should be included in reports of cross-sectional studies.

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Data Availability Statement

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PERMALINK

Prevalence assessment of sexually transmitted infections among pregnant women visiting an antenatal care center of Nepal: Pilot of the World Health Organization’s standard protocol for conducting STI prevalence surveys among pregnant women

Rubee Dev

Shambhu P Adhikari

Anjana Dongol

Surendra K Madhup

Pooja Pradhan

Sunila Shakya

Shrinkhala Shrestha

Sneha Maskey

Melanie M Taylor

Roles

Abstract

Introduction

Materials and methods

Results

Conclusions

Introduction

Materials and methods

Study design

Study site and population

Sample size and sampling technique

Eligibility criteria for the enrolment site and pregnant woman

Study procedures

Enrollment, consenting, counseling, and follow-up of participants

Laboratory tests

Treatment

Statistical analysis

Ethical approval

Results

Socio-demographic characteristics

Table 1. Characteristics of pregnant women visiting antenatal care clinic in Dhulikhel Hospital, Nepal (N = 591).

Prevalence of STIs

Table 2. Prevalence of STIs among pregnant women visiting antenatal care clinic in Dhulikhel Hospital, Nepal (N = 591).

Table 3. Characteristics of study participants by types of STI (N = 591).

Treatment of participants

Discussion

Conclusions

Supporting information

Acknowledgments

Data Availability

Funding Statement

References

Decision Letter 0

R Matthew Chico

Roles

Author response to Decision Letter 0

Decision Letter 1

R Matthew Chico

Roles

Acceptance letter

R Matthew Chico

Roles

Associated Data

Supplementary Materials

Data Availability Statement

ACTIONS

PERMALINK

RESOURCES

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