Prevalence of Chlamydia trachomatis and Neisseria gonorrhoeae infection and associated factors among asymptomatic pregnant women in Botswana

Abstract

Background

Chlamydia trachomatis (C. trachomatis) and Neisseria gonorrhoeae (N. gonorrhoeae) are curable sexually transmitted infections (STIs) that cause adverse pregnancy and neonatal outcomes. Most countries, including Botswana, do not offer C. trachomatis or N. gonorrhoeae screening during antenatal care (ANC) and instead use a syndromic approach for management of STIs.

Methods

The Maduo Study is a prospective, cluster-controlled trial in Botswana evaluating the impact of diagnostic screening for antenatal C. trachomatis and N. gonorrhoeae infections to prevent adverse neonatal outcomes. Using baseline data from the Maduo Study (March 2021–March 2022), we determined the prevalence of C. trachomatis and N. gonorrhoeae infection among asymptomatic pregnant women in Botswana and correlates of infection using multivariable logistic regression.

Results

Of 251 women who underwent C. trachomatis and N. gonorrhoeae screening at first ANC visit, 55 (21.9%, 95%CI 17.0–27.5) tested positive for C. trachomatis, 1 (0.4%, 95%CI 0–2.2) for N. gonorrhoeae; and 2 (0.8%, 95%CI 0–2.8) for dual C. trachomatis and N. gonorrhoeae infection. Older age was associated with lower odds (aOR 0.93; 95%CI 0.88–0.98; p = 0.011) while any alcohol use during pregnancy was associated with higher odds (aOR = 3.53; 95%CI 1.22–10.16; p = 0.020) of testing positive for C. trachomatis or N. gonorrhoeae.

Conclusions

A high frequency of C. trachomatis infections was detected among asymptomatic pregnant women in Botswana indicating that many antenatal STIs are missed by the syndromic management approach. Our results highlight the need for diagnostic C. trachomatis screening during ANC in Botswana and other low- and middle-income countries that rely solely on the syndromic approach for management of STIs.

Keywords

Africa Botswana STIs chlamydia gonorrhoea pregnancy antenatal care

Introduction

Chlamydia trachomatis (C. trachomatis) and Neisseria gonorrhoeae (N. gonorrhoeae) are treatable sexually transmitted infections (STIs). If undiagnosed and untreated in pregnancy, C. trachomatis and N. gonorrhoeae can cause adverse maternal and neonatal outcomes including pre-term birth, stillbirth, spontaneous abortion, small for gestational age, pelvic inflammatory disease and infertility.^1,2 In Botswana, as in most developing countries, diagnostic C. trachomatis and N. gonorrhoeae screening is not routinely offered during antenatal care (ANC).³ Instead, Botswana adapted World Health Organization (WHO)-endorsed syndromic management, which relies on the use of algorithms to classify signs and symptoms into STI syndromes, and treatment with standardised combinations of antibiotics.⁴ Syndromic management has low sensitivity, and misses asymptomatic infections.⁵ An older study (2000–2001) conducted in Gaborone, Botswana found that diagnosing antenatal C. trachomatis and N. gonorrhoeae based on symptoms (vaginal discharge and/or lower abdominal pain) had a sensitivity of 16%.⁶ Other studies conducted in Botswana and South Africa have shown that 50–76% of C. trachomatis and N. gonorrhoeae infections are asymptomatic.^7–9 Furthermore, during pregnancy, many women experience an increase in vaginal discharge which can lead to overtreatment for STIs in settings where syndromic management is used.^9,10

Due to the lack of routine antenatal screening, the prevalence of C. trachomatis and N. gonorrhoeae infection among pregnant women is unknown. Only two studies have reported C. trachomatis and N. gonorrhoeae prevalence among pregnant women.^6,7 The first study reported a prevalence of 8% for C. trachomatis and 3% for N. gonorrhoeae infection among pregnant women in Botswana.⁶ However, this study is over 20 years old and was implemented prior to roll-out of antiretroviral therapy in Botswana.¹¹ The second study found a C. trachomatis and N. gonorrhoeae prevalence of 8% and 1.3%, respectively, however the sample was limited to a single antenatal clinic in Gaborone, Botswana.⁷ In addition, these studies enrolled both symptomatic and asymptomatic pregnant women.

We determined the prevalence and correlates of C. trachomatis or N. gonorrhoeae infection among asymptomatic pregnant women in Gaborone, Botswana, where asymptomatic was defined as not requiring syndromic management for an STI by a healthcare provider in the last 30 days, including day of their first ANC visit. Thus, our sample includes women who, if infected with C. trachomatis or N. gonorrhoeae, were missed by the syndromic management approach and therefore represent a missed opportunity for treatment.

Methods

Ethical considerations

The Maduo Study was approved by the Botswana Health Research Development Committee of the Botswana Ministry of Health and a reliance agreement was approved by the University of Southern California.

Parent study and setting

We conducted a cross-sectional analysis using baseline data from participants in the testing arm of the Maduo Study, an ongoing, cluster-controlled trial evaluating the impact of diagnostic screening for antenatal C. trachomatis and N. gonorrhoeae infections to prevent adverse neonatal outcomes. Women were recruited from four District Health Management Team clinics in Gaborone, Botswana.¹² Botswana national ANC guidelines recommend that pregnant women attend five follow-up visits during pregnancy, after the initial ANC visit, at 16–20, 24–28, 32, 34–36, and 38–40 weeks.⁴ At the first ANC visit, assessment of obstetric and medical history, and a pelvic examination is performed by a midwife and women undergo human immunodeficiency virus (HIV) and syphilis testing. Women are identified for syndromic management through self-reported and clinically determined signs and symptoms. Women meeting the criteria for an STI syndrome are provided with a combination of antibiotics which target all the common causes of that particular syndrome.⁴

Recruitment and enrolment

Women were eligible to participate in the study if they were aged ≥15 years, currently pregnant, attending their first ANC visit, ≤27 weeks’ gestation, residing in the greater Gaborone area through time of delivery and first postnatal care visit, willing to be tested for C. trachomatis and N. gonorrhoeae, potentially have infants tested at postnatal care, not treated for an STI in the last 30 days, and not identified for STI syndromic management at the first ANC visit. Initially, women in the clinic waiting room were provided with information about the study by a research assistant. Thereafter, recruitment and informed consent was provided after participants were seen by a midwife and the need for syndromic management was ascertained. Reasons for ineligibility and decline of participation were documented. Eligible women who were interested in the study provided informed written consent for participation. For women under the age of 18, verbal parental consent was obtained in addition to participant informed assent.

Sexually transmitted infection screening and treatment

Participants at testing clinics of the Maduo Study provided a self-collected vaginal specimen using the Xpert^® Swab Specimen Collection Kit for diagnostic C. trachomatis and N. gonorrhoeae testing. Vaginal specimens were processed using the Cepheid Xpert^® CT/NG test, which takes 90 min to result. Women were provided results within 24 h. At study start, samples were processed on site, however, due to clinic space limitations, sample processing was moved to the study offices at the Botswana Harvard Partnership in September 2021. Participants testing positive for C. trachomatis or N. gonorrhoeae were treated by a study nurse, under the supervision of a study doctor, in accordance with US CDC guidelines (C. trachomatis: 1 g oral azithromycin; N. gonorrhoeae: 500 mg intramuscular ceftriaxone) and counselled on partner notification as per Botswana STI guidelines.¹³ They were additionally offered expedited partner treatment, which is not currently part of Botswana STI guidelines.

Data collection

All participants completed an interviewer-administered questionnaire, which collected information on socioeconomic and demographic characteristics, obstetric and medical history, partner characteristics, including history of intimate partner violence (using the Conflict Tactics Scale);¹⁴ recent sexual history, HIV status and treatment, previous STI diagnoses and treatment, depression risk (using the Edinburgh Postnatal Depression Scale),¹⁵ alcohol use (using the AUDIT-C questionnaire)¹⁶ and smoking during pregnancy. Additional information was abstracted by study staff from the participant hand-held obstetric record, including last menstrual period, estimated date of delivery, past obstetric history, hospital admissions during current pregnancy, rapid HIV and laboratory (haemoglobin, syphilis, and Rhesus factor) test results as well as height, weight and blood pressure taken at the first ANC visit. All study data were entered directly into REDCap (Research Electronic Data Capture, Vanderbilt University).

Statistical analysis

Descriptive statistics were used to assess the socioeconomic and demographic characteristics of the study population. Prevalence of C. trachomatis and N. gonorrhoeae at first ANC visit was determined by dividing the number of individuals that tested positive by the number of women enrolled in the testing arm, and exact binomial 95% confidence intervals for prevalence were estimated.

Multivariable logistic regression analysis was used to assess factors associated with C. trachomatis or N. gonorrhoeae infection. Potential correlates of infection were identified based on findings from previous literature.^6,7,9,17 These variables included maternal age, gestational age at first ANC visit, relationship status, education, income, HIV status, nationality, gravida, parity, recruitment site, concern about having an STI, diagnosed with an STI within the last year, smoking and alcohol during pregnancy, depression risk, intimate partner violence, and variables concerned with father of baby i.e. STI symptoms, HIV status, whether father of baby is current partner, condom frequency prior to pregnancy with father of baby, and whether father of baby has other partners. Variables with a p-value ≤0.25 in the univariable analysis were included in the multivariable model. Multicollinearity was assessed by calculating the variance inflation factor and the intraclass correlation coefficient was calculated to check for clustering by clinic. Stata version 17 was used for all statistical analyses.

Results

We enrolled 251 pregnant women in the testing arm of the Maduo Study between 1 March 2021 and 30 March 2022.

Characteristic of study participants

Baseline characteristics of participants are shown in Table 1. Median age of participants in the testing arm was 27 years (interquartile range 24, 33). Most women had a secondary level of education or below (73.3%) and were unmarried (85.3%). Forty percent of women earned ≤ BWP 2000 (∼150 USD) per month and most were citizens of Botswana (92.0%). The majority of women had been pregnant before (n = 177, 70.5%) and 91 (36.3%) women had given birth more than once. Fifty-four (21.5%) women were living with HIV.

Table 1.

Characteristics of participants enrolled in the Maduo Study.

	n = 251
	mean (IQR)
Age (years)	27 (24–33)
Gestational age at first ANC (weeks)	17 (12–21)
	n (%)
Education
Secondary or below	184 (73.3)
Tertiary or higher	67 (26.7)
Marital status
Married	37 (14.7)
Not married	214 (85.3)
Income
≤BWP2000/month	102 (40.6)
>BWP2000/month	130 (51.8)
Unknown	18 (7.2)
Missing	1 (0.4)
Nationality
Motswana	231 (92.0)
Zimbabwean	19 (7.6)
Other	1 (0.4)
HIV status
Not living with HIV	197 (78.5)
Living with HIV	54 (21.5)
Gravida
Primigravida	74 (29.5)
Multigravida	177 (70.5)
Parity
Nulliparous	82 (32.7)
Primiparous	78 (31.1)
Multiparous	91 (36.3)
Recruitment site
Old naledi clinic	102 (40.6)
Mafitlhakgosi clinic	36 (14.3)
Lesirane clinic	88 (35.1)
Tlokweng clinic	25 (10.0)

ANC antenatal care, BWP Botswana Pula; IQR interquartile range.

Thirty-four (13.6%) women had concerns they had an STI at the first ANC visit and nine (3.6%) reported they had been told they had an STI within the last year by a healthcare worker. Most women said the father of the baby was their current partner (n = 245, 97.6%) and no women reported a current partner other than father of the baby.

Prevalence of C. trachomatis and N. gonorrhoeae

Of 251 women who underwent C. trachomatis and N. gonorrhoeae screening at their first ANC visit, 55 (21.9%, 95% confidence interval [CI] 17.0–27.5) tested positive for C. trachomatis, one (0.4%, 95%CI 0–2.2) for N. gonorrhoeae; and two (0.8%, 95%CI 0.1–2.8) for dual C. trachomatis and N. gonorrhoeae infection (Table 2).

Table 2.

C. trachomatis and/or N. gonorrhoeae prevalence among pregnant women in Botswana, screened at the first antenatal care visit.

	First antenatal care visit (n = 251)
	% (n/N)	95% CI
C. trachomatis	21.9 (55/251)	17.0	27.5
N. gonorrhoeae	0.4 (1/251)	0	2.2
C. trachomatis and N. gonorrhoeae	0.8 (2/251)	0.1	2.8

Prevalence of STIs by age is shown in Figure 1. The highest prevalence of C. trachomatis was in the 15–24 age group (31.0%) while N. gonorrhoeae prevalence was 1.4% in both 15–24 and 25–35 age groups.

Figure 1.

Prevalence of Chlamydia trachomatis (C. trachomatis) and Neisseria gonorrhoeae (N. gonorrhoeae) by age among pregnant women in Botswana.

Factors associated with C. trachomatis or N. gonorrhoeae infection

The results of the regression analysis to identify factors independently associated with C. trachomatis or N. gonorrhoeae infection are shown in Table 3. In multivariable logistic regression analysis, older age was associated with lower odds (adjusted odds ratio [aOR] 0.93; 95%CI 0.88–0.98; p = 0.011) while any alcohol use during pregnancy was associated with three times higher odds (aOR = 3.53; 95%CI 1.22–10.16; p = 0.020) of testing positive for C. trachomatis or N. gonorrhoeae.

Table 3.

Univariable and multivariable logistic regression results assessing correlates of C. trachomatis or N. gonorrhoeae infection among pregnant women in Botswana.

	Total^a n = 251	C. trachomatis or N. gonorrhoeae negative^a n = 193	C. trachomatis or N. gonorrhoeae positive^a n = 58	uOR (95% CI)	p-value	aOR (95% CI)	p-value
Age (years)	27 (24–33)	28 (24–34)	26 (22–29)	0.93 (0.88–0.98)	0.004	0.93 (0.88–0.98)	0.011
Gestational age at first ANC visit (weeks)	17 (12–21)	17 (12–21)	17 (14–21)	1.03 (0.98–1.09)	0.287
Education
Secondary or below	184	139 (75.5)	45 (24.5)	ref	ref
Tertiary or higher	67	54 (80.6)	13 (19.4)	0.76 (0.37–1.49)	0.402
Marital status
Not married	214	161 (75.2)	53 (24.8)	ref	ref	ref	ref
Married	37	32 (86.5)	5 (13.5)	0.47 (0.18–1.28)	0.141	0.70 (0.24–2.02)	0.509
Income^b
≤BWP2000/month	102	75 (73.5)	27 (26.5)	ref	ref
>BWP2000/month	130	103 (79.2)	27 (20.8)	0.73 (0.40–1.34)	0.309
Unknown	18	14 (77.8)	4 (22.2)	1.09 (0.33–3.58)	0.887
Nationality
Motswana	231	176 (76.2)	55 (23.8)	ref	ref
Zimbabwean/other	20	17 (85.0)	3 (15.0)	0.56 (0.16–2.00)	0.376
HIV status
Not living with HIV	197	150 (76.1)	47 (23.9)	ref	ref
Living with HIV	54	43 (79.6)	11 (20.4)	0.82 (0.39–1.71)	0.591
Gravida
Primigravida	74	56 (75.7)	18 (24.3)	1.10 (0.58–2.08)	0.768
Multigravida	177	137 (77.4)	40 (22.6)	ref	ref
Parity
Nulliparous	82	62 (75.6)	20 (24.4)	1.15 (0.56–2.32)	0.707
Primiparous	78	60 (76.9)	18 (23.1)	1.07 (0.52–2.20)	0.865
Multiparous	91	71 (78.0)	20 (22.0)	ref	ref
Recruitment site
Old Naledi Clinic	102	74 (72.6)	28 (27.5)	ref	ref	ref	ref
Mafitlhakgosi Clinic	36	30 (83.3)	6 (16.7)	0.53 (0.20–1.41)	0.202	0.76 (0.27–2.14)	0.605
Lesirane Clinic	88	68 (77.3)	20 (22.7)	0.78 (0.40–1.51)	0.455	0.92 (0.45–1.89)	0.825
Tlokweng Clinic	25	21 (84.0)	4 (16.0)	0.50 (0.16–1.60)	0.244	0.64 (0.19–2.15)	0.469
Concerns of an STI
Yes	34	25 (73.5)	9 (26.5)	1.21 (0.53–2.79)	0.652
No	192	148 (77.1)	44 (22.9)	ref	ref
Don’t know	25	20 (80.0)	5 (20.0)	0.84 (0.30–2.37)	0.743
STI diagnosis in last year^b
Yes	9	6 (66.7)	3 (33.3)	1.69 (0.41–6.98)	0.468
No	241	186 (77.2)	55 (22.8)	ref	ref
Is FOB current partner?
Yes	245	189 (77.1)	56 (22.9)	ref	ref
I don’t have a current partner	6	4 (66.7)	2 (33.3)	1.69 (0.30–9.46)	0.552
FOB HIV status different?
Yes	39	32 (82.1)	7 (17.9)	0.60 (0.24–1.48)	0.270	0.84 (0.32–2.19)	0.718
No	135	99 (73.3)	36 (26.7)	ref	ref	ref	ref
Don’t know	77	62 (80.5)	15 (19.5)	0.67 (0.34–1.31)	0.241	0.68 (0.32–1.45)	0.320
Condom frequency prior to pregnancy with FOB
Never	57	41 (71.9)	16 (28.1)	1.48 (0.72–3.01)	0.283
Yes, sometimes	134	106 (79.1)	28 (20.9)	ref	ref
Yes, always	60	46 (76.7)	14 (23.3)	1.15 (0.56–2.39)	0.703
Suspects FOB has other partners
Yes	17	15 (88.2)	2 (11.8)	0.39 (0.09–1.80)	0.229	0.41 (0.08–1.99)	0.268
No	134	100 (74.6)	34 (25.4)	ref	ref	ref	ref
Don’t know	100	78 (78.0)	22 (22.0)	0.83 (0.45–1.53)	0.550	1.06 (0.54–2.07)	0.866
FOB STI-related symptoms
Yes	11	9 (81.8)	2 (18.2)	0.75 (0.16–3.57)	0.713
No	209	161 (77.0)	48 (23.0)	ref	ref
Don’t know	31	23 (74.2)	8 (25.8)	1.17 (0.49–2.78)	0.727
Any alcohol in pregnancy
Yes	19	10 (52.6)	9 (47.4)	3.36 (1.29–8.73)	0.013	3.53 (1.22–10.16)	0.020
No	232	183 (78.9)	49 (21.2)	ref	ref	ref	ref
Smoking during pregnancy
Yes	5	2 (40.0)	3 (60.0)	5.21 (0.85–31.96)	0.075	2.85 (0.37–22.97)	0.314
No	246	191 (77.6)	55 (22.4)	ref	ref	ref	ref
Intimate partner violence
Yes	23	17 (73.9)	6 (26.1)	1.09 (0.41–2.92)	0.859
No	213	161 (75.6)	52 (24.4)	ref	ref
Declined	5	5 (100.0)	0 (0)	—	—
Depression risk
Yes	29	22 (75.9)	7 (24.1)	1.07 (0.43–2.64)	0.889
No	222	171 (77.0)	51 (23.0)	ref	ref

Abbreviations: ANC antenatal care, BWP Botswana Pula, C. trachomatis Chlamydia Trachomatis, N. gonorrhoeae Neisseria gonorrhoeae, STI sexually transmitted infection, HCW healthcare worker, FOB father of baby, uOR unadjusted odds ratio, aOR adjusted odds ratio.

^aexpressed as n, n (%) or median(IQR).

^bIntimate partner violence, missing data for 10, STI diagnosis in last year and Income, missing data for 1.

Discussion

We found a high prevalence of C. trachomatis infections among 251 asymptomatic pregnant women attending four public antenatal clinics in Gaborone, Botswana (C. trachomatis only 21.9%; dual C. trachomatis and N. gonorrhoeae 0.8%). Alcohol use during pregnancy was significantly associated with increased odds of testing positive while older age was associated with reduced odds of a positive C. trachomatis or N. gonorrhoeae test.

The prevalence of C. trachomatis reported in this study was higher than described in previous studies conducted in Botswana, among pregnant women. In a study by Wynn et al., (2018) conducted between 2015 and 2016 at a single ANC clinic (n = 400), the prevalence of C. trachomatis (8%) was 65% lower than that observed in our study.⁷ Similarly, a Botswana-based study by Romoren et al., (2007), among 703 pregnant women in 13 antenatal clinics between 2000 and 2001, reported a C. trachomatis prevalence of 8%.⁶ The above-mentioned studies did not restrict eligibility criteria to asymptomatic women and yet, prevalence of C. trachomatis in our study was still appreciably higher. The observed C. trachomatis prevalence was also higher than reported in systematic reviews by Davey et al., (2016; 4.4%, 95%CI 2.3–6.6), Newman et al., (2019; 4.2%, 95%CI 3.7–4.7) and Hussen et al., (2018; 7.8%, 95%CI 5.6–10.6) which looked at STI prevalence among pregnant women in Southern Africa, women in the WHO African Region, and women of reproductive age in Sub-Saharan Africa, respectively.^18–20

The Botswana-based studies by Wynn et al. and Romoren et al. were conducted 5 and 20 years prior to the current study, respectively.^6,7 The high C. trachomatis prevalence observed in our study could therefore reflect an increase in prevalence of C. trachomatis among pregnant women in Botswana over time. In the previous studies, testing was not restricted to women attending their first ANC visit, as in our study, potentially giving participants more opportunities to be treated syndromically, resulting in a lower prevalence. As the previous studies did not report past treatment in pregnancy, we were unable to explore these differences further. The higher prevalence of C. trachomatis observed in our study, relative to other studies conducted in Botswana, could also be partly explained by differences in study populations.^6,7 Compared to participants in the testing arm of this study, women enrolled in the study by Wynn et al. had a slightly higher median age (30 vs 27 years) and a larger proportion were married (22% vs 15%) and had a tertiary education level (40% vs 27%).⁷ Younger age, lower education level, and unmarried as opposed to married relationship status have all been shown to be associated with increased STI risk in other studies.^6,9,17,21 Further, in our study, 41% of women in the testing arm were enrolled at Old Naledi Clinic which is located in a neighbourhood with poorer socioeconomic conditions, compared to the other recruitment sites. Although we could not compare income level with the previous studies conducted in Botswana, due to lack of income data reported, these social and economic factors could explain the higher STI prevalence observed in our study. Participants at Old Naledi Clinic (27.5%) had a higher STI prevalence compared to other recruitment sites (Mafitlhakgosi: 16.7%, Tlokweng: 16.0%, Lesirane: 22.7%) however we did not find recruitment site to be significantly associated with testing positive for C. trachomatis or N. gonorrhoeae.

The observed C. trachomatis prevalence was similar to two studies conducted in South Africa in which the study population included a higher proportion of women living with HIV compared to our study.^8,17 The first study among 1459 pregnant women (symptomatic or asymptomatic) in KwaZulu Natal between 2008 and 2010 identified a C. trachomatis prevalence of 18%.⁸ Women who were not living with HIV or had an unknown HIV status were enrolled in this study and 39% of women tested positive for HIV at the first ANC visit. The second study conducted in Cape Town among 242 pregnant women (symptomatic or asymptomatic) between 2017 and 2018 reported a C. trachomatis prevalence of 20%.¹⁷ The proportion of women living with HIV in this study (44%) was double that reported in our study (22%).

The N. gonorrhoeae prevalence in our study (1%) was similar to the prevalence observed in previous studies among pregnant women in Botswana, including the study by Wynn et al. (1%), but slightly lower than that reported by Romoren et al. (3%).^6,7 Previous South African studies have reported a higher prevalence of N. gonorrhoeae (6%) compared to the N. gonorrhoeae prevalence in the current study.^9,17 Those studies had a higher proportion of women living with HIV (44%–85%) relative to our study (22%) and they enrolled both symptomatic and asymptomatic women. The N. gonorrhoeae prevalence in our study was also lower than observed in the systematic review by Davey et al. (4.6%, 95%CI, 4.0–5.2) among pregnant women in Southern Africa but similar to that observed in the review by Newman et al. (0.8%, 95%CI 0.6–1.0) among women in the WHO African Region.^18,19

Consistent with other studies, we found older age to be associated with decreased likelihood of testing positive for C. trachomatis or N. gonorrhoeae.^6,9,17 Our findings also support those of previous research which have found an association between alcohol use and increased likelihood of STI positivity.^22–25 One possible explanation for the association observed between alcohol use during pregnancy and higher risk of STI acquisition is that alcohol use may increase sexual behaviours such as condomless sex and having multiple sex partners.²²We found neither HIV status of the participant nor HIV status concordance/discordance with father of the baby to be associated with testing positive for C. trachomatis or N. gonorrhoeae, which is inconsistent with prior studies in Southern Africa.^8,9,17 A possible explanation for that lack of association could be that women living with HIV in our study were older and more likely to be married than women living without HIV.

Our findings in this study of a high prevalence of C. trachomatis infection among asymptomatic pregnant women in Botswana show that the syndromic management approach, used in Botswana to manage STIs, is likely to miss many chlamydial infections. Romoren et al. reported that using the syndromic management vaginal discharge syndrome algorithm, which is currently widely used in Botswana for STI management, failed to effectively identify many women with C. trachomatis or N. gonorrhoeae infection.⁶ Other studies in Southern Africa have shown that syndromic management is not an effective tool for identifying C. trachomatis and N. gonorrhoeae infections.^26,27 It is estimated that up to two-thirds of curable STIs are asymptomatic.^8,9 In light of that, the high prevalence of STIs among pregnant women which go undetected may be contributing to the high rates of adverse maternal and neonatal outcomes in Botswana.^28,29 Thus, to reduce the burden and negative sequelae of asymptomatic STI infections in Botswana, diagnostic screening of STIs may be valuable.

This study is not without limitations. First, our study population was not representative of the general population of pregnant women in Botswana given the small sample size and recruitment in the capital city, Gaborone. However, when compared to the Tsepamo Study, a nationally-representative birth outcomes surveillance study that captures ∼70% of births in Botswana, the distributions of education, gravida, HIV status, and marital status were generally similar to our sample, with the exception of age.³⁰ Second, given our questionnaire included sensitive questions related to sexual history and behaviours during pregnancy, our findings may be subject to self-report/social desirability bias. Sexual behaviours such as number of sex partners, alcohol use and smoking during pregnancy and condom frequency prior to pregnancy, may have been under-reported and therefore, estimating the association between these variables and positive C. trachomatis or N. gonorrhoeae infection would be biased. However, to mitigate that bias, study staff were trained and experienced at asking sensitive questions and the interviews took place in a private area. Finally, the study may be underpowered for some of the associations tested in regression analysis and therefore, important associations could have been missed.

In conclusion, we found a high prevalence of C. trachomatis infection among asymptomatic pregnant women in Gaborone, Botswana. The results demonstrate that many antenatal STIs are likely missed if programmes solely rely on syndromic management. In efforts to decrease morbidity among pregnant women and infants, policy makers and health authorities in Botswana and other LMICs may need to consider implementation of routine C. trachomatis screening in all pregnant women. Further research is needed to understand the short and long-term costs and benefits of antenatal STI screening to reduce adverse outcomes among women and infants.

Footnotes

Acknowledgements

We wish to thank Cepheid for loaning the GeneXpert instrument and provision of Xpert^® CT/NG kits for this study. We would also like to thank the women who participated in the Maduo study and the staff at participating District Health Management Team clinics.

Authors’ contributions

AW, JDK, CM, AM and RR conceptualised and designed the study. AM, RR, SS, BB, KR, LT, NN, NM and MM implemented the study. AM cleaned and analysed the data, with support from AW. AM wrote the first draft of the manuscript and AW, RR, CMB, EH, CM and JK contributed to subsequent drafts of the manuscript. All authors have read and approved the final manuscript.

Declaration of conflicting interests

The author(s) declared no potential conflicts of interest with respect to the research, authorship, and/or publication of this article.

Funding

The author(s) disclosed receipt of the following financial support for the research, authorship, and/or publication of this article: This work was supported by the Eunice Kennedy Shriver National Institute of Child Health and Human Development (NICHD) [grant number R21 HD100821-01]. The funding source had no role in the design and conduct of the study, data collection, analysis, reporting, and decision to submit the manuscript for publication.

ORCID iDs

Aamirah Mussa

Emily Hansman

Jeffrey D Klausner

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