Research Article

Prevalence and Factors Associated with Sexually Transmitted Infections among Men Who Have Sex with Men Initiating HIV Pre-Exposure Prophylaxis in Benin

by Oscar Nduwimana1,2*, Luc Béhanzin3,4, Fernand A. Guédou4,5, Ella Goma-Matsétsé5,6, Marius Olodo5, Alban Dossouvo5, Flore Gangbo7,8, Djimon Marcel Zannou8,9, Alary Michel1,2,10, Souleymane Diabaté1,2

1Département de médecine sociale et préventive, Université Laval, Québec, Québec, Canada

2Centre de recherche du CHU de Québec - Université Laval, Québec, Québec, Canada

3École nationale de formation des techniciens supérieurs en santé publique et en surveillance épidémiologique, Université de Parakou, Parakou, Bénin

4Organisation pour la Promotion de la Santé et le Développement communautaire, Cotonou, Bénin

5Dispensaire IST, Centre de santé communal de Cotonou 1, Cotonou, Bénin

6Département de microbiologie-Infectiologie et d’immunologie, Université Laval, Québec, Québec, Canada

7Programme Santé de Lutte contre le Sida, Cotonou, Bénin

8Faculté des sciences de la santé, Université d’Abomey-Calavi, Cotonou, Bénin

9Centre national hospitalier universitaire HMK, Cotonou, Bénin

10Institut national de santé publique du Québec, Québec, Québec, Canada

*Corresponding author: Oscar Nduwimana, Research Center of the CHU de Québec-Université Laval, Canada

Received Date: 13 September 2024

Accepted Date: 23 September 2024

Published Date: 26 September 2024

Citation: Nduwimana O, Béhanzin L, Guédou FA, Matsétsé EG, Olodo M, et al. (2024) Prevalence and Factors Associated with Sexually Transmitted Infections among Men Who Have Sex with Men Initiating HIV Pre-Exposure Prophylaxis in Benin. Arch Epidemiol 7: 154. https://doi.org/10.29011/2577-2252.100154.

Abstract

Background: Men who have sex with men (MSM) are at increased risk of sexually transmitted infections (STIs). Data on STIs among MSM in Benin are scarce. This study aimed to assess the prevalence and factors associated with Neisseria gonorrhoeae (NG), Chlamydia trachomatis (CT) and Treponema pallidum (TP) among 204 HIV-negative MSM initiating pre-exposure prophylaxis (PrEP) for HIV prevention in Cotonou, Benin. Methods: In this cross-sectional study, a questionnaire was completed and participants underwent a physical examination by a physician. Blood, anal, pharyngeal, and urinary samples were collected. Prevalences are presented with a 95% confidence interval (95% CI). Poisson regression was used to determine factors associated with STIs. Results: The prevalence was 18.6% (95% CI, 13.3% - 24.0%), 15.2% (95% CI, 10.3% –20.1%), 9.8% (95% CI, 5.7% - 13.9%) and 27.9% (95% CI, 21.8% - 34.1%) for CT, NG-all sites, anorectal NG, and infection by either NG or CT (NG/

CT), respectively. STIs were generally asymptomatic (84.2% for NG/CT) and of biological extra-genital location (70.2% for NG/CT). One case of unconfirmed syphilis was observed. In multivariate analysis, being younger, not being single, and having more than four female sexual partners were associated with CT and NG/CT, while lower monthly income was associated with NG and/or CT. Relative youth, receptive anal sex and paid sex were associated with NG. Only receptive anal sex was associated with anorectal NG. Conclusion: NG and CT infections are common among HIV-negative MSM in Cotonou. Their asymptomatic and extra-genital nature could make syndromic management ineffective and extra genital screening necessary. Syphilis is rare among these MSM. STI control and prevention interventions should target young MSM and their female sexual partners.

Keywords: Gonorrhea; Chlamydia; Sexually Transmitted Infections; Men who have sex with Men; Africa

Introduction

Sexually transmitted infections (STIs), such as the human immunodeficiency virus (HIV) infection, gonorrhea, chlamydia and syphilis remain a major public health problem worldwide. Sub-Saharan Africa is one of the most affected regions [1]. In 2022, it accounted for 50% of all new HIV infections and 66% of all people living with HIV worldwide [2]. Men who have sex with men (MSM) are disproportionately affected by these STIs [2-5]. Recently, a study conducted among MSM initiating pre-exposure prophylaxis (PrEP) to prevent HIV infections in four main cities in West Africa (Abidjan-Côte d’Ivoire, Bamako-Mali, LoméTogo, and Ouagadougou-Burkina Faso) found a high prevalence of chlamydia and gonorrhea: 17.3% and 13.7%, respectively [6].

In Benin, while HIV prevalence in the general population aged 15-49 years was 0.9% in 2017, it was 7% among MSM [2]. In 2020, the incidence of HIV was 0.21 per 1,000 person-years in the general population and 59.1/1,000 person-years among MSM [2,7]. Accordingly, the health authorities of the country have decided to include oral-PrEP within the combined HIV Prevention Package for MSM. To guide the implementation of this biomedical HIV prevention strategy, an oral-PrEP demonstration project was conducted between August 2020 and October 2021 in Cotonou, the main city of Benin. This study was part of the demonstration project and aimed to describe the prevalence and factors associated with Chlamydia trachomatis (CT), Neisseria gonorrhoeae (NG) and Treponema pallidum (TP) infections at baseline. As far as we know, no data address this issue among HIV-negative MSM in Benin. The oral-PrEP demonstration project in which this study was included has been described in detail elsewhere [5].

Materials and methods

To allow for an outcome of interest, the assessment of a prevalence of 50% with a precision of 7%, the study sample was set at 204 participants. They were recruited from August 24 to November 24, 2020, using a two-stage sampling procedure. First, seven of the thirteen districts of Cotonou were selected with a probability proportional to size. Second, based on the size of each, a given number of HIV-negative MSM were selected using a random route method [8]. This process was facilitated by a mapping of the MSM community of Cotonou and its suburbs that was carried out by Bénin Synergie Plus, a MSM dedicated network  [9]. Overall, the recruitment was facilitated by Bénin Synergie Plus and a second identity network named Réseau Sida Bénin. Ten peer-facilitators from these two organizations mobilized the MSM community prior to recruitment. The information provided to MSM in the field was about STIs’ control, the study objective and procedures. The inclusion criteria were being born male, having sex with men, being HIV-negative and at least 18 years old, being a member of one of the two MSM networks of Cotonou (Benin Synergie Plus or Réseau Sida Bénin), living in Cotonou for at least six months, and agreeing to initiate PrEP.

NG, CT, and TP infections were explored at three different sites (pharyngeal, urethral and anal). NG/CT laboratory diagnosis was based on a real-time nucleic acid amplification technique using the GeneXpert platform (Cepheid, Sunnyvale, CA, USA). Fingertip and venous blood samples were collected for a rapid treponemal test and a rapid plasma reagin test for the diagnosis of syphilis using the One Step Multi-Infectious Disease Test (InTec Products, Inc., Xinyang, China). The One Step Multi-Infectious Disease Test was also used to confirm the HIV-negative status of the participants. HIV-positive men received immediate antiretroviral therapy. Following the clinical examination performed by the physician, all men with symptomatic STIs were treated according to national guidelines.

The potential determinants of STIs included sociodemographic variables such as age, marital status, education level, occupation, income, place of residence, religion, and nationality; variables related to sexual practices with men: sexual preference (homosexuality, bisexuality, or heterosexuality), sexual role (insertive, receptive, or versatile), type of sexual activity (oral sex, anal sex, or mutual sexual masturbation), type of partner (stable or casual), number of male partners in the past six months, concurrent male partners at the time of recruitment, condom use during sex, paid sex, and substance use; variables related to sexual practices with women: number and type (casual, regular) of female partners in the past six months; and information on STIs’ symptoms: irritation, sores in the genital region, and urethral discharge in the past six months and four days prior to recruitment. Information on these independent variables was collected through a validated questionnaire administered face-to-face by trained investigators.

Descriptive analyses were computed in terms of means (±standard deviation, sd) for continuous variables and percentages with their 95% confidence intervals (95% CI) for categorical variables. Bivariate analyses between the outcomes (NG, CT, NG/CT, and anorectal NG), and independent variables of interest were performed. Variables with a p <0.20 (Pearson chi-square test) were entered into a multivariate Poisson regression model. The final Poisson multivariate model was based on a backward elimination method and adjusted for potential confounders. The statistical significance level was set at p < 0.05. SAS version 9.4 software (SAS Institute Inc, Cary, NC, USA) was used for the data analysis.

This project was approved by the National Ethics Committee for Health Research of Benin and the Ethics Committee of the CHU de Québec-Université Laval, Canada. Each man willing to participate signed a written free and informed consent form. For those unable to write, a fingerprint was used as a signature mark, in the presence of a witness who validated the appropriateness of the process. No personal information was disclosed. Participants could stop participating at any time during the process. To compensate for the time dedicated to the study, each participant received $8 US. All treatments provided in the context of the study were free of charge (early antiretroviral therapy for men who tested HIV-positive and antibiotics for NG/CT, whether the diagnosis was symptomatic or based on laboratory testing).

Results

A total of 204 MSM initiating PrEP were enrolled in this study. Their mean age was 25.9 ± 4.8 years. Approximately four out of five men were single. Most men (91.7%) reported anal intercourse at least once during the six months that preceded recruitment. Of the 187 participants who reported anal sex in the past six months, 118 (63.1%), 39 (20.9%), and 30 (16.0%) preferred insertive, receptive, and versatile roles, respectively. Consistent condom use was reported in 40.5% of the cases of insertive anal sex versus 32.9% for receptive anal sex (Table 1).

Variables

Number

 %

 95% CI

Socio-demographic characteristics

Age (years) (n=204)

18 - 24

89

43.6

36.8-50.4

25 - 41

115

56.4

49.6-63.2

Occupation (n=204)

Unemployed

14

6.9

3.4-10.3

Occupation with income

137

67.1

60.7-73.6

Students

53

26.0

20.0-32.0

Marital status (n=204)

Married/Cohabiting

34

16.6

11,6-21.8

Single

165

80.9

75.5-86.3

Divorced/Widowed/Separated

5

2.5

3.3-4.6

Level of education (n=204)

Never been in school

1

0.5

0.0-1.5

Primary

14

 6.9

3.4-10.3

Lower secondary

34

16.7

11.6-21.8

Upper secondary

57

27.9

21.8-34.1

Higher education

98

48.0

41.2-54.9

Monthly income in CFA francs * (n=203)

< 40,000

89

43.8

37.0-50.7

40,000-80,000

67

33.0

26.6-39.9

>80,000

47

23.2

17.5-29.6

Living as a couple* (n=201)

Yes

64

31.8

25.5-38.8

No

137

68.2

61.7-74.6

Religion (n=204)

None

8

3.9

1.3-6.6

Traditional

3

 1.5

0.0-3.1

Catholic

128

62.8

56.1-69.4

Other Christian religion

39

19.1

13.7-24.5

Islam

26

12.7

8.2-17.3

Nationality (n=204)

Beninese

195

95.6

92.8-98.4

Other

9

4.4

2.0-8.2

Sexual behaviours with men

Sexual preference* (n=203)

Homosexuality

76

37.5

30.8-44.1

Bisexuality

116

57.1

50.3-64.0

Heterosexuality

11

5.4

2.3-8.5

Sexual activity with men in the past 6 months(n=204)

Anal sex

187

91.7

87.9-95.5

Oral sex

143

70.1

63.8-76.4

Mutual masturbation

118

57.8

51.07-64.6

Anal/oral sex/mutual masturbation

198

97.1

94.7-99.4

Concurrent partners at recruitment (n=204)

Yes (≥ 2)

136

66.7

60.2-73.1

No (0-1)

68

33.3

26.9-39.8

Average number (±sd) of male partners with whom the participant had anal sex (last six months)

2.1± (1.7)

Average number (±sd) of monthly anal sex with males (past six months)

3.1± (2.8)

Insertive anal sex with an HIV-positive partner (past 6 months) (n=187)

Yes

7

3.8

1.0-6.5

No

162

86.6

81.8-91.5

Unknown

18

19.6

5.4-13.8

Type of partner during last insertive anal sex with a man (last 6 months) (n=187)

Occasional

34

18.2

12.7-23.7

Regular

124

66.3

59.4-73.1

No insertive anal sex

29

15.5

10.3-20.7

Condom use during last insertive anal sex with a man (past 6 months) (n=158)

Yes

100

63.3

55.8-70.8

No

58

36.7

29.2-44.7

Frequency of condom use during insertive anal sex (past 6 months (n=158)

Never (0%)

13

8.2

3.9-12.5

Sometimes (1-49%)

53

33.6

26.2-40.9

Often (50-99%)

28

17.7

11.8-23.7

Always (100%)

64

40.5

32.9-48.2

Type of partner during last receptive anal sex with a man (last 6 months) (n=187)

Casual

19

10.2

5.8-14.5

Regular

60

32.1

25.5-39.3

No receptive anal sex

108

57.7

[50.7-64.8

Condom use during last receptive anal sex with a man (past 6 months) (n=79)

Yes

45

57.0

46.0-68.0

No

34

43.0

32.1-54.0

Frequency of condom use during receptive anal sex with men (past 6 months) (n=79)

Never (0%)

8

10.1

3.5-16.8

Sometimes (1-49%)

23

29.1

19.1-40.4

Often (50-99%)

22

27.9

18.0-37.7

Always (100%)

26

32.9

22.7-44.4

Receptive oral sex with men (past 6 months) (n=204)

Never (0%)

118

57.9

51.1-64.6

Less than half the time (1-49%)

57

27.9

21.8-34.1

Half the time or more (50-99%)

29

14.2

9.4-19.0)

Condom use during receptive oral sex with men (past 6 months) (n=86)

Never (0%)

71

82.5

74.5-90.6

Sometimes (1-49%)

9

10.5

4.0-16.9

Often (50-99%)

5

5.8

0.8-10.8

Always (100%)

1

1.2

0.0-3.4

Practice of receptive oral sex (past 6 months) (n=204)

Never (0%)

73

35.8

29.2-42.4

Less than half the time (1-49%)

71

34.8

28.3-41.3

Half the time or more (50-99%)

52

25.5

19.5-31.5

Always (100%)

8

3.9

1.4-6.6

Frequency of condom use during insertive oral sex (past 6 months) (n=131)

Never (0%)

112

85.5

79.5-91.5

Sometimes (1-49%)

9

6.9

2.5-11.2

Often (50-99%)

7

5.3

1.5-9.2

Always (100%)

3

2.3

0.5-6.5

Alcohol use* (past six months) (n=202)

Never

40

19.8

14.3-25.3

95

47.0

40.1-53.9

                         Once-twice a week

38

18.8

13.4-24.2

>Twice a week

29

14.4

9.5-19.2

Marijuana use (past 6 months) (n=204)

Yes

19

9.3

5.3-13.3

No

185

90.7

86.70-94.7

Received money or a gift for sex with a man (past 6 months) (n=204)

Yes

40

19.6

14.2-25.1

No

164

80.4

74.9-85.8

Gave money or a gift for sex (past 6 months) (n=204)

Yes

28

13.7

9.0-18.4

No

176

86.3

81.5-91.0

Sexual behaviours with women

Number of female partners (last 6 months) (n=204)

0

79

38.7

32.0-45.4

1-4

113

55.4

48.6-62.2

>4

12

5.9

2.6-9.1

Condom use during last sexual intercourse with a woman (last 6 months) (n=125)

Yes

64

51.2

42.4-60.0

No

61

48.8

40.0-57.6

Types of female sexual partners (past 6 months) (n=125)

Wife

28

22.4

15.1-29.71

Regular partner

94

75.2

67.6-82.8

Casual partner

53

42.4

33.7-51.1

Sex worker

13

10.4

5.0-15.7

Multiple types of partners

54

43.2

34.5-52.4

Table 1: Characteristics of men who have sex with men initiating HIV pre-exposure prophylaxis in Cotonou, Benin, 2020. Frequency of condom use during receptive anal sex with men (past 6 months) (n=79); MSM, Men who have sex with men; n, Number; GMW, Guaranteed minimum wage: 40,000 CFA francs in 2020 in Benin (US$1 = 500 CFA francs, approximately); SD, Standard deviation; %, Proportion; *Missing values (1, monthly income, sexual preference; 2, alcohol use; 3, living as a couple); †Togo, Nigeria, Ghana, Cameroon; ‡non-mutually exclusive categories

Most men did not receive (80.4%) or give (86.5%) money or gifts in exchange for sex in the six months prior to recruitment. Over three out of five participants reported at least one female partner in the past six months (Table 1). Among the bisexual men, 48.0% had multiple female partners. The proportion of participants with more than three male sexual partners in the last six months was 41.7% among those with more than four female partners, compared with 6.2% among those with one to four female partners, and 21.5% among those without a female partner.

The prevalence of CT and NG at any site were 18.6% (95% CI, 13.3% - 24.0%) and 15.2% (95% CI, 10.3% –20.1%), respectively.

For CT infection, the highest prevalences were observed at the anal (8.8% [95% CI, 4.9% - 12.7%]) and urethral (9.8% [95% CI, 5.7% - 13.9%]) sites. For NG infection, the anal site had the highest prevalence (9.8% [95% CI, 5.7% - 13.9%]), followed by the pharyngeal site (6.4% [95% CI, 3.0% - 9.7%]). The proportion of participants with NG/CT infection was 27.9% (95% CI, 21.8% - 34.1%) for at least one anatomical site and 6.9% (95% CI, 3.4% - 11.3%) for at least two anatomical sites. NG/CT co-infection was observed in 12 of 57 cases (Table 2). For syphilis, only one man had a positive rapid treponemal test followed by a negative Rapid Plasma Reagin test.

Infection

NG/CT

NG

CT

Site

n

%

95% CI

n

%

95% IC

n

%

95% CI

At least one site

57

27.9

21.8-34.1

31

15.2

10.3-20.1

38

18.6

13.3-24.0

Anal

32

15.7

10.7-20.7

20

9.8

5.7-13.9

18

8.8

4.9-12.7

Urethral

22

10.8

6.5-15.0

5

2.5

0.3-4.6

20

9.8

5.7-13.9

Pharyngeal

17

8.3

4.5-12.1

13

6.4

3.0-9.7

5

2.5

0.3-4.6

Two sites*

14

6.9

3.4-11.3

7

3.4

0.9-5.9

5

2.5

0.3- 4.6

Table 2: Prevalence of NG and CT infections among men who have sex with men initiating HIV pre-exposure prophylaxis in Cotonou, Benin, 2020. CT: Chlamydia Trachomatis; CI: Confidence interval; n, Number; NG: Neisseria gonorrhoeae; *multisite localization involved only two sites in this study; %, Proportion

The majority of MSM (90.7%) reported no symptoms of STIs in the four days prior to recruitment. Of the participants with a positive NG test, 80.7% were asymptomatic. This proportion was 84.2% for CT and NG/CT (Table 3).

Modalities

n (%)

Self-reported information (symptom)

In the past six months

                              Burning/irritation of private parts

Yes

35 (17.2)

No

169 (82.8)

Intimate area wounds

Yes

9 (4.4)

No

195 (95.6)

Urethral discharge

Yes

17 (8.3)

No

187 (91.7)

Other symptoms

Yes

14 (6.9)

No

190 (93.1)

In the past four days

                              Burning/irritation of private parts

Yes

14 (40.0)

No

21 (60.0)

Intimate area wounds

Yes

2 (22.2)

No

7 (77.8)

Urethral discharge

Yes

6 (35.3)

No

11 (64.7)

Other symptoms

Yes

3 (21.4)

No

11 (78.6)

                     No symptoms

185 (90.7)

Presence of symptoms (last four days)

NG/CT

  Positive

9 (47.4)

Negative

10 (52.6)

Modalities

n (%)

Urethral discharge/hot urine

NG/CT urethral

 Positive

4 (66.7)

Negative

2 (33.3)

Urethral discharge/hot urine

NG/CT

Positive

5 (83.3)

Negative

1 (16.7)

Burning/irritation of private parts

NG/CT urethral

Positive

5 (35.7)

Negative

9 (64.3)

Physical examination by the physician (clinical sign)

Urethral signs (n=7)

NG/CT

Positive

7 (100.0)

Negative

0 (0.0)

Anal signs (n=8)

NG/CT

Positive

4 (50.0)

Negative

4 (50.0)

Oral signs only (n=4)

NG/CT

Positive

1 (25.0)

Negative

3 (75.0)

Table 3: Distribution of signs and symptoms of sexually transmitted infections among men who have sex with men initiating HIV preexposure prophylaxis in Cotonou, Benin, 2020. †Abscess, pimples, hot urine, flaking testicles, left testicle pain, slight pain, swelling of testicles; n, Number; %, Proportion; ‡Pimples, hot urine

The proportion of positive laboratory tests without any clinical signs of STI based on the physical examination by the study doctor was 74.2%, 73.7% and 75.4% for NG, CT, and NG/CT, respectively. For participants with a positive laboratory diagnosis without symptoms or clinical signs of STI, the proportion was 71.0% for NG and 73.7% for CT and NG/CT. Among positive laboratory diagnosed cases, the proportion of extra-genital STIs (pharyngeal and/or anal sites) was 83.9% for NG, 57.9% for CT and 70.2% for NG/CT.

In bivariate analyses, the sociodemographic variables with a p <0.20 were age, occupation and income for NG; age and marital status for CT; age, occupation, marital status and income for NG/ CT; and age, occupation and income for anorectal NG. Behavioural factors included anal sex, usual sexual role during anal sex with men, concurrent male partners and sex with a man in exchange for money or a gift for NG; number of female partners in the past six months for CT; usual sexual role during anal sex with men and number of female partners in the past six months for NG/CT; and usual sexual role during anal sex with men for anorectal NG. These risk factors were considered in the Poisson multivariate regression model along with potential confounders (Table 4).

Gonorrhea

Chlamydia

Gonorrhea and/or Chlamydia

Anal Gonococcal infection

Positive (%)

Negative

(%)

P-value

Positive

(%)

Negative

(%)

P-value

Positive

(%)

Negative

(%)

P-value

Positive

(%)

Negative

(%)

P-value

Socio-demographic characteristics of participants

Age (years)

18 - 24

21 (23.6)

68 (76.4)

0.0033

22 (24.7)

67 (75.3)

0.0493

34 (38.2)

55 (61.8)

0.0041

16

(18.0)

73 (82.0)

0.0006

25 - 41

10 (8.7)

105

(91.3)

16 (13.9)

99 (86.1)

23 (20.0)

92 (80.0)

4 (3.5)

111 (96.5)

Occupation

Unemployed

5 (35.7)

9 (64.3)

0.0030

1 (7.1)

13 (92.9)

0.2799

6 (42.9)

8 (57.1)

0.0500

4 (28.6)

10 (71.4)

0.0024

Occupation with income

13 (9.5)

124

(90.5)

24 (17.5)

113 (82.5)

31 (22.6)

106 (77.4)

7 (5.1)

130 (94.9)

Students/pupils

13 (24.5)

40 (75.5)

13 (24.5)

40 (75.5)

20 (37.7)

33 (62.3)

9 (17.0)

44 (83.0)

Marital status

Single

25 (15.2)

140

(84.8)

0.9709

28 (17.0)

137 (83.0)

0.2110

43 (26.1)

122 (73.9)

0.2182

17

(10.3)

148 (89.7)

0.7711

Others

6 (15.4)

33 (84.6)

10 (25.6)

29 (74.4)

14 (35.9)

25 (64.1)

3 (7.7)

36 (92.3)

Monthly income in CFA francs *

< 40.000

21 (23.6)

68 (76.4)

0.0129

20 (22.5)

69 (77.5)

0.2391

35 (39.3)

54 (60.7)

0.0063

16

(18.0)

73 (82.0)

0.0019

40,000-80,000

5 (7.5)

62 (92.5)

13 (19.4)

54 (80.6)

14 (20.9)

53 (79.1)

1 (1.5)

66 (98.5)

>80,000

5 (10.6)

42 (89.4)

5 (10.6)

42 (89.4)

8 (17.0)

39 (83.0)

3 (6.4)

44 (93.6)

Sexual behaviour with men

Sexual activity with men in the past 6 months

Anal sex

Yes

31

(16.6)

156

(83.4)

0.0810

34 (18.2)

153 (81.8)

0.5287

53 (28.3)

134 (71.7)

0.7842

20

(10.7)

167 (89.3)

0.3840

No

0 (0.0)

17

(100.0)

4 (23.5)

13 (76.5)

4 (23.5)

13 (76.5)

0 (0.0)

17 (100.0)

Usual sexual role during anal sex with men

Insertive

14 (11.9)

104

(88.1)

0.0066

20 (16.9)

98 (83.1)

0.7200

27 (22.9)

91 (77.1)

0.0442

4 (3.4)

114 (96.6)

<.0001

Receptive

13 (33.3)

26 (66.7)

7 (17.9)

32 (82.1)

17 (43.6)

22 (56.4)

13

(33.3)

26 (66.7)

Versatile

4 (13.3)

26 (86.7)

7 (23.3)

23 (76.7)

9 (30.0)

21 (70.0)

3 (10.0)

27 (90.0)

Concurrent partners at recruitment

Yes

17

(12.5)

119

(87.5)

0.1293

26 (19.1)

110 (80.9)

0.7992

37 (27.2)

99 (72.8)

0.7406

11 (8.1)

125 (91.9)

0.2439

No

14

(20.6)

54 (79.4)

12 (17.6)

56 (82.4)

20 (29.4)

48 (70.6)

9 (13.2)

59 (86.8)

Condom use during anal/oral sex with men in the past 6 months

Never for at least 1 type of sex

21 (16.3)

108

(83.7)

0.5720

27 (20.9)

102 (79.1)

0.2679

40 (31.0)

89 (69.0)

0.2005

14

(10.9)

115 (89.1)

0.5088

Other

10 (13.3)

65 (86.7)

11 (14.7)

64 (85.3)

17 (22.7)

58 (77.3)

6 (8.0)

69 (92.0)

Participant received money or a gift to have sex with a man (last 6 months)

Yes

3 (7.5)

37 (92.5)

0.1305

9 (22.5)

31 (77.5)

0.4829

10 (25.0)

30 (75.0)

0.6438

3 (7.5)

37 (92.5)

0.7704

No

28 (17.1)

136

(82.9)

29 (17.7)

135 (82.3)

47 (28.7)

117 (71.3)

17

(10.4)

147 (89.6)

Sexual behaviour with women

Number of female partners (past 6 months)

0

13 (16.5)

66 (83.5)

0.5179

14 (17.7)

65 (82.3)

0.0152

23 (29.1)

56 (70.9)

0.1724

10

(12.7)

69 (87.3)

0.5517

1-4

15 (13.3)

98 (86.7)

18 (15.9)

95 (84.1)

28 (24.8)

85 (75.2)

9 (8.0)

104 (92.0)

>4

3 (25.0)

9 (75.0)

6 (50.0)

6 (50.0)

6 (50.0)

6 (50.0)

1 (8.3)

11 (91.7)

Type of female partners in the past six months

 Wife/regular partner

10 (14.9)

57 (85.1)

0.9400

10 (14.9)

57 (85.1)

0.3422

18 (26.9)

49 (73.1)

0.8108

6 (9.0)

61 (91.0)

0.7756

 Other

21 (15.3)

116

(84.7)

28 (20.4)

109 (79.6)

39 (28.5)

98 (71.5)

14

(10.2)

123 (89.8)

Table 4: Factors associated in bivariate analyses with NG and CT infections among men who have sex with men initiating HIV pre-exposure prophylaxis in Cotonou, Benin, 2020. CT, Chlamydia Trachomatis; NG, Neisseria gonorrhoeae; %, Proportion; * $1US = 500 CFA francs, approximately.

For the results of multivariate analyses, participants aged 18-24 years were more likely to test positive for NG/CT: adjusted prevalence ratio (aPR); 95% CI=1.80; 1.03- 3.12. MSM who had more than four female partners in the six months prior to recruitment were at higher risk of having NG/CT (aPR 2.30; 95% CI 1.19- 4.43). Participants with higher monthly income had a lower risk of NG/CT (aPR 0.41; 95% CI 0.21- 0.81). Finally, MSM who were not single had a higher risk of having NG/CT (aPR 2.83; 95% CI 1.52- 5.27) (Table 5).

Variables

Modalities

aPR (95% CI)

P-Value

Gonorrhea/Chlamydia1

Age

18-24 years

1.80 (1.03- 3.12)

0.0376

25-41 years

Referent

Marital status

     Single

Referent

     Others

2.83 (1.52- 5.27)

0.0010

Number of female partners (past 6 months)

     0

Referent

      1-4

0.87 (0.47- 1.60)

0.6528

      >4

2.30 (1.19- 4.43)

0.0128

Monthly income in CFA francs *

     < 40,000

Referent

    40,000-80,000

0.58 (0.32- 1.04)

0.0693

      > 80,000

0.41 (0.21- 0.81)

0.0103

Gonorrhea2

Age

18-24 years

2.41 (1.18-4.95)

0.0163

25-41 years

Referent

Participant received money or a gift to have sex with a man (last 6 months)

Yes

0.29 (0.09- 0.94)

0.0384

No

Referent

Usual sexual role during anal sex with men

   Insertive/No anal sex

Referent

    Receptive

2.78 (1.40- 5.51)

0.0034

    Versatile

1.02 (0.34- 3.04)

0.9673

Chlamydia3

Age

18-24 years

2.49 (1.23- 5.06)

0.0115

25-41 years

Referent

Marital status

     Single

Referent

     Others

2.70 (1.32- 5.50)

0.0064

Number of female partners (past 6 months)

     0

Referent

     1-4

1.03 (0.50- 2.11)

0.9388

      >4

2.95 (1.32- 6.59)

0.0082

Anorectal gonococcal infection4

Usual sexual role during anal sex with men

    Insertive/No anal sex

Referent

    Receptive

8.12 (2.82-23.40)

0.0001

    Versatile

2.35 (0.53-10.38)

0.2589

Table 5: Factors associated in multivariate analysis with NG and CT infections among men who have sex with men initiating HIV pre-exposure prophylaxis in Cotonou, Benin, 2020. †Apart from age in model 4, adjustment was made for variables assessed over the last six months; * $1 US = 500 CFA francs, approximately; aPR, adjusted prevalence ratio; CI, Confidence Interval; CT, Chlamydia Trachomatis; NG, Neisseria gonorrhoeae; ‡married, cohabiting, divorced, widowed, or separated.

1: Adjusted for the number of male partners with whom the participant has had anal sex, usual sexual role during anal sex with men, condom use during anal/oral sex with men and type of female partners (exclusively wife and/or regular partner versus other).

2: Adjusted for the number of male partners with whom the participant had anal sex, condom use during anal/oral sex with men, number of female partners, and type of female partners.

3: Adjusted for the number of male partners with whom the participant had anal sex, condom use during anal/oral sex with men, usual sexual role during anal sex with men, and type of female partners

4: Adjusted for age and the number of male partners with whom the participant had anal sex, condom use during anal/oral sex with men, number of female partners, and type of female partners.

Regarding NG, participants younger than 25 were more likely to test positive (p=0.0163). A receptive sexual role was associated with an increased risk of NG (p=0.0034). MSM who received money or a gift to have sex with a man in the past six months had a lower risk of testing positive for NG (p=0.0384) (Table 5).

For CT, there were more cases among MSM under 25 years of age: aPR 2.49; 95% CI: 1.23- 5.06; p=0.0115. Participants who were not single had an increased risk of acquiring CT (aPR 2.70; 95% CI: 1.32- 5.50; p=0.0064). MSM with more than four female partners in the six months prior to recruitment had an elevated risk of CT (aPR 2.95; 95% CI: 1.32- 6.59; p=0.0082) (Table 5). For anal gonococcal infection, only the receptive sexual role was associated with higher risk (aPR 8.12; 95% CI: 2.82-23.40; p=0.0001) (Table 5).

Discussion

The prevalence of CT, NG, and NG/CT infections in all three anatomical sites (anal, urethral and pharyngeal) combined was 18.6% (95% CI, 13.3% - 24.0%), 15.2% (95% CI, 10.3% -20.1%), and 27.9% (95% CI, 21.8% - 34.1%), respectively. These infections were also common in a study of 497 MSM in Abidjan, Bamako, Lomé, and Ouagadougou, with a prevalence of 17.3% for CT and 13.7% for NG [6]. According to the 2020 estimates of the World Health Organization (WHO), the prevalence of NG and CT among adult men in the general population was 1.2% for NG and 4.0% for CT in the WHO African region [1]. Factors such as multiple and concurrent sexual partnerships, and use of psychoactive substances put MSM at high risk of STIs [10]. No active case of syphilis was identified in our study. In a study conducted in Lomé, Abidjan, Bamako, and Ouagadougou, only one case of active syphilis was found, representing a prevalence of 0.2% [11]. This finding suggests a low prevalence of syphilis among HIV-negative MSM in West Africa. The systematic use of antibiotics for genital infections may account for this low prevalence.

In our study, 84.2% of NG/CT cases (80.7% for NG and 84.2% for CT) were asymptomatic. The proportion of asymptomatic NG/CT infections was also high (88.2%) in the study conducted in the four Western African cities [6]. These results suggest that syndromic management, which is the standard treatment for STIs in many resource-limited countries, including Benin, could be ineffective in preventing their transmission among MSM. Hence, whenever possible, laboratory screening should be encouraged in MSM.

The proportion of extra-genital STIs (pharyngeal and/or anal sites) was high: 83.9% for NG, 57.9% for CT and 70.2% for NG/CT. These results are consistent with those of previous studies [6, 12, 13]. In the study conducted in the four Western African cities [6], for example, 77.6% of NG/CT cases were extra-genital. Therefore, a high proportion of STIs could remain undiagnosed if screening is limited to the urethral site in MSM. Extra-genital infections were mostly asymptomatic. To avoid low-noise transmission of these infections, screening should be extended to anal and pharyngeal sites.

Consistent condom use was low. It was 40.5% for insertive anal sex and 32.9% for receptive anal sex. Cheng et al (2014) found comparable results among MSM in Guangzhou, China, with 41.6% consistent condom use during anal sex [14]. Results from a metaanalysis of studies conducted in China showed 47% consistent condom use by MSM during sex with their male partners [15]. In this meta-analysis, condom use was more frequent with nonregular partners compared to regular ones [15]. Given the high prevalence of curable STIs, promotion of regular condom use should be strengthened among MSM. Sixty-one percent of the study participants had at least one female sexual partner in the last six months. Among bisexual men, 48.0% had multiple female partners. Godbole et al (2014) found that 44.0% of MSM had at least one female sexual partner in the last six months in India [16]. In another study from Nigeria, 48.1% of MSM had at least one female sexual partner in the last two months. Among those men who have sex with men and women, 69.0% had multiple female partners [17]. Because of the predominance of asymptomatic NG and CT infections, MSM could contribute to maintaining their transmission within the general population through their female sexual partners [18, 19].

Consistent with our results, Adamson et al (2022) found a higher prevalence of CT and NG/CT infections among MSM under 25 years of age: 24.0% for men under 25 years versus 16.9% for 25-34 years and 15.9% for ≥ 35 years for CT. For NG/CT, this distribution was 30.2%, 24.6%, and 26.2%, respectively [20]. In our adjusted multivariate analyses, young men (<25 years) were at higher risk for NG/CT (aPR; 95% CI: 1.80; 1.03- 3.12), NG (aPR 2.41; 95% CI: 1.18-4.95), and CT (aPR 2.49; 95% CI: 1.23- 5.06) when considering all three anatomic sites (anal, urethral, and pharyngeal). In Nigeria, Kashniro et al (2016) also found that the risk of NG/CT infections decreased with increasing age among MSM [21]. Various biological, cultural, and behavioural factors can explain the vulnerability of younger men to STIs [22]. For example, youth are reluctant to talk openly about their sexual life with health care providers, which may limit their access to health services [23]. They are also reportedly engaged in high-risk STI behaviours such as concurrent sexual partnerships and unprotected sex more often than those who are older [24].

Compared to single MSM, other men were at higher risk of NG/ CT (aPR, 2.83; 95% CI: 1.52- 5.27) and CT (aPR 2.70; 95% CI: 1.32- 5.50). The majority (89.7%) of the participants who were not single have reported at least one female partner in the previous six months compared to 54.5% for single men. The number of female sexual partners was also associated with STIs. Men who reported more than four female partners in the past six months were at higher risk of STIs: NG/CT (aPR 2.30; 95% CI: 1.19- 4.43) and CT (aPR 2.95; 95% CI: 1.32- 6.59). The participants with multiple female partners also had multiple male partners. In the last six months, the proportion of participants with more than three male sexual partners was 41.7% among those with more than four female partners, compared with 6.2% among those with one to four female partners, and 21.5% among those without a female partner, p-value=0.022. These results are consistent with several studies showing that multiple or concurrent sexual partners are a risk factor for STIs [3, 25-27].

More than two out of five men had a monthly income below the state-guaranteed minimum wage of 40,000 CFA francs at the time of the study. An income above 80,000 CFA francs per month was a protective factor against NG/CT infections: aPR 0.41; 95% CI: 0.21- 0.81. Harling et al (2013) found in the United States of America a positive association between low-income individuals and STIs [28]. A low income would limit the choice of sexual partners and the ability to negotiate safe sex (condom use).

A receptive sexual role was associated with NG at the anal site (aPR 8.12; 95% CI: 2.82-23.40) and when all sites were combined (aPR 2.78; 95% CI: 1.40- 5.51). Passaro et al (2018) also found in Lima, Peru, that the receptive sexual role was associated with anorectal NG infection among MSM [29]. Biological factors may explain the high risk of developing NG during receptive anal sex. The rectal mucosa lacks natural lubrification and a protective barrier such as humoral immunity seen in cervico-vaginal secretions in women [30, 31]. Therefore, it is at high risk for lesions, which may facilitate the acquisition of STIs [30].

This first study on the prevalence and factors associated with CT, NG, and TP infections among MSM in Benin has limitations. Because of the face-to-face questionnaire that explored participants’ intimate lives, a social desirability bias was possible. Such a bias could explain why participants who received money/gifts for sex had a lower prevalence of NG: (aPR 0.29; 95% CI: 0.09- 0.94). Indeed, this result is not in line with the literature showing that sex with a paying partner is a risk factor for STIs [32]. Furthermore, all cases of NG observed in participants who received money/gifts for sex occurred among those who reported consistent condom use during paid sex. This suggests that the participants likely provided misinformation about condom use during paid sex. The Poisson multivariate model was adjusted for different potential confounders cited in the literature. However, residual confounding could arise from unmeasured risk factors such as sexual and/or physical abuse. The sample size was limited to 204 participants due to financial constraints. This did not allow us to assess the determinants of NG and CT infections at each anatomic site. Since all participants were affiliated with two identity organizations, some of their characteristics such as exposure to STIs prevention interventions could be different from those of the MSM who did not participate in the study. In addition, as MSM affiliated with identity-based associations are generally more exposed to STIs training and sensitization activities, the generalizability of the results to all MSM in Benin may be limited.

Conclusion

Chlamydia trachomatis and Neisseria gonorrhoeae infections are common among HIV-negative MSM in Benin. They are most often asymptomatic with a high proportion of co-infections and extragenital locations. Prevention programs targeting these infections among men who have sex with men should consider biological screening at urethral, anal, and pharyngeal sites. In addition, they should strengthen preventive interventions for young MSM and extend them to their female sexual partners.

Acknowledgments

We are grateful to The Canadian Institutes of Health Research

(CIHR- FDN-143218) and Plan International Benin (2291/PIB/ CO/PO-BJ06627 and 2508/PIB/CO/PO-BJ06716) for funding the project. Our thanks go also to all participants and all team members in Benin and in Canada.

Authors’ Contributions

MA, SD, LB, FAG, FG and DMZ conceived the study. AD contributed to the supervision of all activities in the field and at the study clinic. EG-M contributed to the lab tests. ON, MO, MA-G, SD, MA and LB contributed to data analyses. The first version of the manuscript was written by ON and revised by SD. All authors read and approved the final version of the manuscript.

Sources of support

The Canadian Institutes of Health Research (CIHR- FDN-143218) and Plan International Benin (2291/PIB/CO/PO-BJ06627 and 2508/PIB/CO/PO-BJ06716).

Conflict of interest

The authors declare no conflict of interest.

References

  1. WHO (2021) Global progress report on HIV, viral hepatitis and sexually transmitted infections: Key data at a glance.
  2. UNAIDS (2022) Global data on HIV epidemiology and response 2022.
  3. Jansen K, Steffen G, Potthoff A, Schuppe AK, Beer D, et al. (2020) STI in times of PrEP: high prevalence of chlamydia, gonorrhea, and mycoplasma at different anatomic sites in men who have sex with men in Germany. BMC Infect Dis 20: 110.
  4. McManus H, Grulich AE, Amin J, Selvey C, Vickers T, et al .(2020) Comparison of Trends in Rates of Sexually Transmitted Infections Before vs After Initiation of HIV Preexposure Prophylaxis Among Men Who Have Sex With Men. JAMA Netw Open 3: e2030806.
  5. Diabaté S, Béhanzin L, Guédou FA, Goma-Matsétsé E, Olodo M, et al. (2023) Pre-exposure prophylaxis in real life: experience from a prospective, observational and demonstration project among men who have sex with men in Benin, West Africa. J Int AIDS Soc 26: e26130.
  6. De Baetselier I, Vuylsteke B, Yaya I, Dagnra A, Diandé S, et al. (2020) To Pool or Not to Pool Samples for Sexually Transmitted Infections Detection in Men Who Have Sex With Men? An Evaluation of a New Pooling Method Using the GeneXpert Instrument in West Africa. Sex Transm Dis. 47: 556-561.
  7. Hessou SPH, Glele-Ahanhanzo Y, Adekpedjou R, Ahoussinou C, Djade CD, et al. (2020) HIV incidence and risk contributing factors among men who have sex with men in Benin: A prospective cohort study. PLoS One. 15 :e0233624.
  8. Abramson JH, Abramson ZH (2008) Rapid Epidemiological Methods. Research Methods in Community Medicine: Wiley Online Library; 313-324.
  9. BeSyP, BeSyP (2017) en Marche: rapport illustré du mapping des hommes qui ont des rapports sexuels avec des hommes au Bénin. Cotonou, Benin: Réseau Bénin Synergie Plus (BeSyP).
  10. Cristaudo A, Giuliani M (2020). Sexually transmitted infections advances in understanding and management. Cham: Springer.
  11. Laurent C, Dembélé Keita B, Yaya I, Le Guicher G, Sagaon-Teyssier L, et al. (2021) HIV pre-exposure prophylaxis for men who have sex with men in west Africa: a multicountry demonstration study. Lancet HIV. 8: e420-e428.
  12. Mimiaga MJ, Mayer KH, Reisner SL, Gonzalez A, Dumas B, et al. (2008) Asymptomatic Gonorrhea and Chlamydial Infections Detected by Nucleic Acid Amplification Tests Among Boston Area Men Who Have Sex With Men. Sex Transm Dis 35: 495-498.
  13. Twahirwa Rwema JO, Herbst S, Hamill MM, Liestman B, Nyombayire J, et al. (2021) Cross-sectional assessment of determinants of STIs among men who have sex with men and transgender women in Kigali, Rwanda. Sex Transm Infect 98: 178-187.
  14. Cheng W, Tang W, Zhong F, Babu GR, Han Z, et al. (2014) Consistently high unprotected anal intercourse (UAI) and factors correlated with UAI among men who have sex with men: implication of a serial cross-sectional study in Guangzhou, China. BMC Infect Dis 14: 696.
  15. Wu J, Hu Y, Jia Y, Su Y, Cui H, et al.(2014) Prevalence of unprotected anal intercourse among men who have sex with men in China: an updated meta-analysis. PLoS One. 9: e98366.
  16. Godbole S, Sane S, Kamble P, Raj Y, Dulhani N, et al. (2014) Predictors of bisexual behaviour among MSM attending intervention sites may help in prevention interventions for this bridge to the heterosexual epidemic in India: Data from HIV sentinel surveillance. PLoS One 9 : e107439.
  17. Sheehy M, Tun W, Vu L, Adebajo S, Obianwu O, et al. (2014) High levels of bisexual behavior and factors associated with bisexual behavior among men having sex with men (MSM) in Nigeria. Aids Care. 26 :116-122.
  18. 18.   Dyer TV, Khan MR, Sandoval M, Acheampong A, Regan R, et al. (2017) Drug Use and Sexual HIV Transmission Risk Among Men Who have Sex with Men and Women (MSMW), Men Who have Sex with Men only (MSMO), and Men Who have Sex with Women Only (MSWO) and the Female Partners of MSMW and MSWO: A Network Perspective. AIDS Behav 21 :3590-3598.
  19. Williamson DA, Chow EPF, Gorrie CL, Seemann T, J Ingle D, et al. (2019) Bridging of Neisseria gonorrhoeae lineages across sexual networks in the HIV pre-exposure prophylaxis era. Nat Commun 10: 3988.
  20. Adamson PC, Bhatia R, Tran KDC, Bui HTM, Vu D, et al. (2022) Prevalence, Anatomic Distribution, and Correlates of Chlamydia trachomatis and Neisseria gonorrhoeae Infections Among a Cohort of Men Who Have Sex With Men in Hanoi, Vietnam. Sex Transm Dis 49: 504-510.
  21. Keshinro B, Crowell TA, Nowak RG, Adebajo S, Peel S, et al. (2016) High prevalence of HIV, chlamydia and gonorrhoea among men who have sex with men and transgender women attending trusted community centres in Abuja and Lagos, Nigeria. J Int AIDS Soc 19: 21270.
  22. CDC (2019) Sexually Transmitted Disease Surveillance.
  23. CDC (2022) Information for Teens and Young Adults: Staying Healthy and Preventing STDs.
  24. Steinberg L (2005) Cognitive and affective development in adolescence. Trends Cogn Sci. 9: 69-74.
  25. Mor Z, Shohat T, Goor Y, Dan M (2012) Risk behaviors and sexually transmitted diseases in gay and heterosexual men attending an STD clinic in Tel Aviv, Israel: a cross-sectional study. Isr Med Assoc J. 14:147-151.
  26. Philipova I, Birindjieva E, Milanov A, Stoitsova S (2022) Prevalence of pharyngeal and rectal chlamydia trachomatis and neisseria gonorrhoeae infections among MSM in Sofia, Bulgaria. Probl Infect Parasit Dis 50: 19-24.
  27. Wati EE, Lubis R, Rochadi RK (2018) The effects of multiple sexual partners and condoms use on the incidence of HIV in men having sex with men. J health promotion behavior 3: 150-154.
  28. Harling G, Subramanian S, Bärnighausen T, Kawachi I, et al. (2013) Socioeconomic disparities in sexually transmitted infections among young adults in the United States: examining the interaction between income and race/ethnicity. Sex Transm Dis 40: 575-581.
  29. Passaro RC, Segura ER, Perez-Brumer A, Cabeza J, Montano SM, et al. (2018) Body Parts Matter: Social, Behavioral, and Biological Considerations for Urethral, Pharyngeal, and Rectal Gonorrhea and Chlamydia Screening Among MSM in Lima, Peru. Sex Transm Dis. 45: 607-614.
  30. Hladik F, McElrath MJ (2008) Setting the stage: host invasion by HIV. Nat Rev Immunol 8: 447-457.
  31. Monin L, Whettlock EM, Male V (2020) Immune responses in the human female reproductive tract. Immunology 160: 106-115.
  32. Solomon MM, Nureña CR, Tanur JM, Montoya O, Grant RM, et al. (2015) Transactional sex and prevalence of STIs: a cross-sectional study of MSM and transwomen screened for an HIV prevention trial. Int J STD AIDS 26: 879-886.

© by the Authors & Gavin Publishers. This is an Open Access Journal Article Published Under Attribution-Share Alike CC BY-SA: Creative Commons Attribution-Share Alike 4.0 International License. With this license, readers can share, distribute, download, even commercially, as long as the original source is properly cited. Read More About Open Access Policy.

Archives of Epidemiology

Update cookies preferences