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PLOS One logoLink to PLOS One
. 2024 Mar 7;19(3):e0295224. doi: 10.1371/journal.pone.0295224

A ‘hidden problem’: Nature, prevalence and factors associated with sexual dysfunction in persons living with HIV/AIDS in Uganda

Brian Byamah Mutamba 1, Godfrey Zari Rukundo 2,*, Wilber Sembajjwe 3, Noeline Nakasujja 4, Harriet Birabwa-Oketcho 1, Richard Stephen Mpango 5,6, Eugene Kinyanda 3,5
Editor: Habil Otanga7
PMCID: PMC10919729  PMID: 38451991

Abstract

Background

We conducted a clinic-based cross-sectional survey among 710 people living with HIV/AIDS in stable ‘sexual’ relationships in central and southwestern Uganda. Although sexual function is rarely discussed due to the private nature of sexual life. Yet, sexual problems may predispose to negative health and social outcomes including marital conflict. Among individuals living with HIV/AIDS, sexual function and dysfunction have hardly been studied especially in sub-Saharan Africa. In this study, we aimed to determine the nature, prevalence and factors associated with sexual dysfunction (SD) among people living with HIV/AIDS (PLWHA) in Uganda.

Methods

We conducted a clinic based cross sectional survey among 710 PLWHA in stable ‘sexual’ relationships in central region and southwestern Uganda. We collected data on socio-demographic characteristics (age, highest educational attainment, religion, food security, employment, income level, marital status and socio-economic status); psychiatric problems (major depressive disorder, suicidality and HIV-related neurocognitive impairment); psychosocial factors (maladaptive coping styles, negative life events, social support, resilience, HIV stigma); and clinical factors (CD4 counts, body weight, height, HIV clinical stage, treatment adherence).

Results

Sexual dysfunction (SD) was more prevalent in women (38.7%) than men (17.6%) and majority (89.3% of men and 66.3% of women) did not seek help for the SD. Among men, being of a religion other than Christianity was significantly associated with SD (OR = 5.30, 95%CI 1.60–17.51, p = 0.006). Among women, older age (> 45 years) (OR = 2.96, 95%CI 1.82–4.79, p<0.01), being widowed (OR = 1.80, 95%CI 1.03–3.12, p = 0.051) or being separated from the spouse (OR = 1.69, 95% CI 1.09–2.59, p = 0.051) were significantly associated with SD.

Depressive symptoms were significantly associated with SD in both men (OR = 0.27, 95%CI 0.74–0.99) and women (OR = 1.61, 95%CI 1.04–2.48, p = 0.032). In women, high CD4 count (OR = 1.42, 95% CI 1–2.01, p = 0.05) was associated with SD.

Conclusion

Sexual dysfunction has considerable prevalence among PLWHA in Uganda. It is associated with socio-demographic, psychiatric and clinical illness factors. To further improve the quality of life of PLWHA, they should be screened for sexual dysfunction as part of routine assessment.

Introduction

Normal sexuality is a psycho-biological activity necessary for psychological and biological balance in most humans, and for the continuation of human life. It involves the feelings of desire, behaviour that brings pleasure to oneself and one’s partner, and stimulation of the primary sex organs, including coitus. The activity should be devoid of inappropriate feelings of guilt or anxiety, and compulsions [1]. Anatomy, physiology, psychology, the culture in which one lives, relationships with others, and the developmental experiences throughout the life cycle determines sexuality. Satisfying sexual life is a key quality of life concern that is rarely inquired into. Although sexual dysfunction is not well studied, according to available literature, it has a global prevalence of about 40–45% among adult women and 20–30% among adult men and the prevalence increases with age [2, 3]. There are four main domains of sexual disorders depending on the affected aspect: desire, arousal, orgasm and pain associated with sex [4]. The most common factors associated with sexual dysfunction differ according to gender but the shared factors include general health status, diabetes mellitus, cardiovascular disease, genitourinary disease, psychological problems and socio‐demographic characteristics [2].

Sexual function in the context of HIV/AIDS has mainly been studied with respect to HIV transmission [5]. From a public health perspective, sexual problems may predispose individuals to unsafe sexual practices as well as intimate partner relationship discord including marital violence, and poor ART adherence. In addition, sexual dysfunction may be a symptom of an undiagnosed mental disorder such as major depressive disorder [6]. Both women and men living with HIV experience common risk factors for sexual dysfunction including poor mental health, hormonal imbalances, pharmacological and other co-morbid conditions and substance abuse [7, 8].

The life-span of people living with HIV/AIDS (PLWHA) has improved significantly due to the availability of highly effective antiretroviral therapy (ART). PLWHA are living longer and healthier lives with less comorbidity due to the availability of effective ART with the majority remaining sexually active for many years. As a result, attention has now shifted to improving quality of life [9]. Previous research in this area has mainly focused on sexual behaviour in the context of assessing HIV transmission risk dynamics, condom use and on the determinants of unintended pregnancy [10–12]. Other aspects of sexual health including sexual dysfunction (SD) and satisfaction with sexual relationships have not been studied as much [13]. Although it was initially thought to be unimportant to this sub-population, the few studies done so far indicate that poor sexual functioning is an important area of concern for PLWHA [14]. According to studies by Rosen [15, 16], sexual dysfunction can be categorised as: i) desire disorders; ii) arousal disorders; iii) orgasm disorders; and iv) pain disorders. Another area of sexual dysfunction is satisfaction with one’s sexual relationship. In this study, we aimed to determine the nature, prevalence and factors associated with SD among PLWHA in Uganda.

Methods

Study design

We conducted a cross sectional survey among 710 PLWHA at HIV clinics run by The AIDS Support Organisation (TASO) in Entebbe (central region) and Masaka (southwestern) in Uganda. The sample consisted of males and females in stable sexual relationships that consented to participate in this sub-study. This sub-study was undertaken as part of Prof Eugene Kinyanda’s Senior EDCTP Fellowship funded study entitled, ‘Clinical trials in HIV/AIDS in Africa: Should they routinely control for mental health factors?’

Study setting

TASO is the oldest indigenous organization that provides HIV/AIDS care and support services in Uganda and Sub-Saharan Africa [17]. It was founded in 1987 and has several branches in many parts of Uganda. TASO offers a comprehensive care package including medical care, psychosocial support, and sensitization about adherence to medication, especially ART. The service of TASO directly complements the efforts of the Ugandan Ministry of Health. Although the TASO centers are located in the district towns, they provide services to clients within a radius of 75 kilometers.

The TASO centre in Masaka was established in 1988 and is located within the Masaka regional referral hospital premises in southwestern Uganda. TASO Masaka serves over 40000 HIV-positive clients, their families and communities. On the other hand, TASO Entebbe commenced work in 1991 and is located within Entebbe Municipal Council in central Uganda. Entebbe being urbanized has an ever-growing and transient population including traders, fish mongers, and uniformed personnel. It is the first and last stop for international tourists. TASO Entebbe serves 7000 clients, their families and surrounding communities.

Sampling and sample size

This was a cross-sectional study that was part of a prospective cohort of HIV positive adults attending at 2 specialized HIV clinics run by The AIDS Support Organization (TASO) in Uganda: TASO HIV clinic in Masaka and Entebbe (rural and semi-urban). The study enrolled a sample of 710 ART naı’ve HIV positive adults. Initiation of ART was implemented by TASO independently of the study. At the time of the study, national treatment guidelines for HIV-infected individuals recommended the initiation of ART at a CD4 cell count of below 250 cells/mL. In addition, individuals initiating ART were required to have identified an appropriate treatment supporter.

Eligibility criteria

Inclusion criteria. i) A person who was living with HIV (PLWH) who was ART naïve and registered with the outpatient clinic at either TASO Entebbe and TASO Masaka clinics; ii) was an adult at the time of enrolment (at least 18 years old); iii) was conversant with English or Luganda, the language into which the research protocols were translated; iv) gave informed consent after adequate explanation of the study objectives, procedures and expected benefits. Exclusion criteria. i) was too sick (those patients who came to the HIV clinics with severe physical health problems and were unwell and needed emergency assessment and hospitalization)] and ii) unable to understand the study instruments.

Study variables

A range of explanatory variables that included socio-demographic, psychiatric illness and clinical factors were assessed. The socio-demographic factors included age, highest educational attainment, religion, food security, employment, income level, marital status and socio-economic status (assessed using an index constructed from having common household items and facilities such as electricity, a car, a radio, a bicycle, a telephone, a refrigerator, a lantern and a flask) [18]. Two categories of low and high socio-economic status were generated using principal component analysis. The psychiatric illness factors included major depressive disorder and suicidality (assessed using the Mini International Neuropsychiatric interview (M.I.N.I. Plus) [19]; severity of depressive symptoms was assessed using the Centre for Epidemiological Studies-Depression questionnaire (CES-D) [20]. Psychosocial factors assessed included: Maladaptive Coping Style (MCS) (assessed using the Carver Brief COPE (Coping Orientation to Problems Experienced Inventory) [21], negative life events (assessed using the adverse life events module of the European Parasuicide Interview Schedule modified for the Ugandan situation [22], Social support (assessed using the Multidimensional Scale of Perceived Social Support (MSPSS) [23], resilience (assessed using the Connor-Davidson Resilience Scale (CD-RISC) [24] and HIV stigma (assessed using the brief HIV Stigma Scale) [25]. Clinical factors assessed included: CD4 nadir, CD4 counts in the last 6 months, body weight, height and HIV clinical stage (assessed using the WHO clinical staging criteria [26] and treatment adherence.

Sexual behaviour differs between males and females and hence two different instruments were used to assess for the dependent variable of sexual dysfunction. Among males, SD was assessed using the IIEF [27]. The IIEF is a 15-item

questionnaire that was developed by Rosen and colleagues (1997) for use in heterosexual men to assess five domains of male sexual function, including: desire (items 11 and 12), erectile function (items 1–5 and 15), orgasmic function (items 9 and 10), intercourse satisfaction (items 6, 7 and 8) and overall satisfaction (items 13 and 14) [25]. It has questions such as, ‘How often were you able to get an erection during sexual activity?’ Responses are scored on a 6-point Likert scale with items: 0 = No sexual activity; 1 = Almost never or never; 2 = A few times (less than half the time); 3 = Sometimes (about half the time); 4 = Most times (more than half the times); 5 = Almost always or always. It has been linguistically validated in 32 languages including in South African dialects [27]. In this study responses were restricted to the period covering the last 4 weeks.

The primary outcome measure for sexual dysfunction among men was erectile dysfunction (defined as a cut-off score of 25 or less on the erectile function domain of the IIEF for a man in a stable relationship) [27]. The other 4 domains of the IIEF and the total score on the IIEF were considered as secondary outcomes among men in this study.

Sexual dysfunction in women was assessed using the FSFI a tool that was developed by Rosen and colleagues]. The FSFI is a 19-item questionnaire which among western respondents has been found to consist of 6 domains, namely: desire (items 1 and 2), subjective arousal (items 3–6), lubrication (items 7–9), orgasm (items 11–13), global satisfaction (items 14–16) and pain (items 17–19) [28]. It consists of question items such as, ‘Over the past 4 weeks, how often did you feel sexual desire or interest?’. Responses are scored on a 5-point Likert scale with items: 1 = Almost never or never; 2 = A few times (less than half the time); 3 = Sometimes (about half the time); 4 = Most times (more than half the times); 5 = Almost always or always. In this study responses were restricted to the period covering the last 4 weeks (last month). The primary outcome measure for sexual dysfunction among women was the total FSFI score (where a cut-off score of 26.55 or less is regarded as suggestive of sexual dysfunction) [29]. Weigel and colleagues in cross-validation studies of the FSFI have recommended a total cut-off score of 26.55 for differentiating females with or without sexual dysfunction [29].

Since both the IIEF and the FSFI were used in this socio-cultural setting for the first time, they were taken through a local translation process from English to Luganda (the predominant language spoken in central and south-western region) and subsequent determination of their internal consistency (assessed using the Cronbach’s alpha). The local translation process involved forward and back translation of each of these instruments by two independent teams of mental health professionals. The teams selected to undertake this process were conversant with both English and Luganda. The teams then met for a consensus meeting in which the final back-translated English version was compared to the initial English version to assess for consistency. A consensus meeting was then held to address those items where there were wide variations in the two English versions. In this study, the internal consistency of the IIEF was 0.96 and that of the FSFI was 0.97 (a value greater than 0.70 is considered adequate). Trained study psychiatric nurses administered the study tools to the study participants.

Statistical analysis

Statistical analyses were conducted using Stata release 15 (Stata Corp, TX, USA). Analyses were carried out separately for males and females. Frequencies to the FSFI and IIEF were estimated with their percentages. Categorical variables were described using frequencies and percentages while continuous variables were described using median (IQR). Health seeking behaviour of the respondents was also described using frequencies and percentages. Two binary outcome variables “sexual dysfunction for men and sexual dysfunction for women” were generated. To investigate the association of sexual dysfunction with socio-demographic and psychosocial and psychiatric illness factors, a two-step procedure was adopted. social economic status was categorized into categories from a list of household items using Principal Component Analysis. During the first step, bivariate associations between each of the outcome variables and the independent variables were assessed using simple logistic regression models.

In the second step, those socio-demographic, psychosocial and psychiatric illness factors that attained a level of significance of P ≤ 0.2 (liberal cut-off point) with bivariate analyses were included in the final multivariate logistic regression models that assessed for the factors that were independently significantly associated with sexual dysfunction. We were not able to conduct subgroup analyses by homo- and heterosexual respondents. Education was categorized as no formal education, primary, secondary and tertiary. Religion was also categorised into 2 categories i.e. ‘christian’ and ‘muslim & others’. All analyses adjusted for age.

Results

Participant characteristics

A total of 159 men and 551 women participated in the study. The small number of men in the study could have affected the results. The majority of the participants were married and they belonged to the Christian faith (Table 1). The respondents were females and the age of the participants ranged between the age 18 and 65 years.

Table 1. Characteristics of study participants on key socio-demographic variables (should not include analyses of associated factors).

Variable Level Women N = 551(%) Men N = 159(%)
Highest education attained No formal education 69(12.5) 30(18.9)
Primary 328(59.5) 80(50.3)
Secondary 139(25.2) 20(12.6
Tertiary 14(2.5) 28(17.6)
Religion Christians 469(85.1) 146(91.8)
Muslims & others 82(14.9) 13(8.2)
Age Median (IQR) 33(20; 57) 35 (21; 57)
Food security status Yes 445(80.8) 133(83.6)
No 104(18.9) 26(16.4)
Employment status Farmer 159(28.9) 50(31.4)
Professionals 16(2.9) 12(7.5)
Self-employed/Business 202(36.7) 48(30.2)
Unemployed 163(29.6) 32(20.1)
Socio economic status (SES) Low SES 228(41.4) 36(22.6)
High SES 321(58.3) 123(77.4)
Marital status Currently married 273(49.5) 102(64.1)
Widowed 90(16.3) 10(6.3)
Separated 137(24.9) 30(18.9)
Single 50(9.1) 17(10.7)

Nature and prevalence of sexual dysfunction

Low sexual desire, reduced levels of sexual arousal, not reaching orgasm and experiencing pain or discomfort were the prevalent problems among women. A considerable number of women (≥35%) did not engage in sexual activity in the previous month compared to men (< 20%). Among men; low levels of sexual desire and number of times sexual intercourse was attempted were the prevalent problems. The number of times sexual intercourse was attempted was measured as” no attempts, one to two attempts/ three to four attempts, five to six attempts, seven to ten attempts/ Eleven or more attempts”. In this case, fewer sexual attempts were assumed to indicate lower sex drive and, therefore sexual dysfunction.

Overall, the prevalence of sexual dysfunction was 17.6% (15.1 to 19.1) and 38.7% (35.9 to 40.1) in men and women respectively, indicating that in PLWHA, women are more affected than men. The majority of both men (89.3%) and women (66.3%) did not seek help for sexual dysfunction, but more women (25%) sought help from a health worker compared to men (7.1%)). Of note, 3.4% and 6.6% of women sought help from a traditional or faith healer respectively compared to 0% and 3.6% in men (Tables 2 and 3).

Table 2. Prevalence of sexual dysfunctions among women living with HIV/AIDS in Uganda.

Disorder Level Frequencies n (%)
Over the last four weeks
Sexual Desire problems
How often did you feel sexual desire or interest? (n = 551) Almost never or never 147(26.7)
How would you rate your level (degree) of sexual desire or interest?
(n = 548)
Very low or none at all 135(24.5)
Sexual Desire problems (at least one positive item from items 1 to 2)
N = 551
Positive 176(31.9%)
Number of Female that are sexually active*N = 551 Yes 345(62.6%)
Sexual Arousal problems* n = 345
How often did you feel aroused (“turned on”) during sexual activity or intercourse? Almost never or never 48(13.9%)
How would you rate your level of sexual arousal (“turn on”) during sexual activity or intercourse? Very low or none at all 41(11.9%)
How confident were you about becoming sexually aroused during sexual activity or intercourse? Very low or no confidence 45(13.0%)
How often have you been satisfied with your arousal (excitement) during sexual activity or intercourse? Almost never or never 26(7.5%)
Sexual Arousal problems* (at least one positive item from items 3 to 6) Positive 99(28.7%)
Sexual Lubrication problems* n = 345
How often have you become lubricated (“wet”) during sexual activity or intercourse? Almost never or never 26(7.5%)
How difficult was it to become lubricated (“wet”) during sexual activity or intercourse? Extremely /very difficult or impossible 31(8.9%)
How often did you maintain your lubrication (“wetness”) until completion sexual activity or intercourse Almost never or never 22(6.4%)
How difficult was it to maintain your lubrication (“wetness”) until completion sexual activity or intercourse Extremely /very difficult or impossible 28(8.1%)
Sexual Lubrication problems* (at least one positive item from items 7 to 10) Positive 45(13.0%)
Orgasm problems* n = 345
When you had sexual stimulation or intercourse How often did you reach orgasm (climax)? Almost never or never 46(13.3%)
When you had sexual stimulation or intercourse how difficult was it for you to reach orgasm (climax)? Extremely /very difficult or impossible 45(13.0%)
How satisfied were you with your ability to reach (climax) orgasm during sexual activity or intercourse? Moderately and Very dissatisfied 100(28.9%)
Orgasm problems* (at least one positive item from items 11 to 13) Positive 115(33.3%)
Sexual Pain problems* n = 345
How often did you experience discomfort or pain following vaginal penetration? Almost always or Most times 105(30.4%)
How often did you experience discomfort or pain during vaginal penetration Almost always or Most times 37(10.7%)
How would you rate your level (degree) of discomfort or pain during vaginal penetration? High 36(10.4%)
Sexual Pain problems* (at least one positive item from items 14 to 16)* Positive 139(40.3%)
Sexual dysfunction (at least one positive item from item 1 to 13 and then 17 to 19) Positive 348(63.2%)
Dissatisfaction with sexual experience with current partner** n = 551
How satisfied have you been with the amount of emotional closeness during sexual activity or intercourse between you and your partner? Moderately and Very dissatisfied 78(14.2%)
How satisfied have you been with sexual relationship with your partner? Moderately and Very dissatisfied 193(35.0%)
How satisfied have you been with your overall sexual life? Moderately and Very dissatisfied 192(34.8%)
Dissatisfaction with sexual experience with current partner (at least one positive from items 14 and 15) Positive 214(38.8%)

Note *Percentage among sexually active

**Percentage among those in an intimate partner relationship

Table 3. Prevalence of sexual dysfunctions among men living with HIV/AIDS in Uganda.

Disorder Level Frequencies (%)
Over the last four weeks …….
Sexual Desire problems n = 157
How often have you felt sexual desire? Almost never/ A few times 54(34.4%)
How would you rate your level of sexual desire? Very low/ Low 39(24.8%)
Sexual Desire problems (at least one positive item from items 11 to 12) Positive 62(39.5%)
Number of Male that are sexually active Yes 139(88.5%)
Sexual Arousal problems* n = 139
How often were you able to get an erection during sexual activity Almost never/ a few times 39(28.1%)
When you had erections with sexual stimulation, how often were your erections hard enough for penetration? Almost never/ A few times 37(26.6%)
When you attempted intercourse, how often were you bale to penetrate (enter) your partner? Almost never/ A few times 30(21.6%)
During sexual intercourse, how often were you able to maintain your erection after you had penetrated (entered) your partner? Almost never/ A few times 33(23.7%)
During sexual intercourse, how difficult was it to maintain your erection to completion of intercourse? Extremely difficult/ Very difficult 5(3.6%)
How do you rate your confidence that you could get and keep an erection? Very Low/ Low 33(23.7%)
Sexual Arousal problems (at least one positive item from items 1 to 5 and item 15) Positive 84(60.4%)
Ejaculation problems
When you had sexual stimulation or intercourse, how often did you ejaculate? Almost never/ A few times 16(11.5%)
When you had sexual stimulation or intercourse, how often did you have the feeling of orgasm or climax? Almost never/ A few times 42(30.2%)
Ejaculation problems (at least one positive item from items 9 to 10) Positive 49(35.2%)
Sexual dysfunction (at least one positive item from items: 11,12, 1 to 5, 15, 9,10) Positive 102(73.4%)
Dissatisfaction with Sexual experience
When you attempted sexual intercourse, how often was it satisfactory for you? Almost never/ A few times 18(12.9%)
How much have you enjoyed sexual intercourse? No enjoyment at all/ Not very enjoyable 9(6.5%)
How satisfied have you been with your overall sex life? Very dissatisfied/ Moderately dissatisfied 35(25.2%)
How satisfied have you been with your sexual relationship with your partner? Very dissatisfied/ Moderately dissatisfied 30(21.6%)
Dissatisfaction with Sexual experience (at least one positive item from items 7,8,13,14) Positive 36.7%

Note *Percentage among sexually active

Some of the factors met the apriori cut-off and were statistically significant at bivariate analysis (Table 4). However, they presented multicollinearity in the multivariate model and therefore reducing precision of the estimates and were therefore eliminated.

Table 4. Factors associated to sexual dysfunction at Bivariate (unadjusted) analysis).

Variable Level Women Crude odds ratio (95% CI) Men Crude odds ratio (95% CI)
Highest education attained P = 0.422 P = 0.819
No formal education 1 1
Primary 0.83(0.49–1.41) 0.90(0.37–2.21)
Secondary 0.66(0.38–1.20) 0.36(0.18–1.20)
Tertiary 1.3(0.41–4.11) 1.3(0.41–4.11)
Age P<0.001 P<0.001
18–44 years 1 1
45 years and above 2.96(1.82–4.79) 3.96(1.02–6.31)
Religion P = 0.194 P = 0.009
Christians 1 1
Muslims & Others 1.37(0.85–2.20) 4.83(1.48–15.74)
Food security status P = 0.450 P = 0.74
Yes 1.18(0.76–1.85) 1.21(0.38–3.84)
No 1 1
Employment status P = 0.03 P = 0.66
Farmer 1 1
Professionals 0.96(0.34–2.72) 1.05(0.19–5.72)
Self-employed/Business 0.86(0.57–1.32) 1.56(0.57–4.30)
Unemployed 0.52(0.33–0.82) 0.75(0.2–2.73)
Socio economic status P = 0.157 P = 0.409
Low ses 1 1
High ses 0.78(0.55–1.10) 0.68(0.27–1.71)
Marital status P<0.001 P = 0.70
Currently married 1 1
Widowed 2.64(1.62–4.30) 0.52(0.62–4.35)
Separated 1.78(1.16–2.71) 1.42(0.52–3.81)
Single 1.14(0.60–2.16) 0.62(0.13–3.0)
Major Depressive disorder P = 0.033 P = 0.81
Yes 1.59(1.03–2.43) 1.14(0.39–3.3)
no 1 1
Suicidality P = 0.902 P = 0.481
Yes 1.04(0.57–1.90) 0.50(0.06–4.1)
no 1 1
Severity of depressive symptoms P = 0.151 P = 0.073
0 symptoms 1 1
1–10 symptoms 0.66(0.39–1.10) 0.31(0.11–0.86)
11–20 symptoms 0.57(0.32–1.01) 0.28(0.78–1.02)
Negative life events P = 0.412 P = 0.368
0–5 events 1 1
6–10 events 0.78(0.53–1.15) 0.68(0.24–1.97)
11–17 events 0.81(0.43–1.51) 2.06(0.57–7.39)
Social support P = 0.406 P = 0.019
Yes 1 1
No 1.18(0.79–1.76) 0.35(0.15–0.83)
HIV neurocognitive impairment P = 0.503 -
Have dementia 1.15(0.76–1.73)
No dementia 1
weight P = 0.386 P = 0.913
> = 61 kgs 1 1
30–60 kgs 0.86(0.60–1.22) 0.94(0.40–2.22)
CD4 count P = 0.025 P = 0.368
<500 1 1
> = 500 1.48(1.05–2.09) 0.65(0.26–1.67)
Adherence to HIV medication P = 0.783 P = 0.234
Yes 1.06(0.69–1.62) 1.23(0.42; 1.49)
No 1 1
Risky sexual behaviour P = 0.732 P = 0.433
Yes 0.91(0.54–1.54) 0.98(0.76; 1.97)
No 1 1
Diabetes P = 0.294 P = 0.043
Yes 2.4(0.39–14.5) 1.99(1.01; 2.13)
No 1 1
stroke P = 0.001 P = 0.002
Yes 2.19(1.15–6.43) 1.94(1.01; 5.21)
No 1 1

* HIV neurocognitive impairment among men was not included due to perfect collinearity.

Factors associated with sexual dysfunction

With respect to women; age was significantly associated with sexual dysfunction, with women aged 45 years and above almost three times more likely to have the problem. A marital status indicated as widowed or separated was a risk factor for SD in women (Table 5). Employment status was found to be associated with sexual dysfunction. Major depressive disorder was the only psychological/social factor significantly associated with sexual dysfunction (1.61 (1.04–2.48), p = 0.032) in women. With respect to HIV-related factors, a high CD4 count (≥ 500) was the only one with a statistically significant association to sexual dysfunction (1.42 (1–2.01; p = 0.05) (Table 5). Stroke was also found highly associated with sexual dysfunction.

Table 5. Factors associated with sexual dysfunction (Multivariate model).

Factor Level Women aOR (95%CI) Men aOR (95%CI)
Age P<0.001 * P<0.001 *
18–44 years 1 1
45 years and above 2.92(1.78–4.79) 3.90(1.02–6.01)
Religion P = 0.194 P = 0.009 *
Christians 1 1
Muslims & Others 1.40(0.85–2.20) 4.83(1.50–15.74)
Employment status P = 0.030 * P = 0.461
Farmer 1 1
Professionals 0.96(0.34–2.72) 1.05(0.19–5.72)
Self-employed/Business 0.86(0.57–1.32) 1.56(0.57–4.30)
Unemployed 0.52(0.33–0.82) 0.75(0.2–2.73)
Marital status P<0.001 * P = 0.120
Currently married 1 1
Widowed 2.64(1.62–4.30) 0.52(0.62–4.35)
Separated 1.78(1.16–2.71) 1.42(0.52–3.81)
Single 1.14(0.60–2.16) 0.62(0.13–3.0)
Major Depressive disorder P = 0.032 * -
Yes 1.61 (1.04–2.48)
no 1
Severity of depressive symptoms - P = 0.050
0 symptoms 1
1–10 symptoms 0.29(0.10–0.83)
11–20 symptoms 0.27(0.74–0.99)
CD4 count P = 0.05 -
<500 1
> = 500 1.42(1–2.01)
Stroke P = 0.016 * P = 0.023 *
Yes 2.89(1.95–8.81) 2.54(1.03; 6.61)
No 1 1
Social support - P = 0.065
Yes 1
No 0.37(0.15–0.89)

*Significant at 5% level of significance

With respect to men, religion (being Muslim or other faith) and age were the only socio-demographic factors significantly associated with erectile dysfunction. Severity of depressive symptoms was the only psychological and social factor significantly associated with ED. Stroke was also found highly associated with erectile dysfunction.

No HIV-related or anthropometric factors were significantly associated with ED.

Discussion

We sought to explore the topic of sexual functioning among patients living with HIV in Uganda, a rather taboo topic in this setting, with an aim of informing quality of care initiatives. SD is a relatively common problem experienced by men and women living with HIV in Uganda, with one in five men and two in five women affected. Studies on SD in PLWHA in similar contexts is scarce, however some of our findings compare with those in the extant literature. It is worth noting that for both men and women with SD, majority did not seek treatment. This was especially so for men, with less than 1 in 10 seeking any form of help. Understanding why women seek help from alternate care providers (traditional and faith healers), and what help is received is an area for further inquiry.

Nature and prevalence of dysfunction among PLWHA

We found that SD was more prevalent in women (38.7%) compared to men (17.6%). However, there was disproportionate representation of women in the sample. It is possible that this could have led to the difference in the burden of SD. Our findings are similar to what has been reported in previous studies [30–33] which have also found high prevalence of sexual dysfunction among women than in men. Unfortunately, SD is a burden that is rarely discussed in clinical encounters and therefore often goes unattended. According to our study findings, 89.3% of men and 66.3% of women did not seek help for the dysfunction. This finding is similar to what has been reported in previous studies which found that the healthcare system may not be prepared for the immediate and continuing support for sexual complaints [34–37].

Factors associated with SD in HIV-infected men

Poor erectile function is thought to be due to HIV associated co-morbid physical conditions particularly when it manifests among HIV-infected men without AIDS [5, 38]. This is not consistent with our findings that no HIV-related physical or anthropometric factors were associated with SD. Studies from elsewhere have identified a range of physical factors associated with SD in men; hypogonadism and low serum testosterone levels were the more commonly reported factors [8, 39]. Other physical conditions that have been reported to be associated with SD in HIV-infected individuals include hepatopathy, diabetes mellitus, hyperlipidaemia, hypertension, vascular disease, and alcohol dependence [38, 40]. Similar to previous studies, in our study, the physical conditions were significantly associated with SD in men were stroke and diabetes. The two disease conditions have known vascular complications that often cause sexual dysfunction. However, the number of men was smaller than that of women in this study. This could have affected the results.

Psychological or mental health factors are thought to play a major role in sexual dysfunction. Feelings of guilt from having acquired HIV via sexual transmission has been reported to negatively influence sexual response in men [40]. This may explain the significant association between religion and SD in men. However, this has not been documented elsewhere. In keeping with the evidence, severity of depression was associated with SD in men. Depression and anxiety are some of the most important mental health factors associated with sexual dysfunctions [8, 39]. In a study of men infected with HIV, those who reported SD had significantly higher scores of psychological symptoms although it was not clear whether the psychological symptoms were a cause or an effect of altered sexual function [39, 41].

Sexual function can negatively be impacted by the effects of HIV treatment [42]. In one study by Lallemand and colleagues (2002), SD was found to be prevalent in HIV-infected men receiving ART irrespective of whether the treatment regimen contained protease inhibitors (PIs) or not. In that study the most prevalent forms of SD were loss of libido, erectile dysfunction and orgasmic disorders [14]. Though low level of sexual desire was one of two prevalent problems among men in our study, it was not found to be associated with ART adherence. A number of studies on the other hand have reported that SD is more common in people taking Protease Inhibitors [38, 43–45]. Other non-antiretroviral factors that have been associated with SD in HIV-infected men include age, sexual preference, duration of HIV infection, CD4 T-cell nadir and the occurrence of opportunistic infection [46].

Factors associated with SD in HIV-infected women

Our study found a prevalence of FSD (38.7%) which is comparable to 32% in a study conducted among HIV-positive women on ART in Italy [47] but much lower than a prevalence of 61% among HIV-positive women in Nigeria [48]. These are higher than the prevalence of 25% found in study of HIV-positive women in Europe [49] indicating the wide-ranging variability in the prevalence of FSD among HIV-positive women across the globe. This could be as a result of contextual and cultural factors related to experience and disclosure about SD [48].

Wilson and colleagues reported a higher burden of sexual problems among HIV-positive women compared to HIV negative women, indicating a clear link between HIV infection and sexual problems [13]. In our study, a number of sexual problems, relating to reduced desire for and difficulties during sexual activity, were experienced by women. These findings are similar to findings in HIV-positive women in Nigeria [50]. Reduced sexual desire in women after testing positive for HIV has been reported to be associated with fear of HIV transmission, depression, stress and interpersonal problems [51]. Concerns about HIV transmission, HIV treatment including ART and its side effects may have deleterious effects on female sexual functioning as is the use of alcohol and street drugs [7, 51]. This could be a possible explanation why one in three women who participated in the study did not engage in sexual activity in the month prior.

We found that older age (>45 years) and being widowed or separated were associated with an increased risk of FSD. Oyedokun and others found no association between FSD and religion among HIV-positive women in Nigeria, however, increasing age [47], was significantly associated with FSD [52]. These findings are corroborated in our study. It has been observed that self-perceived body image is a major determinant of FSD [52] and one can argue that increasing or an older age is a contributory factor. Unlike in their study, we did not find education level to be significantly associated with FSD [52].

Consistent with our findings where we did not find any significant association between FSD and ART, most studies that have explored the association between ART and female sexual functioning have not shown any significant association [52–54]. Comparisons of HIV-positive women who were ART naïve and those who had been treated found no difference in sexual functioning [53]. In another study HIV-positive women described diminished sexual activity, a loss of sexual interest and decreased feelings of attractiveness, both before and after the advent of ART [55].

Similar to our findings that CD4 cell count was the only HIV-related factor significantly associated with FSD, a study by Wilson and others (2010) also showed that those with CD4 count of ≤199 cells/mm3 had more impaired sexual functioning as assessed by the female sexual function index (FSFI) as compared with those with CD4 counts of 200 cells/mm3 or higher [13]. This was also similar to findings by Oyedokun and others in their study on HIV-positive women in Nigeria [47]. It is possible that that when an individual has low CD4 count they may be more focused on their other physical health problems, with less interest in sex.

Psychosocial variables such as mental health status, quality of life, but not clinical status (illness stage), have been reported to be the main determinants of sexual impairment among HIV-positive women [54, 56]. Depression was the only psychosocial factor associated with FSD in our study, a finding similar to that in other studies of FSD in HIV-positive women in which psychological distress was a significant risk factor for FSD [52, 53]. In another study, women with greater depressive symptoms and greater intrusive thoughts reported poorer sexual quality-of-life with depressive symptoms mediating the association between intrusive thoughts and lower sexual quality-of-life [57]. On the other hand, according to our data and previous studies, age is also associated with sexual dysfunction among men.

Limitations

This was a cross-sectional study thus it was difficult to establish the direction of causality. We did not study SD in non-HIV-positive men and women and are therefore not able to compare our findings with this population to further understand the role of HIV in SD. In addition, we did we have a qualitative component to further understand sexual behavior and experiences of the respondents. We were not able to conduct subgroup analyses by homo- and heterosexual respondents. There could have been differences according to sexual orientation.

Conclusion and recommendations

SD is prevalent among PLWHA in Uganda and it is associated with socio-demographic, psychiatric and clinical illness factors. Underreporting and Lack of Seeking Help: A significant percentage of individuals experiencing SD did not seek help for their condition. This underscores the need for increased awareness and open discussions about SD in clinical encounters, as well as improved support systems for those affected.

Factors Associated with SD: Among HIV-infected men, no HIV-related physical or anthropometric factors were associated with SD. However, stroke and diabetes showed a significant association. In contrast, psychological factors, such as religion and severity of depression, played a role in SD among men. For women, older age (>45 years) and being widowed or separated were associated with an increased risk of female sexual dysfunction (FSD). CD4 cell count was the only HIV-related factor significantly associated with FSD. Depression emerged as a significant psychosocial factor linked to FSD.

Routine assessments and targeted, culturally appropriate interventions for SD should be provided as part of the integrated mental health services in HIV care.

Implications to LMIC

LMICs can benefit from raising awareness about sexual dysfunction among people living with HIV/AIDS (PLWHA). Health authorities and organizations should prioritize educational campaigns aimed at healthcare providers, PLWHA, and the general population to reduce stigma and encourage open discussions about sexual health.

Abbreviations

FSD

Female sexual disorder

LMICs

Low- and Middle-Income Countries

MSD

Male sexual disorder

PLWHA

People living with HIV/AIDS

SD

Sexual dysfunction

WHO

World Health Organization

Data Availability

All relevant data are within the paper.

Funding Statement

This study was funded by MRC TA.10.40200.011 core funding to the Mental health project of MRC/UVRI and LSHTM under the headship of Professor Eugene Kinyanda to undertake the ‘HIV clinical trials preparedness studies among patients with Severe Mental ILlnEss in HIV endemic Uganda (SMILE Study) The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.

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Decision Letter 0

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9 Nov 2022

PONE-D-22-24725A ‘hidden problem’: Nature, prevalence and factors associated with sexual dysfunction in persons living with HIV/AIDS in UgandaPLOS ONE

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Reviewers' comments:

Reviewer's Responses to Questions

Comments to the Author

1. Is the manuscript technically sound, and do the data support the conclusions?

The manuscript must describe a technically sound piece of scientific research with data that supports the conclusions. Experiments must have been conducted rigorously, with appropriate controls, replication, and sample sizes. The conclusions must be drawn appropriately based on the data presented.

Reviewer #1: Partly

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2. Has the statistical analysis been performed appropriately and rigorously?

Reviewer #1: I Don't Know

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3. Have the authors made all data underlying the findings in their manuscript fully available?

The PLOS Data policy requires authors to make all data underlying the findings described in their manuscript fully available without restriction, with rare exception (please refer to the Data Availability Statement in the manuscript PDF file). The data should be provided as part of the manuscript or its supporting information, or deposited to a public repository. For example, in addition to summary statistics, the data points behind means, medians and variance measures should be available. If there are restrictions on publicly sharing data—e.g. participant privacy or use of data from a third party—those must be specified.

Reviewer #1: Yes

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4. Is the manuscript presented in an intelligible fashion and written in standard English?

PLOS ONE does not copyedit accepted manuscripts, so the language in submitted articles must be clear, correct, and unambiguous. Any typographical or grammatical errors should be corrected at revision, so please note any specific errors here.

Reviewer #1: No

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5. Review Comments to the Author

Please use the space provided to explain your answers to the questions above. You may also include additional comments for the author, including concerns about dual publication, research ethics, or publication ethics. (Please upload your review as an attachment if it exceeds 20,000 characters)

Reviewer #1: Dear authors, I am providing specific comments in the assigned space, but I am also attaching these in a PDF file, should these be easier to work with.

General

Abstract, sentence starting with ‘Among individuals living with HIV/AIDS…’: Suggest changing to ‘…have hardly been studied, especially in sub-Saharan Africa…’

Hyphenation is a recurring problem in the manuscript:

• Recommend changing first sentence of Abstract to read ‘We conducted a clinic-based cross-sectional survey among 710 PLWHA in stable ‘sexual’ relationships in central and southwestern Uganda.

• Recommend changing ‘HIV related’ to ‘HIV-related’ in the Abstract, Methods section and throughout the manuscript.

• Please change ‘HIV infected’ to ‘HIV-infected’ throughout the manuscript.

• Please change ‘HIV positive’ to ‘HIV-positive’ throughout the manuscript.

Abstract, Methods section: Suggest changing to ‘…psychosocial factors (maladaptive coping styles, negative life events, social support, resilience, HIV stigma)…’

Inappropriate capitalisation if a recurring problem in the manuscript:

• Recommend changing sentence in Abstract, Methods section to ‘…and clinical factors (CD4 counts, body weight, height, HIV clinical stage, treatment adherence).’

• Recommend changing to ‘negative life events’, ‘social support’, and ‘resilience’ in Methods, Study variables, fourth sentence.

• Introduction, third paragraph, fifth sentence: Categories of sexual dysfunction do not need to be capitalised.

• Methods, Study variables, fifth sentence: Recommend changing to ‘body weight’ and ‘height’.

• Table 1: ‘Others’ in ‘Moslems & Others’ don’t need to be capitalised.

• Table 2a, Orgasm problems, second item: ‘How’ does not need to be capitalised.

• Results, Factors associated with sexual dysfunction, first paragraph, third sentence: ‘Depressive’ in ‘Major Depressive disorder’ does not need to be capitalised.

Abstract, first sentence of Results: Suggest changing to ‘SD was more prevalent in women (38.7%) than men (17.6%) and the majority (89.3% of men and 66.3% of women)…’

Abstract, first sentence of Conclusion: Suggest changing to ‘Sexual dysfunction has considerable prevalence among PLWHA in Uganda. It is associated with socio-demographic, psychiatric and clinical illness factors. To further improve the quality of life of PLWHA, they should be screened for sexual dysfunction as part of routine assessment.’

Introduction, first paragraph, second sentence: Suggest changing to ‘As a result, attention has now shifted to…’

Introduction, first paragraph, fourth sentence: Suggest changing to ‘Sexual function in the context of HIV/AIDS has mainly been studied with respect to…’

Introduction, first paragraph, fifth sentence: Suggest changing to ‘From a public health perspective, sexual problems may predispose individuals to unsafe sexual practices as well as intimate partner relationship discord, including marital violence, and poor ART adherence.

Introduction, first paragraph, seventh sentence: Recommend changing ‘ill mental health’ to ‘poor mental health’.

Introduction, second paragraph, second sentence: Suggest changing to ‘It involves the feelings of desire, behavior that brings pleasure to oneself and one’s partner, and stimulation of the primary sex organs, including coitus. The activity should be devoid of…’

Introduction, second paragraph, third sentence: Suggest changing to ‘Anatomy, physiology, psychology, the culture in which one lives, relationships with others, and the developmental experiences throughout the life cycle determines sexuality.’

Introduction, third paragraph, third sentence: Please replace ‘FSD’ with ‘SD’.

Methods, Study setting, second paragraph, third sentence: Suggest changing to ‘On the other hand, TASO Entebbe commenced its work in 1991 and…’

Methods, Study setting, second paragraph, fourth sentence: Suggest changing to ‘Entebbe, being urbanized, has an ever-growing and transient population including traders, fish-mongers, and uniformed personnel. It is also a first and last stop for international tourists.’

Methods, Study variables, first paragraph, first sentence: Suggest changing to ‘A range of explanatory variables that included socio-demographic, psychiatric illness, and clinical factors were assessed.’

Methods, Study variables, first paragraph, second sentence: Suggest changing ‘…constructed from common household items…’ to ‘…constructed from having common household items…’

Methods, Study variables, first paragraph, third sentence: Suggest changing to ‘The psychiatric illness factors included major depressive disorder and suicidality (assessed using the Mini International Neuropsychiatric interview (M.I.N.I. Plus) (Sheehan and Lecrubier 2006); severity of depressive symptoms was assessed using the Centre for Epidemiological Studies-Depression questionnaire (CES-D).’

Methods, Study variables, first paragraph, fourth sentence: The abbreviation ‘COPE’ needs to be defined at first mention.

Methods, Study variables, first paragraph, fifth sentence: The reference here, presumably WHO 2007, needs to be reviewed for style.

Methods, Study variables, fifth paragraph, first sentence: Recommend removing ‘International Index of Erectile Function’ in favour of abbreviation ‘IIEF’, as this has been previously defined.

Methods, Study variables, fifth paragraph, first sentence: Recommend removing ‘Female Sexual Functioning Index’ in favour of abbreviation ‘FSFI’, as this has been previously defined.

Methods, Study variables, fifth paragraph, first sentence: Recommend changing ‘…and determination of their internal consistency…’ to ‘…and subsequent determination of their internal consistency…’

Methods, Study variables, fifth paragraph, first sentence: Please change ‘Cronbach alpha’ to ‘Cronbach’s alpha’.

Methods, Study variables, fifth paragraph, second sentence: Please change ‘undertaken’ to ‘undertake’.

Methods, Study variables, fifth paragraph, third sentence: Please change ‘consistence’ to ‘consistency’.

Methods, Study variables, fifth paragraph, fifth sentence: Again, please remove the whole name of measures in favour of their abbreviations, IIEF and FSFI, since these have been previously defined.

Methods, Statistical analysis, first paragraph, fourth sentence: Please change to “sexual dysfunction for men” and “sexual dysfunction for women” as these are separate variables.

Methods, Statistical analysis, first paragraph, fifth sentence: Suggest changing to ‘To investigate the association of sexual dysfunction with socio-demographic, psychosocial and psychiatric illness factors…’

Methods, Statistical analysis, second paragraph: Suggest changing ‘at bivariate analyses’ to ‘with bivariate analyses’.

Results, Participant characteristics, second sentence: Suggest changing to ‘The majority of the participants…’

Table 1: ‘Moslems’ should be ‘Muslims’

Table 1: ‘ses’ should be ‘SES’ (three instances)

Results, Nature and prevalence of sexual dysfunction, second paragraph, second sentence: Suggest changing to ‘The majority of both men (89.3%) and women (66.3%) did not seek help for sexual dysfunction, but more women (25%) sought help from…’

Results, Nature and prevalence of sexual dysfunction, second paragraph, third sentence: Suggest changing ‘Of note 3.4% and 6.6%’ to ‘Of note, 3.4% and 6.6%’.

Table 2a: Please check the bolding of certain words and letters. This does not seem to be for emphasis or, if it is, has been applied incorrectly.

Table 2a, Sexual Pain problems, third item: ‘Over the past 4 weeks’ is unnecessary as it’s indicated at the top of the table.

Table 2b: Please check the underline of certain words. Is this necessary?

Table 2b, Sexual dysfunction, second row: Please delete empty row.

Results, Factors associated with sexual dysfunction, first paragraph, second sentence: Suggest changing to ‘A marital status indicated as widowed or separated…’

Results, Factors associated with sexual dysfunction, first paragraph, second sentence: Please change ‘Table 3’ to ‘Table 3 and 4’ since these results are the same using bivariate or multivariate analysis.

Results, Factors associated with sexual dysfunction, first paragraph, fourth sentence: Please change ‘Table 5’ to ‘Table 4’. There is no Table 5.

Discussion, general: Please replace ‘sexual dysfunction’ with ‘SD’ as the abbreviation is well-defined at this stage.

Discussion, first paragraph, first sentence: Suggest changing to ‘We sought to explore the topic of sexual functioning among patients living with HIV in Uganda, a rather taboo topic in this setting, with an aim of informing…’

Discussion, first paragraph, second and third sentences: Suggest changing to ‘SD is a relatively common problem experienced by men and women living with HIV in Uganda, with one in five men and two in five women affected. Studies on SD in PLWHA…’

Discussion, first paragraph, fourth sentence: Suggest changing to ‘It is worth noting that for both men and women with SD, the majority did not seek treatment. This was especially so for men, with less…’

Discussion, Nature and prevalence of dysfunction among PLWHA, second sentence: Please change ‘dysfunctions’ to ‘dysfunction’.

Discussion, Nature and prevalence of dysfunction among PLWHA, fourth sentence: Suggest changing to ‘This finding is similar to what has been reported in previous studies which found that the healthcare system may not be prepared for immediate or continuing support…’

Discussion, Factors associated with sexual dysfunction in HIV infected men, second paragraph, eighth sentence: Please change ‘2’ to ‘two’.

Discussion, Factors associated with sexual dysfunction in HIV infected men, second paragraph, ninth sentence: Please remove duplication of ‘on the’ in ‘on the on the other hand’.

Discussion, Factors associated with sexual dysfunction in HIV infected women, second paragraph, second sentence: Suggest changing to ‘In our study, a number of sexual problems, relating to reduced desire for and difficulties during sexual activity, were experienced by women. These findings are similar to findings…’

Discussion, Factors associated with sexual dysfunction in HIV infected women, second paragraph, fourth sentence: Suggest changing to ‘Concerns about HIV transmission, HIV treatment including ART and its side-effects…’

Discussion, Factors associated with sexual dysfunction in HIV infected women, second paragraph, fifth sentence: Suggest changing to ‘This could be a possible explanation why one in three women who participated…’

Discussion, Factors associated with sexual dysfunction in HIV infected women, third paragraph, first sentence: Suggest changing to ‘We found that older age (>45 years) and being widowed or separated…’

Discussion, Factors associated with sexual dysfunction in HIV infected women, third paragraph, second sentence: Suggest changing to ‘Oyedokun and others (2014) found no association between FSD and religion among HIV-positive women in Nigeria, however, increasing age (Oyedokun, Odeigah et al. 2014), was significantly associated with FSD (Luzi, Guaraldi et al. 2009). These findings are corroborated in our study.’

Discussion, Factors associated with sexual dysfunction in HIV infected women, third paragraph, third sentence: Please add a space after the bracket in ‘(Luzi, Guaraldi et al. 2009) and one can’.

Discussion, Factors associated with sexual dysfunction in HIV infected women, fifth paragraph, first sentence: Please add a space before the bracket in ‘higher (Wilson, Jean-Louis et al. 2010)’.

Discussion, Factors associated with sexual dysfunction in HIV infected women, sixth paragraph, first sentence: Suggest changing to ‘Psychosocial variables such as mental health status and quality of life, but not clinical status (illness stage), have been reported…’

References: References should be numbered and their style should be standardised throughout the manuscript.

Abstract

Sentence starting with ‘However, it is rarely discussed…’: Recommend replacing ‘secretive’ with ‘private’.

Introduction

Introduction, second paragraph, first sentence: Recommend changing to ‘Normal sexuality if a psycho-biological activity necessary for psychological and biological balance in most humans, and for the continuation of human life.’ It is dangerous to make blanket statements about sexuality being necessary for all people as it marginalises those who cannot, or choose not to, engage with their sexuality.

Introduction, third paragraph, section from ‘PLWHA are living longer and healthier lives…’ up to ‘…unintended pregnancy (Harrison and O’Sullivan 2010, Okigbo and Speizer 2015, Wasswa, Kabagenyi et al. 2020). In the first instance, the references should be standardised to a single format. In the second instance, this seems to be a repetition and expansion of what was said in the first paragraph of the introduction. Recommend working in the contents of the first paragraph into this one, resulting in the paragraph starting with ‘Normal sexuality…’ being the first of the Introduction.

Methods

Methods, Study design, second sentence: Please explain why sexual is written in inverted commas (‘sexual’ relationships). I have not been able to find a rationale for this in the manuscript. It seems unnecessary and could alienate readers.

Methods, Statistical analysis, general: I can appreciate that this may have been difficult to ascertain and potentially impossible to obtain reliable reporting on, given the setting, but did the authors consider subgroup effects by homo- and heterosexual respondents? While I understand potential legal ramifications of exploring this, it should at least be noted in the limitations as important subgroup effects might exist – particularly since major depressive disorder is a risk factor for sexual dysfunction. It is likely that MDD disproportionately affects homosexual people, particularly in a context where they are not free to express their sexuality.

Results

Results, Participant characteristics: Please make some mention of the disproportionate representation of women in the sample. Conclusions based on a sample of 159 men, particularly when juxtaposed or compared with women, could be spurious, and should be noted.

Results, Nature and prevalence of sexual dysfunction, first paragraph, third sentence: ‘number of times sexual intercourse was attempted’ is listed as a prevalent problem. What does this mean? Is a high number of attempts bad or indicative or sexual dysfunction?

Table 3: It is not clear from this table or the accompanying methodological text why certain parameters are set at 1 with no 95% confidence interval indicated. Were these variables set as such in the model? This needs to be explained.

Table 3: It is not clear why no results of HIV neurocognitive impairment is given for men. This needs to be described, either by a footnote to the table or in text.

Table 4: Please provide the results of stroke from the bivariate model in Table 3, as it is not listed there. Stroke, presumably previous stroke, shows significant association with SD for both men and women, and the results from the bivariate analysis should be shown. In addition, the outcome should be capitalised to ‘Stroke’ and the significance level for men should be shown as ‘P=0.023’.

Table 4: Bivariate analysis of diabetes in men meets the a priori cut-off of P=0.2 for inclusion in the multivariate model. Why are these results not presented?

Results, Factors associated with sexual dysfunction: It is not clear why some results from the bivariate model and some results from the multivariate model are reported. Results from the multivariate model, representing the most adjusted measures, should be used preferentially – unless there is a reason not to do so. If the latter is the case, this needs to be explicitly explained. If both results need to be reported, they should be clearly identified according to the model it is derived from.

Results, Factors associated with sexual dysfunction, first paragraph: In addition to other socio-demographic variables listed, employment is also significantly associated with SD in women at the 5% level.

Results, Factors associated with sexual dysfunction, first paragraph: It is not clear why only some numeric results from statistical models are reported in text.

Results, Factors associated with sexual dysfunction, first paragraph, third sentence: Please change ‘0.61’ to ‘1.61’ in accordance with the result in Table 4.

Results, Factors associated with sexual dysfunction, second paragraph, first sentence: Suggest changing to ‘With respect to men, religion (being of the Muslim or another faith) was the only…’

Results, Factors associated with sexual dysfunction, second paragraph: In addition to other socio-demographic variables listed, age is also highly significantly associated with SD in men. Why is this not mentioned here?

Results, Factors associated with sexual dysfunction, second paragraph: Stroke is also significantly associated with SD in men according to the results presented in Table 4. This needs to be reported here, particularly in the light of the role of the vascular system in erectile function.

Results, Factors associated with sexual dysfunction, third paragraph: It is not clear why this information is presented here. The text relating to the ages of respondents should be placed at the start of the Results section, though the age of male respondents should also be reported. Furthermore, the categorisation of education and religion should be described in the Methods section. Finally, it is not clear why this section describes the categorisation of religion as ‘Christian and non-Christian’ when all other sections report ‘Christian’ and ‘Muslim and others’.

Discussion

Discussion, Factors associated with sexual dysfunction in HIV infected men, general: The authors state that their study did not find associations with physical or anthropometric factors and SD. However, both stroke (in the multivariate model) and diabetes (in the bivariate model, with no results for multivariate analysis despite meeting the a priori cut-off) are significantly associated with male SD. Both of these also have known vascular causes and/or effects; the vascular system, in turn, is arguably the most important system for erectile function. As such, the statement that no associations between physical factors and SD were found is patently incorrect.

Discussion, Factors associated with sexual dysfunction in HIV infected men, second paragraph, sixth sentence: It is not clear what the (10) at the end of this sentence refers to. The next sentence seems to follow on from this, stating ‘In that study’, but reference 10 in the manuscript does not correspond to Lallemand, Salhi et al. 2002.

Discussion, Factors associated with sexual dysfunction in HIV infected men, second paragraph, eighth sentence: The authors state the no association was found with ART, however, ‘ART’ as an explanatory variable was not measured – only ART adherence. Please specify here whether ART adherence is the intention, or whether some other dimension of ‘ART’ was measured and its association tested.

Discussion, Factors associated with sexual dysfunction in HIV infected women, third paragraph, general: It is noticeable how much discussion is had around the causal pathways of age in SD in women living with HIV, yet nothing is said about the effect of age for men. This is a glaring omission.

Limitations

As noted previously, it is acknowledged that the legal environment in Uganda may have precluded the accurate gathering of information around homo- and heterosexuality among the sample. However, there may be important subgroup effects and this possibility should be noted here.

Author contributions

The authors state that detailed contributions are to be listed under the section in the second sentence, however, no such information is forthcoming. The only explicit contribution that is listed is analysis and interpretation by WS. This is not sufficient detail to determine whether ICMJE authorship criteria have been met.

**********

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Reviewer #1: No

**********

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Attachment

Submitted filename: Peer review comments on PONE-D-22-24725_.pdf

pone.0295224.s001.pdf (639.2KB, pdf)
PLoS One. 2024 Mar 7;19(3):e0295224. doi: 10.1371/journal.pone.0295224.r002

Author response to Decision Letter 0


28 Dec 2022

Dear Sir/Madam,

Response to review comments

Comment Response

General

Abstract, sentence starting with ‘Among individuals living with HIV/AIDS…’: Suggest adding changing

to ‘…have hardly been studied, especially in sub-Saharan Africa…’ Thank you for the comment. The change has been effected as advised. Page 1

[Lack of] hyphenation is a recurring problem in the manuscript:

• Recommend changing first sentence of Abstract to read ‘We conducted a clinic-based cross-sectional

survey among 710 PLWHA in stable ‘sexual’ relationships in central and southwestern

Uganda. The first sentence of abstract has been changed to read as: We conducted a clinic-based cross-sectional survey among 710 people living with HIV/AIDS in stable ‘sexual’ relationships in central and southwestern Uganda.

• Recommend changing ‘HIV related’ to ‘HIV-related’ in the Abstract, Methods section and

throughout the manuscript ‘HIV related’ has been changed to ‘HIV-related’ throughout the manuscript

• Please change ‘HIV infected’ to ‘HIV-infected’ throughout the manuscript. ‘HIV infected’ has been changed to ‘HIV-infected’ throughout the manuscript

• Please change ‘HIV positive’ to ‘HIV-positive’ throughout the manuscript. ‘HIV positive’ has been changed to ‘HIV-positive’ throughout the manuscript

Abstract, Methods section: Suggest changing to ‘…psychosocial factors (maladaptive coping styles,

negative life events, social support, resilience, HIV stigma)…’ The change has been effected as advised Page 1

Inappropriate capitalisation is a recurring problem in the manuscript: Recommend changing sentence in Abstract, Methods section to ‘…and clinical factors (CD4 counts, body weight, height, HIV clinical stage, treatment adherence).’ The sentence has been changed as recommended

Recommend changing to ‘negative life events’, ‘social support’, and ‘resilience’ in Methods,

Study variables, fourth sentence. The sentence has been changed as recommended

Introduction, third paragraph, fifth sentence: Categories of sexual dysfunction do not need to be capitalised. Thank you for the observation. The capitalisation has been removed

Methods, Study variables, fifth sentence: Recommend changing to ‘body weight’ and ‘height’. Thank you. The change has been effected as recommended

Table 1: ‘Others’ in ‘Moslems & Others’ don’t need to be capitalised. The capitalisation has been removed

Table 2a, Orgasm problems, second item: ‘How’ does not need to be capitalised. The capitalisation has been removed

Results, Factors associated with sexual dysfunction, first paragraph, third sentence: ‘Depressive’ in ‘Major Depressive disorder’ does not need to be capitalised. The capitalisation has been removed

Abstract, first sentence of Results: Suggest changing to ‘SD was more prevalent in women (38.7%) than men (17.6%) and the majority (89.3% of men and 66.3% of women)…’ The change has been effected as suggested

Abstract, first sentence of Conclusion: Suggest changing to ‘Sexual dysfunction has considerable prevalence among PLWHA in Uganda. It is associated with socio-demographic, psychiatric and clinical illness factors. To further improve the quality of life of PLWHA, they should be screened for sexual dysfunction as part of routine assessment.’ The change has been effected as recommended

Introduction, first paragraph, second sentence: Suggest changing to ‘As a result, attention has now shifted to…’ The change has been effected as recommended

Introduction, first paragraph, fourth sentence: Suggest changing to ‘Sexual function in the context of HIV/AIDS has mainly been studied with respect to…’ The change has been effected as recommended

Introduction, first paragraph, fifth sentence: Suggest changing to ‘From a public health perspective, sexual problems may predispose individuals to unsafe sexual practices as well as intimate partner relationship discord, including marital violence, and poor ART adherence. The change has been effected as recommended

Introduction, first paragraph, seventh sentence: Recommend changing ‘ill mental health’ to ‘poor mental health’. The change has been effected as recommended

Introduction, second paragraph, second sentence: Suggest changing to ‘It involves the feelings of desire, behavior that brings pleasure to oneself and one’s partner, and stimulation of the primary sex organs, including coitus. The activity should be devoid of…’ The change has been effected as recommended

Introduction, second paragraph, third sentence: Suggest changing to ‘Anatomy, physiology, psychology, the culture in which one lives, relationships with others, and the developmental

experiences throughout the life cycle determines sexuality.’

Introduction, third paragraph, third sentence: Please replace ‘FSD’ with ‘SD’. The change has been effected as recommended

Methods, Study setting, second paragraph, third sentence: Suggest changing to ‘On the other hand,

TASO Entebbe commenced its work in 1991 and…’ The change has been effected as recommended

Methods, Study setting, second paragraph, fourth sentence: Suggest changing to ‘Entebbe, being urbanized, has an ever-growing and transient population including traders, fish-mongers, and uniformed personnel. It is also a first and last stop for international tourists.’ The change has been effected as recommended

Methods, Study variables, first paragraph, first sentence: Suggest changing to ‘A range of explanatory variables that included socio-demographic, psychiatric illness, and clinical factors were assessed.’ The change has been effected as recommended

Methods, Study variables, first paragraph, second sentence: Suggest changing ‘…constructed from common household items…’ to ‘…constructed from having common household items…’ The change has been effected as recommended

Methods, Study variables, first paragraph, third sentence: Suggest changing to ‘The psychiatric illness factors included major depressive disorder and suicidality (assessed using the Mini International Neuropsychiatric interview (M.I.N.I. Plus) (Sheehan and Lecrubier 2006); severity of depressive symptoms was assessed using the Centre for Epidemiological Studies-Depression questionnaire (CESD).’ The change has been effected as recommended

Methods, Study variables, first paragraph, fourth sentence: The abbreviation ‘COPE’ needs to be defined at first mention. The abbreviation COPE has been defined as ‘Coping Orientation to Problems Experienced’

Methods, Study variables, first paragraph, fifth sentence: The reference here, presumably WHO 2007, needs to be reviewed for style. The reference has been revised to WHO 2007

Methods, Study variables, fifth paragraph, first sentence: Recommend removing ‘International Index of Erectile Function’ in favour of abbreviation ‘IIEF’, as this has been previously defined. The change has been effected as recommended

Methods, Study variables, fifth paragraph, first sentence: Recommend removing ‘Female Sexual Functioning Index’ in favour of abbreviation ‘FSFI’, as this has been previously defined. The change has been effected as recommended

Methods, Study variables, fifth paragraph, first sentence: Recommend changing ‘…and determination of their internal consistency…’ to ‘…and subsequent determination of their internal consistency…’ The change has been effected as recommended

Methods, Study variables, fifth paragraph, first sentence: Please change ‘Cronbach alpha’ to ‘Cronbach’s alpha’. The change has been effected as recommended

Methods, Study variables, fifth paragraph, second sentence: Please change ‘undertaken’ to ‘undertake’. The change has been effected as recommended

Methods, Study variables, fifth paragraph, third sentence: Please change ‘consistence’ to ‘consistency’. The change has been effected as recommended

Methods, Study variables, fifth paragraph, fifth sentence: Again, please remove the whole name of measures in favour of their abbreviations, IIEF and FSFI, since these have been previously defined. The change has been effected as recommended

Methods, Statistical analysis, first paragraph, fourth sentence: Please change to “sexual dysfunction for men” and “sexual dysfunction for women” as these are separate variables. The change has been effected as recommended

Methods, Statistical analysis, first paragraph, fifth sentence: Suggest changing to ‘To investigate the association of sexual dysfunction with socio-demographic, psychosocial and psychiatric illness factors…’ The change has been effected as recommended

Methods, Statistical analysis, second paragraph: Suggest changing ‘at bivariate analyses’ to ‘with bivariate analyses’. The change has been effected as recommended

Results, Participant characteristics, second sentence: Suggest changing to ‘The majority of the participants…’ The change has been effected as recommended

Table 1: ‘Moslems’ should be ‘Muslims’ The change has been effected as recommended

Table 1: ‘ses’ should be ‘SES’ (three instances) The change has been effected as recommended

Results, Nature and prevalence of sexual dysfunction, second paragraph, second sentence: Suggest changing to ‘The majority of both men (89.3%) and women (66.3%) did not seek help for sexual dysfunction, but more women (25%) sought help from…’ The change has been effected as recommended

Results, Nature and prevalence of sexual dysfunction, second paragraph, third sentence: Suggest changing ‘Of note 3.4% and 6.6%’ to ‘Of note, 3.4% and 6.6%’. The change has been effected as recommended

Table 2a: Please check the bolding of certain words and letters. This does not seem to be for emphasis or, if it is, has been applied incorrectly. The bolding has been removed

Table 2a, Sexual Pain problems, third item: ‘Over the past 4 weeks’ is unnecessary as it’s indicated at the top of the table. It has been removed

Table 2b: Please check the underline of certain words. Is this necessary? The underline has been removed

Table 2b, Sexual dysfunction, second row: Please delete empty row. The empty row has been deleted

Results, Factors associated with sexual dysfunction, first paragraph, second sentence: Suggest changing to ‘A marital status indicated as widowed or separated…’ The change has been effected as recommended

Results, Factors associated with sexual dysfunction, first paragraph, second sentence: Please changes ‘Table 3’ to ‘Table 3 and 4’ since these results are the same using bivariate or multivariate analysis. ‘Table 3’ has been changed to ‘Table 3 and 4’

Results, Factors associated with sexual dysfunction, first paragraph, fourth sentence: Please change ‘Table 5’ to ‘Table 4’. There is no Table 5. ‘Table 5’ has been changed to ‘Table 4’

Discussion, general: Please replace ‘sexual dysfunction’ with ‘SD’ as the abbreviation is well-defined at this stage. The change has been effected as recommended

Discussion, first paragraph, first sentence: Suggest changing to ‘We sought to explore the topic of sexual functioning among patients living with HIV in Uganda, a rather taboo topic in this setting, with an aim of informing…’ The change has been effected as recommended

Discussion, first paragraph, second and third sentences: Suggest changing to ‘SD is a relatively common problem experienced by men and women living with HIV in Uganda, with one in five men and two in five women affected. Studies on SD in PLWHA…’ The change has been effected as recommended

Discussion, first paragraph, fourth sentence: Suggest changing to ‘It is worth noting that for both men and women with SD, the majority did not seek treatment. This was especially so for men, with less…’ The change has been effected as recommended

Discussion, Nature and prevalence of dysfunction among PLWHA, second sentence: Please change ‘dysfunctions’ to ‘dysfunction’. The change has been effected as recommended

Discussion, Nature and prevalence of dysfunction among PLWHA, fourth sentence: Suggest changing to ‘This finding is similar to what has been reported in previous studies which found that the healthcare system may not be prepared for immediate or continuing support…’ The change has been effected as recommended

Discussion, Factors associated with sexual dysfunction in HIV infected men, second paragraph, and eighth sentence: Please change ‘2’ to ‘two’. The change has been effected as recommended

Discussion, Factors associated with sexual dysfunction in HIV infected men, second paragraph, ninth Sentence: Please remove duplication of ‘on the’ in ‘on the on the other hand’. The change has been effected as recommended

Discussion, Factors associated with sexual dysfunction in HIV infected women, second paragraph, second sentence: Suggest changing to ‘In our study, a number of sexual problems, relating to reduced desire for and difficulties during sexual activity, were experienced by women. These findings are similar to findings…’ The change has been effected as recommended

Discussion, Factors associated with sexual dysfunction in HIV infected women, second paragraph, fourth sentence: Suggest changing to ‘Concerns about HIV transmission, HIV treatment including ART and its side-effects…’ The change has been effected as recommended

Discussion, Factors associated with sexual dysfunction in HIV infected women, second paragraph, and fifth sentence: Suggest changing to ‘This could be a possible explanation why one in three women who participated…’ The change has been effected as recommended

Discussion, Factors associated with sexual dysfunction in HIV infected women, third paragraph, and first sentence: Suggest changing to ‘We found that older age (>45 years) and being widowed or separated…’ The change has been effected as recommended

Discussion, Factors associated with sexual dysfunction in HIV infected women, third paragraph, second sentence: Suggest changing to ‘Oyedokun and others (2014) found no association between FSD and religion among HIV-positive women in Nigeria, however, increasing age (Oyedokun, Odeigah et al. 2014), was significantly associated with FSD (Luzi, Guaraldi et al. 2009). These findings are corroborated in our study.’ The change has been effected as recommended

Discussion, Factors associated with sexual dysfunction in HIV infected women, third paragraph, third sentence: Please add a space after the bracket in ‘(Luzi, Guaraldi et al. 2009) and one can’. A space has been added

Discussion, Factors associated with sexual dysfunction in HIV infected women, fifth paragraph, first sentence: Please add a space before the bracket in ‘higher (Wilson, Jean-Louis et al. 2010)’. The change has been effected as recommended

Discussion, Factors associated with sexual dysfunction in HIV infected women, sixth paragraph, first sentence: Suggest changing to ‘Psychosocial variables such as mental health status and quality of life, but not clinical status (illness stage), have been reported…’ The change has been effected as recommended

References: References should be numbered and their style should be standardised throughout the manuscript. The references have been numbered

Abstract

Sentence starting with ‘However, it is rarely discussed…’: Recommend replacing ‘secretive’ with ‘private’. This seems to be a more appropriate word as sexual life is considered private by many, but not necessarily a secret. The change has been effected as recommended

Introduction

Introduction, second paragraph, first sentence: Recommend changing to ‘Normal sexuality if a psychobiological activity necessary for psychological and biological balance in most humans, and for the continuation of human life.’ It is dangerous to make blanket statements about sexuality being necessary for all people as it marginalises those who cannot, or choose not to, engage with their sexuality. The change has been effected as recommended

Introduction, third paragraph, section from ‘PLWHA are living longer and healthier lives…’ up to‘…unintended pregnancy (Harrison and O’Sullivan 2010, Okigbo and Speizer 2015, Wasswa, Kabagenyi et al. 2020). In the first instance, the references should be standardised to a single format. In the second instance, this seems to be a repetition and expansion of what was said in the first paragraph of the introduction. Recommend working in the contents of the first paragraph into this one, resulting in the paragraph starting with ‘Normal sexuality…’ being the first of the Introduction. The section has been revised and the sentence on normal sexuality is now the first one in the introduction

Methods

Methods, Study design, the second sentence: Please explain why sexual is written in inverted commas (‘sexual’ relationships). I have not been able to find a rationale for this in the manuscript. It seems unnecessary and could alienate readers. Thank you for the comment. The inverted commas have been removed.

Methods, Statistical analysis, general: I can appreciate that this may have been difficult to ascertain and potentially impossible to obtain reliable reporting on, given the setting, but did the authors consider subgroup effects by homo- and heterosexual respondents? While I understand potential legal ramifications of exploring this, it should at least be noted in the limitations as important subgroup effects might exist – particularly since major depressive disorder is a risk factor for sexual dysfunction. It is likely that MDD disproportionately affects homosexual people, particularly in a context where they are not free to express their sexuality. We were not able to conduct subgroup analyses by homo- and heterosexual respondents. In Uganda, homosexuality is still a sensitive issue to discuss.

Results

Results, Participant characteristics: Please make some mention of the disproportionate representation of women in the sample. Conclusions based on a sample of 159 men, particularly when juxtaposed or compared with women, could be spurious, and should be noted. A sentence has been added to the 3rd paragraph in the discussion section ‘However, the number of men was smaller than that of women in this study. This could have affected the results.’

Results, Nature and prevalence of sexual dysfunction, first paragraph, third sentence: ‘number of times sexual intercourse was attempted’ is listed as a prevalent problem. What does this mean? Is a high number of attempts bad or indicative or sexual dysfunction? The number of times sexual intercourse was attempted was measured as” no attempts, one to two attempts/ three to four attempts, five to six attempts, seven to ten attempts/ Eleven or more attempts”. In this case, fewer sexual attempts were assumed to indicate lower sex drive and, therefore sexual dysfunction.

Table 3: It is not clear from this table or the accompanying methodological text why certain parameters are set at 1 with no 95% confidence interval indicated. Were these variables set as such in the model? This needs to be explained. The parameters that were set at 1 are the comparison factors. The odds of these other parameters/categories are interpreted in relation to the comparison parameters

Table 3: It is not clear why no results of HIV neurocognitive impairment are given for men. This needs to be described, either by a footnote to the table or in text. * HIV neurocognitive impairment among men was not included due to perfect collinearity. This has been added as a footnote

Table 4: Please provide the results of stroke from the bivariate model in Table 3, as it is not listed there. Stroke, presumably previous stroke, shows significant association with SD for both men and women, and the results from the bivariate analysis should be shown. In addition, the outcome should be capitalised to ‘Stroke’ and the significance level for men should be shown as ‘P=0.023’. Thank you for the observation. The results have been included in table 3

Table 4: Bivariate analysis of diabetes in men meets the a priori cut-off of P=0.2 for inclusion in the multivariate model. Why are these results not presented? Some of the factors met the apriori cut-off. However they presented multicollinearity in the multivariate model and therefore reducing precision of the estimates and were therefore eliminated.

Results, Factors associated with sexual dysfunction: It is not clear why some results from the bivariate model and some results from the multivariate model are reported. Results from the multivariate model, representing the most adjusted measures, should be used preferentially – unless there is a reason not to do so. If the latter is the case, this needs to be explicitly explained. If both results need to be reported, they should be clearly identified according to the model it is derived from. Some of the factors met the apriori cut-off. However they presented multicollinearity in the multivariate model and therefore reducing precision of the estimates and were therefore eliminated.

Results, Factors associated with sexual dysfunction, first paragraph: In addition to other sociodemographic variables listed, employment is also significantly associated with SD in women at the 5% level. This has been indicated

Results, Factors associated with sexual dysfunction, first paragraph: It is not clear why only some numeric results from statistical models are reported in text. The details of the results are in the table. It would have been repetition to report all results in text and table

Results, Factors associated with sexual dysfunction, first paragraph, third sentence: Please change ‘0.61’ to ‘1.61’ in accordance with the result in Table 4. Thank you for the observation. This has been addressed

Results, Factors associated with sexual dysfunction, second paragraph, first sentence: Suggest changing to ‘With respect to men, religion (being of the Muslim or another faith) was the only…’ This has been changed. Thanks for the comment. This has been addressed

Results, Factors associated with sexual dysfunction, second paragraph: In addition to other sociodemographic variables listed, age is also highly significantly associated with SD in men. Why is this not mentioned here? Age has been included. Thank you for the observation

Results, Factors associated with sexual dysfunction, second paragraph: Stroke is also significantly associated with SD in men according to the results presented in Table 4. This needs to be reported here, particularly in the light of the role of the vascular system in erectile function. It has been included. Thank you

Results, Factors associated with sexual dysfunction, third paragraph: It is not clear why this information is presented here. The text relating to the ages of respondents should be placed at the start of the Results section, though the age of male respondents should also be reported The information has been removed from this section and taken to methods and the beginning of the results section

Furthermore, the categorisation of education and religion should be described in the Methods section. This has been taken to the end of the methods section

Finally, it is not clear why this section describes the categorisation of religion as ‘Christian and non-Christian’ when all other sections report ‘Christian’ and ‘Muslim and others’. This has been harmonised. Religion is categorised as Christian and, muslim and other religion

Discussion

Discussion, Factors associated with sexual dysfunction in HIV infected men, general: The authors state that their study did not find associations with physical or anthropometric factors and SD. However, both stroke (in the multivariate model) and diabetes (in the bivariate model, with no results for multivariate analysis despite meeting the a priori cut-off) are significantly associated with male SD. Both of these also have known vascular causes and/or effects; the vascular system, in turn, is arguably the most important system for erectile function. As such, the statement that no associations between physical factors and SD were found is patently incorrect. Thank you so much for the observarion . it was a wrong statement and it has been corrected. Indeed, diabetes and stroke and known risk factors for sexual dysfunction. In our results, they were associated with SD.

Discussion, Factors associated with sexual dysfunction in HIV infected men, second paragraph, sixth sentence: It is not clear what the (10) at the end of this sentence refers to. The next sentence seems to follow on from this, stating ‘In that study’, but reference 10 in the manuscript does not correspond to Lallemand, Salhi et al. 2002. The mistake has been corrected. The reference is Lallemand et al 2002

Discussion, Factors associated with sexual dysfunction in HIV infected men, second paragraph, eighth sentence: The authors state the no association was found with ART, however, ‘ART’ as an explanatory

variable was not measured – only ART adherence. Please specify here whether ART adherence is the intention, or whether some other dimension of ‘ART’ was measured and its association tested. Thank you for the comment. The section refers to ART adherence and has been edited

Discussion, Factors associated with sexual dysfunction in HIV infected women, third paragraph, general: It is noticeable how much discussion is had around the causal pathways of age in SD in women living with HIV, yet nothing is said about the effect of age for men. This is a glaring omission. Thank you for this comment. A section has been added on the effect of age on sexual dysfunction among men.

Limitations

General: As noted previously, it is acknowledged that the legal environment in Uganda may have precluded the accurate gathering of information around homo- and heterosexuality among the sample. However, there may be important subgroup effects and this possibility should be noted here. Thank you for the comment. We did not do subgroup analysis. It is possible that there could have been important subgroup effects

Author contributions

General: The authors state that detailed contributions are to be listed under the section in the second sentence, however, no such information is forthcoming. The only explicit contribution that is listed is analysis and interpretation by WS. This is not sufficient detail to determine whether ICMJE authorship criteria have been met. Thank you for this reminder. It has been updated

Attachment

Submitted filename: Response to Review comments.pdf

pone.0295224.s002.pdf (491.4KB, pdf)

Decision Letter 1

Habil Otanga

22 May 2023

PONE-D-22-24725R1A ‘hidden problem’: Nature, prevalence and factors associated with sexual dysfunction in persons living with HIV/AIDS in UgandaPLOS ONE

Dear Dr. Godfrey Zari Rukundo,

Thank you for submitting your manuscript to PLOS ONE. After careful consideration, we feel that it has merit but does not fully meet PLOS ONE’s publication criteria as it currently stands. Therefore, we invite you to submit a revised version of the manuscript that addresses the points raised during the review process.

==============================

ACADEMIC EDITOR: Your work requires thorough editorial revision from grammar to in-text citations to referencing style.Revise the Methods and Discussion sections

==============================

Please submit your revised manuscript by Jul 06 2023 11:59PM. If you will need more time than this to complete your revisions, please reply to this message or contact the journal office at plosone@plos.org. When you're ready to submit your revision, log on to https://www.editorialmanager.com/pone/ and select the 'Submissions Needing Revision' folder to locate your manuscript file.

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We look forward to receiving your revised manuscript.

Kind regards,

Habil Otanga, Ph.D

Academic Editor

PLOS ONE

Additional Editor Comments (if provided):

1. Your work suffers serious editorial shortcomings, from grammar to in-text citations to referencing style.

2. Methods: ED was measured using 6 items on the IIEF. How was the cut-off score of 25 derived (on a 5 point Likert Scale) which is erroneously presented as a 6 point Likert Scale (Section on Study Variables Line 27)? What informed the cut-off score? Reviewers found fault with sampling techniques and determination of sample size, data collection tools and techniques.

Why was the definition for SD different for men and women judging by the fact that authors used a single subscale for men (6 items) and the total FSFI score for women?

3. Discussion/Results: All tables must be presented in APA format

-If scales were used, one would expect Table 2 (a, b) to present frequencies/means of variables and not items. Why were the tables presented item by item? When do variables cease to be items and become variables for analysis? What was used in analysis - items in the questionnaire or variables? Reviewers suggest that authors discuss the statistical part of how categorical and continuous data are reported

[Note: HTML markup is below. Please do not edit.]

Reviewers' comments:

Reviewer's Responses to Questions

Comments to the Author

1. If the authors have adequately addressed your comments raised in a previous round of review and you feel that this manuscript is now acceptable for publication, you may indicate that here to bypass the “Comments to the Author” section, enter your conflict of interest statement in the “Confidential to Editor” section, and submit your "Accept" recommendation.

Reviewer #2: (No Response)

Reviewer #3: (No Response)

**********

2. Is the manuscript technically sound, and do the data support the conclusions?

The manuscript must describe a technically sound piece of scientific research with data that supports the conclusions. Experiments must have been conducted rigorously, with appropriate controls, replication, and sample sizes. The conclusions must be drawn appropriately based on the data presented.

Reviewer #2: Partly

Reviewer #3: Yes

**********

3. Has the statistical analysis been performed appropriately and rigorously?

Reviewer #2: No

Reviewer #3: Yes

**********

4. Have the authors made all data underlying the findings in their manuscript fully available?

The PLOS Data policy requires authors to make all data underlying the findings described in their manuscript fully available without restriction, with rare exception (please refer to the Data Availability Statement in the manuscript PDF file). The data should be provided as part of the manuscript or its supporting information, or deposited to a public repository. For example, in addition to summary statistics, the data points behind means, medians and variance measures should be available. If there are restrictions on publicly sharing data—e.g. participant privacy or use of data from a third party—those must be specified.

Reviewer #2: Yes

Reviewer #3: Yes

**********

5. Is the manuscript presented in an intelligible fashion and written in standard English?

PLOS ONE does not copyedit accepted manuscripts, so the language in submitted articles must be clear, correct, and unambiguous. Any typographical or grammatical errors should be corrected at revision, so please note any specific errors here.

Reviewer #2: Yes

Reviewer #3: Yes

**********

6. Review Comments to the Author

Please use the space provided to explain your answers to the questions above. You may also include additional comments for the author, including concerns about dual publication, research ethics, or publication ethics. (Please upload your review as an attachment if it exceeds 20,000 characters)

Reviewer #2: Thanks for your paper. Whereas the paper presents an amazing perspective to sexual dysfunction among persons living with HIV in Uganda, there are issues that you need to address:

1. Editing: Your entire work suffers from poor editorial work. Words that are not proper nouns start with capital letters e.g., Line 2 of abstract.

-Line 2 of abstract is either incomplete or poorly punctuated (Sentence beginning with "Although"

2. Citations: You need to revise the entire work to be in line with the appropriate journal citation format.

Introduction: Line 5

Paragraph 2 of Introduction: Line 1, 3, 7, 9

Paragraph 3: Line 5, 8, 10, 12. for instance what citation style is "Wilson, Jean-Louis et al 2010"? Decide who the first author is, use their surname followed by et al and year of publication.

3. Methods: ED was measured using 6 items on the IIEF. How was the cut-off score of 25 derived (on a 5 point LS) which is erroneously presented as a 6 point LS (Section on Study Variables Line 27)? What informed the cut-off score?

Why was the definition for SD different for men and women judging by the fact that using a single subscale for men (6 items) and the total FSFI score for women?

4. Results: All tables must be presented in APA format

-If scales were used, one would expect Table 2 (a, b) to present frequencies/means of variables and not items. Why were the tables presented item by item? When do variables cease to be items and become variables for analysis? What was used in analysis - items in the questionnaire or variables?

5. References do not follow any distinct style. Check PLoS ONE requirements for presenting references.

Reviewer #3: Dear Editor, I would like to thank you for inviting me to review this cross-sectional study titled "Nature, prevalence, and factors associated with sexual dysfunction in persons living with HIV/AIDS in Uganda." This study addresses a novel and little-researched issue that affects both the general public and people living with HIV/AIDS. Despite the fact that there were interesting concepts scattered throughout the work, I've highlighted a few of my complaints below with subheadings that the authors should take into account before considering publishing.

Abstract:

- By taking into account the study period, sampling technique, data collection tools, and statistical methodologies (descriptive or inferential statistics), the authors needed to update the methods part of the abstract once more in light of their objectives.

- The authors must indicate the percentage with a 95% confidence interval for the prevalence of sexual disfunction for males and females, respectively.

- In light of their findings, the authors ought to revise their recommendations.

Introduction:

- The introduction section focuses primarily on the definition, nature, and determinants of sexual dysfunction, with little to no discussion of its prevalence. I should suggest that the authors review the global literature on the prevalence in order to briefly explain the epidemiology (the distribution) of sexual dysfunction.

Methods:

-When was this study done? considering that the information came from a secondary source and that the patients with HIV/AIDS were chosen from medical records from what years?

- In addition to mentioning that this research was conducted as part of Prof Eugene Kinyanda’s Senior EDCTP Fellowship funded study entitled, ‘Clinical trials in HIV/AIDS in Africa: Should they routinely control for mental health factors?’, I believe the authors missed an important section of the materials and methods section, such as how the participants for the study were selected (sampling technique) and the determination of sample size, data collection tools and techniques, the operational definitions of some concepts, etc.

- The authors should thoroughly discuss the statistical part of how categorical and continuous data are reported, respectively, and for variables in the final multivariate model, the authors should plan the adjusted odds ratio (AOR) along with the 95% confidence interval. When measuring the outcome variable, the authors needed to clearly categorize it into binary data by coding it.

- The authors had to identify at what level of significance the variables should be deemed significant in the final multivariate model, which also needed to be assessed and presented together with an AOR and a 95% confidence interval.

- Additionally, the authors had to disclose the precise categorization (their levels) of each independent variable measured in addition to stating the scales.

Results:

- I'm not sure why the authors chose to use the median rather than the mean when reporting the age.

- The authors had to specify what low and high socioeconomic status meant when classifying socioeconomic status based on the wealth index in the method section before reporting here.

- It is required to give the mean, plus or minus standard deviation, or the sub-total frequency of each domain of measurement scales when reporting sexual dysfunction in males and females. Additionally, for each outcome variable, the authors needed to indicate the 95% confidence interval.

- I'll advise you to place the subheading factors related to sexual dysfunction before presenting the tables labelled "bivariate analysis of related factors (not adjusted) and "multivariate model (tables 3 and 4).

Discussion:

- The finding was well discussed by the authors. The authors were also required to expand on their discussion by including earlier prevalence research related to sexual dysfunction as well as further implications of the study for low-income nations like those in sub-Saharan Africa.

- Although it appears that the authors are talking about qualitative findings in their discussion, I believe that they should concentrate on quantitative results instead because they evaluated the study in a quantitative manner, unless they felt the need to include qualitative data.

Conclusion and recommendation:

- The authors should have provided a more thorough summary of the main findings and recommendations based on those findings, particularly for those stakeholders working on behavioural changes related to HIV/AIDS and for concerned policymakers.

At last, the authors produced some excellent work, but they should pay particular attention to the methods section because the majority of its components are missing.

**********

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Reviewer #2: No

Reviewer #3: No

**********

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PLoS One. 2024 Mar 7;19(3):e0295224. doi: 10.1371/journal.pone.0295224.r004

Author response to Decision Letter 1


1 Nov 2023

October 27, 2023

Dr. Habil Otanga, Ph.D

Academic Editor

PLOS ONE

Dear Dr. Otanga,

Re: PONE-D-22-24725R1: A ‘hidden problem’: Nature, prevalence and factors associated with sexual dysfunction in persons living with HIV/AIDS in Uganda

Thank you for the opportunity to resubmit this manuscript. Your effort and that of the reviewers is highly appreciated. Here below is a point-by-point response to the review comments.

Comment Response Page with changes

Editor’s comments

1. Your work suffers serious editorial shortcomings, from grammar to in-text citations to referencing style.

Thak you for your comment. The manuscript has been revised and improved. Throughout the manuscript

2. Methods: ED was measured using 6 items on the IIEF. How was the cut-off score of 25 derived (on a 5-point Likert Scale) which is erroneously presented as a 6-point Likert Scale (Section on Study Variables Line 27)? What informed the cut-off score? Reviewers found fault with sampling techniques and determination of sample size, data collection tools and techniques.

Why was the definition for SD different for men and women judging by the fact that authors used a single subscale for men (6 items) and the total FSFI score for women?

This has been corrected to a 15 item tool.

the cut off score was informed by a previous study (IIEF (Rosen, Riley et al. 1997))

The definition from ISD is different as assessed differently by the different tools i.e IIEF & FSFI Page 7

3. Discussion/Results: All tables must be presented in APA format

-If scales were used, one would expect Table 2 (a, b) to present frequencies/means of variables and not items. Why were the tables presented item by item? The APA format has been implemented Pages 11, 12,13,14,15,16,17,18

When do variables cease to be items and become variables for analysis? What was used in analysis - items in the questionnaire or variables?

Items from the questionnaire were used to generate composite variables for the outcomes.

Standard variables like sociodemographic were also used.

Reviewers suggest that authors discuss the statistical part of how categorical and continuous data are reported This has been added Page 10

Reviewer #2: Thanks for your paper. Whereas the paper presents an amazing perspective to sexual dysfunction among persons living with HIV in Uganda, there are issues that you need to address:

1. Editing: Your entire work suffers from poor editorial work. Words that are not proper nouns start with capital letters e.g., Line 2 of abstract.

-Line 2 of abstract is either incomplete or poorly punctuated (Sentence beginning with "Although"

Thank you for the observation. This has been addressed in the revised manuscript

2. Citations: You need to revise the entire work to be in line with the appropriate journal citation format.

Introduction: Line 5

Paragraph 2 of Introduction: Line 1, 3, 7, 9

Paragraph 3: Line 5, 8, 10, 12. for instance what citation style is "Wilson, Jean-Louis et al 2010"? Decide who the first author is, use their surname followed by et al and year of publication.

Thank you for the guidance. The citations have been revised as advised.

3. Methods: ED was measured using 6 items on the IIEF. How was the cut-off score of 25 derived (on a 5 point LS) which is erroneously presented as a 6 point LS (Section on Study Variables Line 27)? What informed the cut-off score?

Why was the definition for SD different for men and women judging by the fact that using a single subscale for men (6 items) and the total FSFI score for women?

This has been addressed in comment 2 above.

4. Results: All tables must be presented in APA format

-If scales were used, one would expect Table 2 (a, b) to present frequencies/means of variables and not items. Why were the tables presented item by item? When do variables cease to be items and become variables for analysis? What was used in analysis - items in the questionnaire or variables?

This has been addressed. All tables are in APA format Pages 11, 12,13,14,15,16,17,18

5. References do not follow any distinct style. Check PLoS ONE requirements for presenting references. The references have been revised

Reviewer #3:

Abstract:

- By taking into account the study period, sampling technique, data collection tools, and statistical methodologies (descriptive or inferential statistics), the authors needed to update the methods part of the abstract once more in light of their objectives.

The methods section of the abstract has been revised. We added that ‘Statistical analyses were conducted using Stata release 15, separately for males and females. Frequencies to the FSFI and IIEF were estimated with their percentages. Categorical variables were described using frequencies and percentages while continuous variables were described using median (IQR). Two binary outcome variables “sexual dysfunction for men and sexual dysfunction for women” were generated. To investigate the association of sexual dysfunction with socio-demographic and psychosocial and psychiatric illness factors, a two-step procedure was adopted. During the first step, bivariate associations between each of the outcome variables and the independent variables were assessed using simple logistic regression models. In the second step, those socio-demographic, psychosocial and psychiatric illness factors that attained a level of significance of P ≤ 0.2 (liberal cut-off point) with bivariate analyses were included in the final multivariate logistic regression models that assessed for the factors that were independently significantly associated with sexual dysfunction. We were not able to conduct subgroup analyses by homo- and heterosexual respondents)

- The authors must indicate the percentage with a 95% confidence interval for the prevalence of sexual disfunction for males and females, respectively.

This has been incorporated Page 12

- In light of their findings, the authors ought to revise their recommendations.

Although SD exists in both female and male patients with HIV, there need for specific interventions for the different genders.

Introduction:

- The introduction section focuses primarily on the definition, nature, and determinants of sexual dysfunction, with little to no discussion of its prevalence. I should suggest that the authors review the global literature on the prevalence in order to briefly explain the epidemiology (the distribution) of sexual dysfunction.

The section has been revised to include information on the global burden of SD 5

Methods:

-When was this study done? considering that the information came from a secondary source and that the patients with HIV/AIDS were chosen from medical records from what years?

- In addition to mentioning that this research was conducted as part of Prof Eugene Kinyanda’s Senior EDCTP Fellowship funded study entitled, ‘Clinical trials in HIV/AIDS in Africa: Should they routinely control for mental health factors?’, I believe the authors missed an important section of the materials and methods section, such as how the participants for the study were selected (sampling technique) and the determination of sample size, data collection tools and techniques, the operational definitions of some concepts, etc.

Thank you for the observation. More details have been added on page 7 of the revised manuscript 7

- The authors should thoroughly discuss the statistical part of how categorical and continuous data are reported, respectively, and for variables in the final multivariate model, the authors should plan the adjusted odds ratio (AOR) along with the 95% confidence interval. When measuring the outcome variable, the authors needed to clearly categorize it into binary data by coding it.

This has been done Page 12

- The authors had to identify at what level of significance the variables should be deemed significant in the final multivariate model, which also needed to be assessed and presented together with an AOR and a 95% confidence interval.

This has been done on the multi variate model. Page 18

- Additionally, the authors had to disclose the precise categorization (their levels) of each independent variable measured in addition to stating the scales.

Results:

This has been added Page 11

- I'm not sure why the authors chose to use the median rather than the mean when reporting the age.

We chose the median over mean because the mean did not accurately reflect the central tendency

- The authors had to specify what low and high socioeconomic status meant when classifying socioeconomic status based on the wealth index in the method section before reporting here.

This has been added Page 7

- It is required to give the mean, plus or minus standard deviation, or the sub-total frequency of each domain of measurement scales when reporting sexual dysfunction in males and females. Additionally, for each outcome variable, the authors needed to indicate the 95% confidence interval.

This was reported using prevalence and 95% confidence intervals. Page 12

- I'll advise you to place the subheading factors related to sexual dysfunction before presenting the tables labelled "bivariate analysis of related factors (not adjusted) and "multivariate model (tables 3 and 4).

This has been done Pages 16 and 17

Discussion:

- The finding was well discussed by the authors. The authors were also required to expand on their discussion by including earlier prevalence research related to sexual dysfunction as well as further implications of the study for low-income nations like those in sub-Saharan Africa.

This has been done Page 26 and 27

- Although it appears that the authors are talking about qualitative findings in their discussion, I believe that they should concentrate on quantitative results instead because they evaluated the study in a quantitative manner, unless they felt the need to include qualitative data.

Conclusion and recommendation:

The study did not include any qualitative analyses – this was highlighted in the limitations

- The authors should have provided a more thorough summary of the main findings and recommendations based on those findings, particularly for those stakeholders working on behavioural changes related to HIV/AIDS and for concerned policymakers.

At last, the authors produced some excellent work, but they should pay particular attention to the methods section because the majority of its components are missing. This has been included Page 26

Attachment

Submitted filename: Response to review comments Oct 23.pdf

pone.0295224.s003.pdf (157.5KB, pdf)

Decision Letter 2

Habil Otanga

6 Nov 2023

PONE-D-22-24725R2A ‘hidden problem’: Nature, prevalence and factors associated with sexual dysfunction in persons living with HIV/AIDS in UgandaPLOS ONE

Dear Dr. Rukundo,

Thank you for submitting your manuscript to PLOS ONE. After careful consideration, we feel that it has merit but does not fully meet PLOS ONE’s publication criteria as it currently stands. Therefore, we invite you to submit a revised version of the manuscript that addresses the points raised during the review process.

==============================

ACADEMIC EDITOR: Deal with citations (both in-text and reference page) in line with journal requirements.==============================

Please submit your revised manuscript by Dec 21 2023 11:59PM. If you will need more time than this to complete your revisions, please reply to this message or contact the journal office at plosone@plos.org. When you're ready to submit your revision, log on to https://www.editorialmanager.com/pone/ and select the 'Submissions Needing Revision' folder to locate your manuscript file.

Please include the following items when submitting your revised manuscript:

  • A rebuttal letter that responds to each point raised by the academic editor and reviewer(s). You should upload this letter as a separate file labeled 'Response to Reviewers'.

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If you would like to make changes to your financial disclosure, please include your updated statement in your cover letter. Guidelines for resubmitting your figure files are available below the reviewer comments at the end of this letter.

If applicable, we recommend that you deposit your laboratory protocols in protocols.io to enhance the reproducibility of your results. Protocols.io assigns your protocol its own identifier (DOI) so that it can be cited independently in the future. For instructions see: https://journals.plos.org/plosone/s/submission-guidelines#loc-laboratory-protocols. Additionally, PLOS ONE offers an option for publishing peer-reviewed Lab Protocol articles, which describe protocols hosted on protocols.io. Read more information on sharing protocols at https://plos.org/protocols?utm_medium=editorial-email&utm_source=authorletters&utm_campaign=protocols.

We look forward to receiving your revised manuscript.

Kind regards,

Habil Otanga, Ph.D

Academic Editor

PLOS ONE

Journal Requirements:

Please review your reference list to ensure that it is complete and correct. If you have cited papers that have been retracted, please include the rationale for doing so in the manuscript text, or remove these references and replace them with relevant current references. Any changes to the reference list should be mentioned in the rebuttal letter that accompanies your revised manuscript. If you need to cite a retracted article, indicate the article’s retracted status in the References list and also include a citation and full reference for the retraction notice.

Additional Editor Comments:

Your work still suffers serious citation lapses. Go to the PLoS ONE webpage and find out how in-text and reference page citations are done.

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PLoS One. 2024 Mar 7;19(3):e0295224. doi: 10.1371/journal.pone.0295224.r006

Author response to Decision Letter 2


17 Nov 2023

The references have been revised and put in the Vancouver style. I hope they are now in the acceptable format. I have also corrected some punctuations and spelling mistakes. Thank you.

Decision Letter 3

Habil Otanga

20 Nov 2023

A ‘hidden problem’: Nature, prevalence and factors associated with sexual dysfunction in persons living with HIV/AIDS in Uganda

PONE-D-22-24725R3

Dear Dr. Godfrey Zari Rukundo,

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.

Within one week, you’ll receive an e-mail detailing the required amendments. When these have been addressed, you’ll receive a formal acceptance letter and your manuscript will be scheduled for publication.

An invoice for payment will follow shortly after the formal acceptance. To ensure an efficient process, please log into Editorial Manager at http://www.editorialmanager.com/pone/, click the 'Update My Information' link at the top of the page, and double check that your user information is up-to-date. If you have any billing related questions, please contact our Author Billing department directly at authorbilling@plos.org.

If your institution or institutions have a press office, please notify them about your upcoming paper to help maximize its impact. If they’ll be preparing press materials, please inform our press team as soon as possible -- no later than 48 hours after receiving the formal acceptance. Your manuscript will remain under strict press embargo until 2 pm Eastern Time on the date of publication. For more information, please contact onepress@plos.org.

Kind regards,

Habil Otanga, Ph.D

Academic Editor

PLOS ONE

Additional Editor Comments (optional):

Reviewers' comments:

Acceptance letter

Habil Otanga

27 Nov 2023

PONE-D-22-24725R3

A ‘hidden problem’: Nature, prevalence and factors associated with sexual dysfunction in persons living with HIV/AIDS in Uganda

Dear Dr. Rukundo:

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.

If your institution or institutions have a press office, please let them know about your upcoming paper now to help maximize its impact. If they'll be preparing press materials, please inform our press team within the next 48 hours. Your manuscript will remain under strict press embargo until 2 pm Eastern Time on the date of publication. For more information please contact onepress@plos.org.

If we can help with anything else, please email us at customercare@plos.org.

Thank you for submitting your work to PLOS ONE and supporting open access.

Kind regards,

PLOS ONE Editorial Office Staff

on behalf of

Dr. Habil Otanga

Academic Editor

PLOS ONE

Associated Data

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

    Supplementary Materials

    Attachment

    Submitted filename: Peer review comments on PONE-D-22-24725_.pdf

    pone.0295224.s001.pdf (639.2KB, pdf)
    Attachment

    Submitted filename: Response to Review comments.pdf

    pone.0295224.s002.pdf (491.4KB, pdf)
    Attachment

    Submitted filename: Response to review comments Oct 23.pdf

    pone.0295224.s003.pdf (157.5KB, pdf)

    Data Availability Statement

    All relevant data are within the paper.


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