Abstract
The relationships between hygiene, sexual behaviour and HIV infection are poorly understood. We examine these relationships in Indian truck drivers, a group at high risk for HIV infection. Truck drivers (n = 189) were recruited into an integrated HIV and hygiene Information Motivation (IM) programme. Sociodemographic characteristics, sexual and hygiene behaviour and HIV prevalence were determined. Multivariate logistic regression and linear generalized estimating equation models were utilized. At baseline, 2.1% of drivers were HIV infected and 34% who reported having contact with female sex workers (FSWs) had contact within the previous six months. Those who washed their hands postdefecation were less likely to report genital symptoms (OR 0.02; P = 0.01) and have sex with an FSW (OR [odds ratio] 0.21; P = 0.05). After an IM intervention, there were no changes in sexual risk-taking behaviour (coefficient −0.15 to −0.02; P = 0.13–0.75); however, hygiene behaviour improved from baseline (coefficient 0.09–0.31; P < 0.01 to P = 0.03). Personal hygiene habits, like handwashing, seem to be a modifiable behaviour after a modest intervention, whereas HIV risk-taking behaviour was not. The association between hygiene and HIV risk-taking suggests the need for further evaluation of the relationship and that of other hygiene practices in high-risk men in India.
INTRODUCTION
It is estimated that there are approximately five million truck drivers on the roads in India. 1 All research studies examining HIV or sexually transmitted infection (STI) prevalence of truck drivers in India have been cross-sectional in nature. 2–4 Several unpublished reports of truck drivers sampled from roadside stop areas and trucker unions suggest an HIV prevalence of 4–11%, 5,6 11–31 times higher than the HIV prevalence in the general Indian adult population. 7,8 Sentinel surveillance conducted by the high HIV burden Indian State of Andhra Pradesh 9 (population 83 million) has included all the subpopulations thought to be at high risk for HIV and STIs, but has not included truck drivers, 10 although preliminary data suggest that they are at increased risk for HIV and other STIs. 11 Thus, there is need for increased efforts to maintain and create novel HIV prevention programmes that are specific for this mobile population. 12 One recent study examined truck drivers’ sexual behaviour over time as part of an Information Motivation Behavioural change intervention with only modest benefit recorded by self-report, and participants were not tested for HIV. 13
There is increased interest in examining the relationship between general hygiene and HIV or other STIs in high-risk subpopulations. 14–18 For example, bathing, frequency of changing underwear and number of individuals sharing a bathroom, have suggested associations with prevalent HIV infection 15 ; however, this particular analysis did not control for other important covariates such as concurrent sexual partnering or use of condoms. There is also some evidence of an association between penile hygiene and HIV infection 19 and other STIs. 20–22 Causality has yet to be determined; however, results from circumcision studies confirm that the absence of foreskin and thus the subpreputial space decreases the risk of HIV acquisition. 23–25 Moreover, while there have been several studies demonstrating mixed associations of both general and vaginal hygiene and BV, 26–28 HIV 29–31 and other STIs, 32 there have been no studies to date on the relationship between general hygiene and HIV risk-taking behavior. Additionally, most studies suggest that a relationship between STI acquisition and penile hygiene has not taken into account the potential relationship between hygiene behaviours and other high-risk behaviours. 15,22 We sought to determine the relationship between general hygiene and HIV risk-taking behaviour in truck drivers and the potential effect of an Information Motivation (IM) intervention on these behaviours. If a strong relationship is found between these behaviours, hygiene interventions could potentially serve as new HIV bio-behavioural prevention interventions or as adjuncts to current behavioural interventions. If a link between hygiene and HIV risk-taking behaviours or HIV infection is not found, general hygiene remains an important prevention measure 33 for opportunistic 34–36 and non-opportunistic 37–39 infectious diseases in high-risk populations in India, where the vast majority who are infected are unaware of their HIV status.
METHODS
Study population and site
Truck drivers recruited into the study were at least 18 years in age, fluent Hindi or Telugu speakers and employed or contracted by Gati Limited, one of the largest transport companies in India. 40 Truck drivers were recruited by study staff directly from Gati’s main depot centre in Bowenpally, just outside of Hyderabad, the capital of Andhra Pradesh.
A physician and three counsellors with 10 years experience working with high-risk populations and HIV in this region were provided by the partnering International Center for Human Health Advancement (ICHHA). Prior to initiation of the study, all staff received extensive training over five days for standardization of the IM component. This included didactics on HIV and hygiene information and counselling protocols, as well as role-playing among counsellors and truck driver volunteers. Protocols were approved by the Institutional Review Boards at MediCiti Hospital, The Miriam Hospital and the University of Chicago.
Procedures
All study visits included a structured interviewer administered quantitative survey, followed by a 60 minute IM component, HIV pretest counselling, a physical exam and blood draw. After subjects met inclusion criteria and were consented, they were brought to the sound-proof, private counselling room located on the Gati premises. The survey and intervention were conducted there by the counsellor, and physical exam and blood draw in another area of the compound by the physician. All participants were tested for HIV-1 and HIV-2 using three sequential ELISAs (Genscreen HIV 1/2, Bio-Rad; Detect HIV, Adaltis; HIV Tri-Dot, Biotech Inc.) in accordance with national guidelines. Any study participants found to be HIV infected during or after the study period were offered treatment and follow-up by ICHHA, including antiretrovirals if indicated, with costs covered by Gati Limited and other private donors.
Participants were instructed by study staff to return for two additional study visits, one six months after the baseline visit and one six months after the second visit for a total of three study visits. In order to simulate potential application of future sustainable workplace HIV and hygiene prevention programmes in this setting, passive follow-up was conducted. There was neither active outreach nor a reminder given by staff other than for subjects who returned to the clinic area for other unrelated study concerns. Monetary reward for participation was not offered as part of this study. Because of high attrition for the second and third follow-up visits, company docking records were reviewed to examine concordance between clinic hours and docking schedules. Additionally, company and truck vendor employee rosters were reviewed by study staff to determine truck driver turnover among full-time and contracted drivers at the beginning and end of the recruitment period.
Survey
The survey instrument was based on HIV risk factor surveys used by our group previously 41 and was utilized primarily to assess changes in HIV risk-taking behaviour and hygiene practices. The majority of behavioural outcome items included responses ‘yes’, ‘no’ and ‘unknown’ to account for cross-cultural differences in subjective responses to larger Likert type scales. 42 Areas covered included sociodemographics, sexual behaviour and partnering patterns, HIV and STI transmission knowledge and assessment of personal hygiene practices. Personal hygiene practices included evaluation of washing hands and foods prior to consumption, washing hands postdefecation, assessment of frequently used potable water sources and type of toilet used and accessibility to it.
Intervention
From 2005 to 2007, a once-a-week workplace intervention was established at the Gati Limited truck depot outside of Hyderabad. The intervention incorporated information and motivation theory components from the Information-Motivation-Behavioural Skills approach to HIV prevention 43 to provide a uniquely integrative HIV and hygiene behavioural intervention. The information component of the intervention included an introduction to germ theory principles, setting the stage for hygiene and HIV transmission teaching. General hygiene information included discussion of five behavioural areas: cross-contamination, personal hygiene, household hygiene, temperature control and control of unsafe foods. 44 These were discussed within the infectious disease context of communicable disease prevention through sanitary practices. HIV information included previously tested HIV transmission and prevention teachings and materials used in previous studies in rural parts of the state. 41 Examining individual perceptions of risk and dispelling potential false assertions about risk and transmission were also a part of this exercise. Counsellors were trained specifically to integrate HIV prevention and hygiene improvement teaching, but were, however, also instructed to emphasize that HIV transmission cannot be prevented solely by improvements in general hygiene.
The semistructured motivation component of the intervention included individualized counselling on current HIV risk-taking behaviours, potential HIV preventive practices and exploring mechanisms to improve hygiene behaviours. This component was based upon the Theory for Reasoned Action. 45 Motivational counselling utilized subjects’ personal examples as well as hypothetical decisions made by peers to explore attitudes, prevention norms and locus of control. Examples included exploring potential methods of preventing HIV transmission to one's wife and children, and assuring hands are clean before ingestion of food in order to prevent missed days at work due to illness.
Analyses
The final analytical sample included all recruited males who reported having had sex at least once and who had complete data on all hygiene, outcome and control variables (n = 189). All statistical analyses were performed using STATA version 8.0 (StataSoft Corp., Austen, TX, USA). For all statistical tests, variables were considered significant at the P < 0.05 level.
Multivariate logistic regression models were utilized to predict determinants of each hygiene behaviour. Both bivariate and multivariate associations between hygiene behaviour variables and sexual behaviour outcomes were examined. Multivariate logistic regressions were performed with the hygiene behaviour of interest on each sexual behaviour outcome, controlling for age, income, marital status, number of children, urban residence, education, time spent away from home, other sexual behaviours and HIV knowledge.
Longitudinal analyses were conducted to evaluate the effects of the intervention during the first clinic visit on subsequent personal hygiene behaviour and sexual behaviour outcomes on the subset of individuals with follow-up visit data. Mean sample values were compared from the first visit to those from the second visit using t-tests. Linear probability models were generated using generalized estimating equations that captured data from all available follow-up visits. These multivariate models assessed the effect of visit number on outcome variables, while controlling for age, education, number of children and time away from home in the past year.
RESULTS
Baseline characteristics
Of the 235 truck drivers recruited into the study, 189 reported having sex at least once and had complete data on the HIV behavioural and hygiene variables, as well as control variables. Table 1 presents baseline sociodemographic characteristics for the analytical sample. With regards to HIV risk factors, 29.1% of truck drivers reported having sex with a commercial sex worker in their lifetime with nearly a third of those (11.1% of total sample) having sex with a commercial sex worker within the last six months. About 59.1% of men who had visited a female sex worker (FSW) reported ‘always’ using a condom with commercial sex workers in the past six months. At baseline, 2.1% of the sample was found to be HIV-infected, with 3.2% reporting a previous STI diagnosis and 8.5% reporting genital symptoms (burning urination, genital discharge, or genital ulcers/sores) in the past 12 months. Personal hygiene characteristics were generally reported at high levels among the population with 93.1% of the sample reporting washing of hands prior to eating, 94.7% reporting washing vegetables prior to consumption and 96.3% reporting washing hands postdefecation. These three variables were moderately correlated with one another (Crohnbach’s α = 0.47) and made into a scale to measure general hygiene.
Participant baseline characteristics (n = 189)
STI = sexually transmitted infections
Hygiene predictors and association of hygiene with HIV risk
Baseline subject characteristics associated with general hygiene can be found in Table 2. Truck drivers with lower income were less likely to wash hands prior to cooking (OR 0.97; P = 0.04) and postdefecation (OR 0.94; P = 0.01); however, this relationship was not found between income and washing vegetables before eating (OR 0.97; P = 0.31). Truck drivers who were married, however, were more likely to wash vegetables before eating (OR 11.8; P = 0.02) when compared with unmarried truck drivers. At baseline, truck drivers whose primary residence was in an urban area were more likely to wash vegetables before eating (OR 14.6; P = 0.02) and more likely to have heard of the germ theory (OR 15.15; P = 0.01) but demonstrated no difference in washing of hands prior to eating or postdefecation. There was no relationship between education or HIV knowledge and general hygiene behaviour.
Predictors of hygiene variables* (n = 189)
*Adjusted odds ratios; OR = odds ratios; CI = confidence interval
In bivariate analyses, multiple hygiene variables were associated with either HIV infection or HIV risk behaviour (Table 3). The hygiene variables that were associated with sexual risk-taking or HIV infection consistently demonstrated a relationship in the same direction: better hygiene related to decreased risk behaviour or correlates with HIV infection. In multivariate regression analysis, after adjusting for covariates significant at the 10% level in bivariate analysis, washing hands postdefecation was significantly associated only with reporting one of four genital symptoms (OR 0.02; P = 0.01). Washing vegetables before eating was also negatively associated with ever having sex with an FSW (OR 0.21; P = 0.05).
Relationship between hygiene and outcome variables*†
*All first visits
† n = 189
‡All t-Statistics are absolute
§ n = 22 for this outcome
STI = sexually transmitted infections; FSW = female sex workers
Loss to follow-up
During the two-year study period, there were 92 half-days of clinic operation. High attrition was seen at the second follow-up visit, as only 22 of the 143 sexually active subjects eligible for follow-up actually reported for the second study visit (15.4%). A comparison of the truck drivers who were lost to follow-up to those who presented for the second study visit did not demonstrate any differences in HIV risk-taking behaviour, genitourinary symptoms or time away from home. However, those who did not follow-up were more likely to have a lower monthly income (Rs. 3600 vs. Rs. 4100; P = 0.04). Review of company records comparing truck number to date of docking at the centre demonstrated that 17.3% of the truck/truck driver pairs did not dock 0–2 days before clinic operation over the two-year period. Additionally, 46% of drivers initially enrolled in the study were no longer employed by the company or the vendors contracted by the company at the end of the study period. The majority of the drivers in this category, 38% of the total, were drivers working for vendors who held contracts with the company.
Hygiene and HIV risk behaviour over time
There were no incident HIV infections over the follow-up period (Table 4). Additionally, there was no change in correlates of HIV risk behaviour when compared with baseline for report of genital symptoms, FSW in the last six months, condom use and number of sex partners in the last six months (coefficient −0.15 to −0.02; P = 0.13–0.75). This negative finding is in contrast to the significant changes in hygiene practices over time. All individual and scale level hygiene measurements demonstrated improvement from baseline (coefficient 0.09–0.31; P < 0.01 to P = 0.03).
Comparison of HIV risk factors, knowledge and hygiene at follow-up visits compared with baseline (n = 50)
Positive correlation designates positive association between variable of interest and follow-up visit
*This model controls for age, education, number of children and time away from home
† n = 49
‡ n = 48
FSW = female sex workers
DISCUSSION
This study was unique in examining sexual behaviour in high-risk Indian men in the context of other hygienic practices. The use of a workplace prevention intervention, a focus on hand and food washing hygiene as opposed to penile hygiene and longitudinal follow-up of this mobile population were distinguishing features of this study. There were multiple inverse associations between washing-related hygiene behaviours and risk practices increasing the likelihood of HIV infection, with two correlates of HIV infection – STI symptoms, and contact with FSW, remaining significant after multivariate analyses. Finally, an integrated HIV and hygiene IM intervention resulted in improvement in personal hygiene behaviour, but no changes in HIV risk-taking behaviour.
The finding that a one or two session information and motivation session did little to alter HIV risk-taking behaviour is consistent with previous findings. 13 Cognitive interventions have not been successful in some other at-risk male populations. 46 Behavioural interventions based on information and motivation may need multiple sessions over time to have an impact, 47 which may not be feasible or cost-effective in areas with limited resources or with highly mobile populations, and may not be robust in a population where unprotected sex is the norm, and awareness of HIV risk is low. Behavioural interventions, however, might be designed to address the role of alcohol use and sexual risk-taking among truckers, given the frequency of use. 48 Additionally, our findings that changes in behaviour related to hygiene may be affected after a one or two session IM programme could be useful if hygiene, and perhaps genital hygiene behaviour, is found to be related to risk of HIV infection. Our future work will attempt to develop skills building and other culturally appropriate interventions for this population.
More information is needed on what the specific hygiene practices and behaviours are that men at risk for HIV infection practice, although some prior associations between penile hygiene practices and HIV infection have been documented. 15,22 A study in Kisumu, Kenya reported a large protective effect against genital ulcer disease in those who cleansed the penis less than one hour after intercourse. The analytical model, however, did not control for high-risk sexual behaviour that might have confounded the relationship and affected the outcome. 22 For postcoital cleansing (one component of hygiene), the timing, type of cleansing, high variability of cleansing traits and substance used to clean are all poorly understood in this and other populations of uncircumcised men. 49 Surprisingly, there have been no studies of improving precoital genital hygiene and the effect of HIV infection. Determining whether viral or other unmeasured bacterial pathogens decrease the level of barrier protection in the foreskin, or perhaps increased inflammation from bacterial overgrowth allows for additional targets for HIV would be needed to develop a potential biological prevention product.
A question that remains is whether improved hygiene behaviour is causally related to decreases in HIV or STIs, or whether these behaviours are a more proximate measure of HIV/STI infection and are in fact related to other HIV risk-taking behaviours. A biologically plausible explanation can certainly be made for the relationship of penile hygiene and HIV or STI acquisition. However, it is difficult to explain this type of causality in the relationship between washing hands and HIV or STI acquisition. Washing hands, especially postdefecation, may be associated with other hygiene behaviours such as bathing or washing in the subpreputial area, which have been shown to be associated with less risk of HIV infection; however, this potential relationship was not explored as part of this study. It is also possible that these practices are associated with other HIV preventive practices that are also hygienic, such as avoiding FSWs, using condoms and avoiding multiple partners.
A major limitation of this study was the high loss to follow-up of truck drivers and limits the interpretation of the IM intervention. We determined that poor follow-up was primarily due to changes in employer and lack of congruency between delivery and clinic times. Despite this, there were no major differences between the participants that followed up with those that did not. Newer methods currently used for retention of this highly mobile population, such as cell phone contact and counselling, monthly meetings with lorry associations and coordination with other truck driver service providers in the state, were not used at the time of this study. Additionally, testing for STIs in this population may have been a more useful outcome measure given the lower than expected prevalence of HIV infection found in this study. A population-based study in a district in the state where this study was conducted demonstrated HSV-2 and Treponema pallidum seroprevalence rates of 8.2% and 7.3%, respectively, among truck drivers (Lalit Dandona, personal communication).
Overall, these study results (1) add to the growing evidence of a potential relationship in the chain between hygiene behaviour and HIV or STI prevalence and (2) suggest that hygiene behaviour may be modifiable to a greater extent than sexual risk-taking behaviour. The potential ease in modifying hygiene behaviours compared with sexual behaviour, the potential difficulties implementing circumcision as an HIV prevention strategy in India and the potential for improvements in hygiene to help with preventing other communicable diseases in those who are HIV infected make an integrated hygiene programme a potential prevention intervention worthy of future investigation.
Footnotes
ACKNOWLEDGEMENTS
The authors do not have a commercial or other association that might pose a conflict of interest. This study was supported by grants from the International Center for Human Health Advancement ICHHA 001-04 and Gati Limited. Dr Schneider was supported in part by T32-AI007438 from Tufts-New England Medical Center through the Lifespan/Tufts/Brown Center for AIDS Research. This work has been presented in part at the 4th International AIDS Society Conference on HIV Pathogenesis, Treatment and Prevention, 22–25 July 2007, Sydney Australia.
