Recurrent vulvovaginal candidosis among young women in south eastern Nigeria: the role of lifestyle and health-care practices

INTRODUCTION

Recurrent vulvovaginal candidosis (RVVC) can be a debilitating condition and remains a significant problem in women of child-bearing age. It is defined as four or more culture-proven symptomatic episodes of vulvovaginal candidosis (VVC) within a 12-month period. ^1–3 Epidemiological evidence shows that approximately 75% of all women will experience at least one episode of the infection during their life time ⁴ and about 40–50% of these women will experience one further episode. ^2,5 A small proportion of them (5–8%), will suffer recurrences. ^6–9 The highest incidence of RVVC is seen in women between the ages of 20 and 40 years, with a peak during the third and fourth decades of life. It is rarely seen during the prepubertal and postmenopausal period. ^10–15

Although the pathogenesis of RVVC is poorly understood, ¹⁶ several predisposing factors have been identified. These include: pregnancy, ¹⁷ diabetes mellitus, ^18,19 HIV infection, ²⁰ oral contraceptive pills ^1,2,14,17,21 and prolonged use of antibiotics. ²² However, a majority of women with RVVC do not have recognizable predisposing factors. ^6,10,23–25 Alterations in an individual's immune status and vaginal milieu (rise in pH and excess glycogen that has not been converted to lactic acid) caused by lifestyle and aberrant health-care practices have been hypothesized. ^12,26,27 Such lifestyles as frequent unprotected sex with multiple partners, ²⁸ frequent douching with assorted fluids, ²⁹ use of perfumed soap and tampons during menstruation, vaginal deodorants, diets high in sugar, ¹⁸ wearing tight-fitting nylon/synthetic underwear ³⁰ and chronic stress ³¹ have been inconclusively associated with RVVC.

Also aberrant health-care practices by individuals and the medical communities is another area of concern. Such practices as: self-diagnosis and treatment with over-the-counter (OTC) antifungal medications ^12,32 and antibiotics prescribed against recommendations (indiscriminate and prolonged use of antibiotics), under-treatment with antifungal agents, misdiagnosis, delay in treatment, inconsistencies in choices of drugs, dosage, duration of therapy and diagnostic protocols of medical practitioners have been implicated. ⁹

The adverse effect of RVVC on health, quality of life and economy of affected women is significant. Evidence-based studies have shown that women with this condition are more likely to suffer clinical depression, are less satisfied in life, have poor self-esteem and perceive their lives as being stressful. This is probably due to the adverse effects of RVVC on their physical and emotional wellbeing as well as the relationship with their partners. ^4,33 When recurrent, treatment for VVC can become a significant financial burden for the woman. In 1995, the total annual cost for treating candidal vaginitis in the USA was $1.8 billion with projected expenditures of $3.1 billion to be spent annually by 2014. ³⁴ Currently, treatment of RVVC based on USA and international guidelines cost women up to US$900 for six months with recurrence in some of them six months after cessation of therapy. ³⁵ Curbing the increased incidence of RVVC in our communities might help to restore and reinvigorate the lives of the affected women. This could be achieved by investigating and identifying possible risk factors for RVVC for a better understanding of its pathogenesis in order to improve the ability to treat and prevent its recurrence. ³⁶

The main purpose of this work therefore, was to study certain aspects of women's lifestyles and aberrant health-care practices in relation to RVVC with the aim of recommending preventive measures. The result could be of interest to any woman with RVVC as well as health-care providers managing the condition in our communities and similar communities in other parts of the world.

SUBJECTS AND METHODS

This was a cross-sectional multicentre case–control study conducted in seven health institutions (2 government and 5 private health facilities) within Uyo metropolis in south eastern Nigeria. These health facilities take care of the health needs of the entire population (about 1.5 million) of the metropolis with special attention to participants with sexually transmitted infections (STIs). Among the women who visited these health facilities for treatment of pelvic problems (pelvic pain, vaginal discharge, itching, sores and pain during coitus), 216 were recruited for the study. From the 216 recruited, 40 (18.5%) were excluded for conditions that could influence the result such as pregnancy, diabetes mellitus, HIV infection, current antibiotic therapy, immune-suppressive drugs, cancers, inappropriate age for the study, withdrawal from the study and improper completion of questionnaire.

Selection was based on their medical history and records which revealed that 86 (48.9%) of the actual 176 participants had RVVC. They were diagnosed with VVC by a physician at least four times during the previous 12 months, supported by positive vaginal swab culture. This formed the case group. Ninety participants were found to have suffered a single episode of VVC within the same period (culture proven), and hence were grouped as controls. The age of the participants ranged between 20 and 35 years. The study protocol was approved by research and ethics committee of the respective health institutions while informed consent was obtained from all participants.

Enrolled participants were given detailed history and lifestyle questionnaires to complete. The questionnaires were generally formulated to elicit information covering the last 12 months prior to the study period. They were asked to provide information on certain lifestyles and health-care practices that could precipitate persistence or re-infection. These included: information on sexual behaviours, use of contraceptive(s), demographics, dressing patterns, dietary habits and previous treatment protocols. Participants were informed that the questionnaire was about the risk factors for RVVC.

During the process of genital examination by the consulting physician, samples were taken from the participant's posterior vaginal fornix by use of a sterile cotton wool swab. Specimens were conveyed in McCartney bottles containing transport media and taken to the University of Uyo Teaching Hospital (UUTH) for microscopy, culture and sensitivity. The swabs were inoculated onto Sabouraud dextrose agar (40% [w/v] dextrose 1% [w/v], peptone 1.5% [w/v] agar pH 5.6) and incubated at 37°C for three days. The fungal swabs were also placed on Candida Chromagar (ChroMagar, Paris, France) and incubated at 37°C for 48 hours. Green colony-forming units were further evaluated for germ tube formation (evidence of C. albicans). Blood was also taken from participants to establish their HIV status.

STATISTICAL ANALYSIS

Frequencies and simple percentages were computed for categorical variables and descriptive statistics (reported as means ± standard deviation) for continuous variables. The chi-squared (for categorical variables) and independent sample t-test were used to compare differences between cases and control. Multiple logistic regression models were used to test the association between RVVC and its risk factors. Hence, based on this model, odd ratios (OR) and their corresponding 95% confidence interval (CI) with and without adjustment for potential confounders were estimated. All statistical computations were performed using SPSS 17.0 (SPSS Inc, Chicago, IL, USA). P < 0.05 was considered to be statistically significant.

RESULTS

DISCUSSION

In this study, we observed a high response rate from our study participants. A great number of them were in the lower education class, unemployed, single and predominantly of Igbo and Ibibio ethnicity. This level of enthusiasm for the study may have been indicative of their need for information and solution to a problem that has caused distress and unpleasant experiences during their reproductive lives. This assertion has been re-iterated by others in several anecdotal and clinic-based studies. ^4,9,37 Some of these women may have tried everything possible to alleviate their suffering and improve their quality of lives to no avail. ³⁸ This may explain why most of them practised frequent vaginal douching (63%), prolonged use of antibiotics (45%), self-diagnosis and treatment with OTC antifungal medications (34%) and alternatives to medical treatment (12%) than those in the control group.

According to the results of this study, participants who practised vaginal douching had a higher odds (OR_adjusted = 2.41, CI = 1.25–4.66) for RVVC. These findings support previous work in which douching was found to be a risk factor for RVVC and also disagree with others where no such relationship existed. ^1,2,29 Cultural beliefs, educational status, social class and health-care providers strongly influence douching practices. Douching is common in some cultures and is rare in others. ³⁹ A study population such as ours, where a greater proportion were unemployed (low socioeconomic class), single, in low educational class and with diverse ethnic backgrounds, there is likelihood of vaginal douching practices being common, which might alleviate symptoms. Douching behaviour is more common among black women of African descent ^40–42 and patients attending STI clinics than in others. ^43,44 These characteristics were present in our study population. Our findings also agreed with the previously assumed relationship between an individual's socioeconomic status, lifestyle, health-care practices and incident RVVC. ^45–47

Like previous studies ^26,30,48,49 our study showed a significant association between wearing of tight nylon/synthetic underwear and incidence of RVVC. Participants with this habit for ≥90% of the time in a year prior to the study recorded about five times the odds for incident RVVC (OR_adjusted = 4.76 95% CI = 2.28–9.95). A large body of evidence has shown that such fabrics can promote a moist warm environment in the perineal area, thereby creating a favourable atmosphere for overgrowth of yeast. ³⁸ However, other studies have reported contrasting results. ^5,50,51 Differences in some demographic characteristics and climatic variation could explain these conflicting observations, as women with a history of RVVC often report that they get more episodes of recurrence when travelling from a temperate zone to the tropics, where high humidity and high temperatures are believed to trigger RVVC attacks. ¹⁰

In our study, we also found that participants who self-diagnosed and took non-hospital-based treatments such as OTC antifungal medications had more than four times (OR_adjusted = 4.61 CI = 2.29–9.32) odds for RVVC episode. Previous studies with similar findings have shown that such self-diagnosis and treatment is most likely to be incorrect and imprecise, in terms of choice of drugs, dosage and duration of therapy and alternative antifungal medications for repeated and recalcitrant cases. ^37,52,53 However, others found no significant association. ^38,54

Similarly, non-institution of alternative antifungal treatment for repeated and recalcitrant cases increased the odds for incident RVVC to about five times (OR_adjusted = 4.84, CI = 2.94–15.91). This could have been due to the presence of non-C. albicans species which are naturally resistant or have low sensitivity to azole antifungal formulation usually used as the first-line treatment. ^10,55 Previous studies have shown that about 33% of women with RVVC have non-C. albicans species ⁵⁶ and Candida glabrata is the most common non-C. albicans species that contribute to these 33% recurrent cases in women. ⁵⁷ In our study participants, non-C. albicans species constituted about 16.3% cases of RVVC, with C. glabrata being the most common. This could have contributed to the higher incidence of RVVC in cases than control groups. In contrast to the above assertion, Mahmoudabadi et al. ⁵⁸ observed in their studies in Ahvaz, Iran, that all the Candida species (C. albicans and non-C. albicans) isolated were sensitive to the tested azole antifungal. ⁵⁸ The above disparities could be due to geographic, socioeconomic and ethnic variations in distribution and sensitivity of various Candida species. ⁵⁹

Other hypothesized risk factors with insignificant association include: sexual excesses previously shown to be significantly associated with incident RVVC in studies from different populations. ²⁸ However, a well-established body of literature document has provided facts that strengthen the result of our findings. ^2,20

More so, prolonged use of antibiotics, oral contraceptives, systemic steroids and dietary excesses were equally insignificantly associated with incidence of RVVC in this study. This disagrees with findings in other studies in which significant association was recorded. Spinillo et al. ²¹ reported in their studies that patients with vulvovaginal candidosis are two times more likely to have symptoms of the infection after a short course of antibiotic therapy, and three times after broad-spectrum antibiotics for 10–14 days, and such women will typically develop yeast vaginitis two weeks after antibiotics. ^21,23 At other places and time, similar significant relationships were recorded. ^2,14,33 Differences in the lifestyle and health-care practices serve as the possible explanation for such disparities.

Also, insignificant association between the use of oral contraceptive pills and incidence of RVVC in our study contradicts previous findings in other studies that recorded significant association. ^2,14,17,60 Ethnic, cultural practices and other confounding factors could alter the disease-triggering potential of any risk factor. This assertion has been the possible explanation for the higher incidence of RVVC recorded among African-Americans and this is attributed by researchers to the common usage of OTC (antifungal and antibacterial) medications and alternatives to medical treatment at higher rates than any other race. ^34,61,62 This could explain the high prevalence rate (48.9%) of RVVC recorded in this study.

Candida species recovered from vaginal swab fungal cultures showed that C. albicans was the most common species isolated in 83.7% of the participants in the case group. This was followed by non-C. albicans species in 16.3% of those in the same group, with C. glabrata being the most common of these. This is consistent with findings in similar studies. ^14,63,64 In contrast to our findings, Srujana et al. ⁶⁵ reported C. glabrata as the most common Candida species isolated, present in 50.4% of cases of vaginitis followed by C. albicans 35.1%. ⁵⁸ Jamilian et al. ⁶⁴ reported Candida dubliniensis as the most common (29.5%) in Iranian women. Also the diagnostic technique and expertise could affect the ability to properly identify the Candida species available. Variations may also reflect differences in sexual practices and environmental factors such as hygiene and nutrition. ⁵⁹ Again, the presence of non-C. albicans species in 16.3% of cases has underscored the need for culture and sensitivity in recurrent and recalcitrant infections. This will help identify the non-C. albicans species, which may not response to the normally used azole drugs to which the species are naturally resistant. ^10,33,56

Our study was strengthened by participants being examined and vaginal swabs taken for microscopy and culture. Also the diagnosis of RVVC was not only based on the participant's history, but previous medical records in the year prior to the study. This helped in eliminating error or inaccuracy of self-reported cases of RVVC and over-the-phone consultations. Nonetheless, ethnic and cultural differences were present in our study participants and this might have led to confounding which was not completely excluded.

CONCLUSION

The findings of this work show a significant association between certain lifestyle habits and aberrant health-care practices and incident RVVC among young women in south eastern Nigeria. This association has underscored the need for the introduction of preventive programmes aimed at educating young women about the risk factors that could precipitate RVVC. Such health education programmes could be carried out in schools, churches and other social and religious gatherings. We also recommend ‘train-the-trainer’ workshops to update the knowledge of the medical communities involved in the management of patients with RVVC on current management protocols. This might lead to a reduction in the incidence and morbidities associated with RVVC in communities within and outside of Nigeria.