Occurrence and Clinical Characteristics of Vaginitis among Women of Reproductive Age in Lagos, Nigeria
Chinedum Taahie Oparaugo1,2*, Bamidele Abiodun Iwalokun2,3,4, Francisca Obiageri Nwaokorie5, Nathaniel Adeleke Okunloye6, Adesegun Abiola Adesesan7, Idowu Olaide Edu-Muyideen7, Abimbola Modupe Adedeji8, Oliver Chukwujekwu Ezechi9, Mopelola Anotu Deji-Agboola2
1Biochemistry & Nutrition Department, Nigerian Institute of Medical Research, Lagos, Nigeria.
2Department of Medical Microbiology & Parasitology, Olabisi Onabanjo University, Ago-Iwoye, Nigeria.
3Molecular Biology & Biotechnology Department, Nigerian Institute of Medical Research, Lagos, Nigeria.
4Central Research Laboratory, Nigerian Institute of Medical Research, Lagos, Nigeria.
5Department of Medical Laboratory Science, College of Medicine, University of Lagos, Idi-Araba, Lagos, Nigeria.
6Department of Biochemistry, Faculty of Basic Medical Sciences, College of Health Sciences, Ladoke Akintola University of Technology, Ogbomoso, Nigeria.
7Microbiology Department, Nigerian Institute of Medical Research, Lagos, Nigeria.
8Monitoring & Evaluation Unit, Nigerian Institute of Medical Research, Lagos, Nigeria.
9Clinical Science Department, Nigerian Institute of Medical Research, Lagos, Nigeria.
DOI: 10.4236/arsci.2022.104009   PDF    HTML   XML   144 Downloads   989 Views  

Abstract

Background: Vaginitis is an important public health problem globally. It is associated with gynaecological and obstetric complications. Vulvovaginal candidiasis, bacterial vaginosis and trichomoniasis are mainly responsible for vaginitis. The aim of this study is to determine the occurrence, clinical characteristics and associated risk factors of vulvovaginal candidiasis and bacterial vaginosis among women of reproductive age attending Primary Health Care centres in Lagos Nigeria. Methods:This cross-sectional study recruited 258 women with genital complaints after obtaining their informed written consent between May 2017 and March 2018. Structured questionnaires were administered and high vaginal swabs were collected for laboratory examination. The results were analysed with descriptive statistics, chi-square and simple logistic regression. Results: Out of the 210 (81.4%) of the women with one or more vaginal infections, 105 (50.0%), 26 (12.4%) had bacterial vaginosis, and vulvovaginal candidiasis respectively while 78 (37.1%) had both vulvovaginal candidiasis and bacterial vaginosis. Only 1 (0.5%) participant had trichomoniasis and bacterial vaginosis. History of abortion and age below 25 years were associated with vulvovaginal candidiasis while pregnancy, history of miscarriage, age at first sexual activity and discharge were associated with bacterial vaginosis. Itching was associated with both vulvovaginal candidiasis and bacterial vaginosis. Conclusion: This study revealed vulvovaginal candidiasis and bacterial vaginosis as important cause of genital complaints among reproductive age women in Lagos. Health education, robust diagnosis and early treatment are needed in order to reduce the associated risk factors, disease burden and complications.

Share and Cite:

Oparaugo, C. , Iwalokun, B. , Nwaokorie, F. , Okunloye, N. , Adesesan, A. , Edu-Muyideen, I. , Adedeji, A. , Ezechi, O. and Deji-Agboola, M. (2022) Occurrence and Clinical Characteristics of Vaginitis among Women of Reproductive Age in Lagos, Nigeria. Advances in Reproductive Sciences, 10, 91-105. doi: 10.4236/arsci.2022.104009.

1. Introduction

Vaginitis is a global public health challenge among women of reproductive age. It is estimated that more than one million sexually transmitted infections (STIs) are acquired every day and there are 374 million new infections with one of four STIs: Chlamydia, gonorrhea, syphilis and trichomoniasis [1]. Vaginitis contributes to gynaecological morbidity and maternal mortality [2]. Some vaginal infections present with few or no symptoms but many have abnormal vaginal discharge, itching, burning sensation, irritation, and discomfort as common complaints [3]. Though there are many pathogenic agents observed in the vaginal microflora, candidiasis, bacterial vaginosis and trichomoniasis are responsible for majority of vaginal infections in women of reproductive age [4] [5].

Vulvovaginal candidiasis (VVC) is the major cause of fungal vaginitis [4] [6]. It is estimated to be the second most common cause of vaginitis after bacterial vaginosis [7]. Approximately 75% of all women experience at least one episode of VVC during their lives [8]. Candida albicans is the most frequent specie that causes VVC though other species like C. glabrata, C. dubliniensis, C. kefyr, C. pintolopesii, C. guilliermondii have been reported [9] [10]. Risk factors associated with VVC are sexual activity, recent antibiotic use, pregnancy and immunosuppression from such conditions as poorly controlled HIV infection or diabetes [11]. VVC is common in pregnancy and is associated with a significantly increased likelihood of low birth babies [12].

Bacterial vaginosis is a dysbiosis that results in reduction of vaginal lactobacilli leading to growth of anaerobic organisms like Gardnerella vaginalis, Prevotella spp, Mycoplasma hominis, Mobiluncus spp. [6] [13]. Although bacterial vaginosis is often sexually enhanced, it is not a sexually transmitted infection [13]. It is the most common cause of abnormal vaginal discharge in women of reproductive age [3] [4]. Up to half of the women with BV are asymptomatic [14] but for those that are symptomatic, the symptoms cause a lot of distress and impact their quality of life and relationships [15].

Trichomoniasis is caused by a parasitic protozoan, Trichomonas vaginalis, which infects the urogenital tract of females and males [16]. It is the most common non-viral sexually transmitted infection in the world [16]. It is estimated that 156 million people are infected worldwide yearly [1]. Although the main clinical manifestation of trichomoniasis is vaginitis, urethritis and prostatitis, the symptoms of the disease in women are yellowish-green frothy discharge, dysuria and the strawberry cervix which is recognized by punctuates haemorrhagic lesions [17].

Vaginal infections are associated with gynaecological morbidity and maternal mortality. They can cause pelvic inflammatory disease, tubal infertility, ectopic pregnancy, reproductive dysfunction and adverse birth outcomes such as premature rupture of membranes, premature labour, low birth weight, neonatal morbidity and mortality, post abortion or poor hysterectomy infection and enhanced predisposition to neoplastic transformation in cervical tissues. They also increase the risk of HIV and herpes simplex virus acquisition and transmission [16].

Vulvovaginal candidiasis, bacterial vaginosis and trichomoniasis are the main cause of vaginitis among women. In Nigeria, many studies on women with vaginitis focused only on one of the main causes of vaginitis [18] [19] [20] [21] [22]. In cases where there are co-infections, there is poor management of patients and this can lead to recurrence. Bacterial vaginosis recurrence leads to repeated presentations to hospitals or use of home-remedies that have not been proved scientifically [15]. Effective treatment requires accurate diagnosis of vaginitis. Therefore, this study was carried out to investigate the occurrence and clinical characteristics of vaginitis among women of reproductive age with genital complaints in Lagos Nigeria. This will help in the effective management of the infection at grass root level and prevent recurrence.

2. Methods

2.1. Study Settings

The study was conducted at Clinical Diagnostic Laboratory Unit, Nigerian Institute of Medical Research (NIMR) Lagos Nigeria. Ethical approval was obtained from NIMR Institutional Review Board and permission from Primary Health Care centre board.

2.2. Study Design and Population

This is a cross sectional study on reproductive age women (18 - 49 years) with genital complaints who attended twenty Primary Health Care centres in Lagos Nigeria between May 2017 and March 2018. Women who were on antibiotics one month before the date of sample collection were excluded from the study. The women were educated on the causes and prevention of vaginal infections, the study benefits and procedure. They were well informed about some gynaecological disorders that may occur among women of reproductive age such as abortion and post abortion sepsis, miscarriage and pelvic inflammatory syndrome. Participants were recruited from the women who signed consent form and waited for the sample to be collected. A pretested structured questionnaire was used to get information on age, marital status, occupation, educational status, residence, income per month, history of abortion (previous pregnancy terminated by inducement), pregnant now, history of miscarriage (previous pregnancy terminated spontaneously), life time number of sexual partners, age at first sexual activity. The case record files of participants were used to obtain the symptoms (discharge, lower abdominal pain, itching, foul odour from vagina).

2.3. Sample Collection and Processing

High vaginal swab (HVS) was collected using sterile disposable speculum and two swab sticks. One HVS sample was used for Gram stain, saline wet mount for Trichomonas vaginalis by direct light microscopy examination (×40) and assessment of bacterial vaginosis using the Amsel criteria. Presence of three out of the four Amsel criteria (vaginal discharge, vaginal pH greater than 4.5, positive whiff test, clue cell) was used in the diagnosis of bacterial vaginosis. The second HVS sample was inoculated in Sabouraud Dextrose Agar and incubated aerobically at 35˚C - 37˚C for 24 - 48 hours. Identification of Candida species was done based on morphology on wet mount microscopy (×40) and Gram staining while Germ tube test was used to identify Candida albicans [23].

2.4. Data Analysis

Data entry and analysis were done using Statistical Package for Social Sciences version 26. The variables of the study participants were described using frequencies, percentages and charts. Chi square and simple logistic regression were used to compare the vaginal infections with sociodemographic and clinical profile variables. A value of P ≤ 0.05 was considered statistically significant.

3. Result

A total of 258 women with genital complaints were recruited for the study. Only 210 (81.4%) of the women had one or more vaginal infections with 105 (50.0%) and 26 (12.4%) having bacterial vaginosis (BV) and vulvovaginal candidiasis (VVC) respectively. Also, 78 (37.1%) had BV and VVC while 1 (0.5%) had bacterial vaginosis and T. vaginalis (TV). None of the participants had the three infections. Further analysis comparing bacterial vaginosis and vulvovaginal candidiasis (BV versus VVC + BV) showed significant disparity in favour of bacterial vaginosis (P = 0.01) and also when the two groups (VVC + BV, VVC) were compared with the single case of BV and TV pooled with the BV only cases (P < 0.0001) (Figure 1).

The sociodemographic characteristics of the reproductive age women with vulvovaginal candidiasis and bacterial vaginosis are shown in Table 1. Infection with VVC was highest (57.1%) in age groups less than 20 years and 21 - 25 years (P = 0.042), followed by 47.6% and 40.8% in 41 - 45 and 31 - 35 years age group

Figure 1. Prevalence and vagintis profile among the studied women. BV, Bacterial Vaginosis; VVC = Vulvovaginal Candidasis; TV = Trichomoniasis; @Disparity in % occurrence of vaginitis types with the only BV + TV pooled with BV only cases.

Table 1. Sociodemographic characteristics of reproductive aged women with vulvovaginal candidiasis and bacterial vaginosis.

respectively. Also, bacterial vaginosis infection was high (81.8%) in 36 - 40 years age group followed by 76.2% in 21 - 25 and 41 - 45 years age group. Co-infection of VVC with bacterial vaginosis was more (47.6%) in participants less than 20 years but there was no significant difference (P = 0.178). All the participants that were divorced, separated and widowed had bacterial vaginosis compared with 70.6% of the married women with bacterial vaginosis but there was no significant association (P = 0.574). All the women that were divorced had both VVC and bacterial vaginosis, however no significant difference was observed (P = 0.115). Majority of the participants were civil servants (42.6%). Their educational status revealed that 146 (56.6%) of the women attended tertiary institution while 213 (82.6%) were urban dwellers. More than half (58.1%) of the women earned N 10,000 to N 50,000 monthly.

Table 2 shows the association of clinical profiles of reproductive age women with vulvovaginal candidiasis and bacterial vaginosis. Eleven (25.6%) of the participants with history of abortion had VVC compared with 93 (43.3%) that had no abortion (P = 0.031). Almost half (49.2%) of the women that were pregnant had VVC. Pregnancy was associated with bacterial vaginosis (P = 0.013). The women that were not sure of pregnancy were removed from the association between state of pregnancy and infection. Women who were pregnant had 94% increased risk of having VVC (OR = 1.94, 95% CI: 1.03, 3.66), 37% increased risk of co-infection with VVC and bacterial vaginosis (OR = 1.37, 95% CI: 0.71, 2.64; P = 0.354) but the risk estimate is not statistically significant. Majority (90.9%) of the women with history of miscarriage had bacterial vaginosis compared with 164 (69.5%) without bacterial vaginosis (P = 0.034). The only participant that

Table 2. Association of clinical profiles of reproductive age women with vulvovaginal candidiasis and bacterial vaginosis.

had first sexual activity before 10 years had both VVC and bacterial vaginosis and there was significant association with BV (P = 0.020). Out of 127 (49.2%) of the women with discharge, 55 (43.3%) had VVC, 121 (95.3%) had bacterial vaginosis (P < 0.001). Only 24 (9.3%) women had lower abdominal pain with 10 (41.7%) having VVC, 15 (62.5%) having bacterial vaginosis but there was no significant association. Majority 13 (61.9%) of the women with itching had VVC (P = 0.035) while 33.3% had bacterial vaginosis (P < 0.001). Eight (53.3%) and 12(80.0%) of the women with foul odour from vagina had VVC and bacterial vaginosis respectively. However, there was no significant difference. Only 17(6.6%) participants had discharge and itching with majority, 15(88.2%) having bacterial vaginosis.

Further analysis showed that 44 (17.1%) of the reproductive age women had no symptoms, 37 (14.3%) had no symptom and no infection, 7 (2.7%) had infection without symptoms, 11 (4.3%) had symptoms without infection while 203 (78.7%) had both symptoms and infection. There is significant association between symptoms and infections (P = 0001). Infection with T. vaginalis was found only in the 31 - 35 years age group.

4. Discussion

Our study showed that 81.4% of the women had one or more vaginal infections with VVC, bacterial vaginosis or T. vaginalis. This is higher than reports from Osogbo south western Nigeria (76%) [24], Ghana (56.4%) [25], Cameroon (52.44%) [26], Nepal (33.5%) [27], Yemen (37.6%) [7], Ethiopia (15.4%) [4], Kerkuk-Iraq (13.2%) [28]. However, it is lower compared to reports from India (89.0%) [29].

The result revealed that 12.4% of the participants had VVC only. This is lower than reports from Ghana (36.5%) [25], Nepal (40.3%) [27]. It is higher than reports from Yemen (6.6%) [7], Ethiopia (8.3%) [4], Iran (26.2%) [9], India (37.3%) [30]. In Nigeria, higher prevalence of VVC has been observed in different populations. In Ibadan Oyo state, prevalence of 30.9% was reported [31] while prevalence of 30%, 14%, 35.25%, 25.7% were reported in Port Harcourt, Abuja, Zaria, Yenagoa [22] [32] [33] [34] respectively. The differences observed can be as a result of type of study population, changes in vaginal flora and sexual activity.

In this study, women less than 20 and 21 - 25 years age group had the highest frequency (57.1%) of VVC. Uzoh et al. [35] reported 20 - 29 years age group as having highest frequency (38.5%) in Asaba Nigeria. However, Wariso et al. [22] reported 40% as highest frequency in age group 26 - 30 years in Southern Nigeria while Sahoo et al. [36] reported 39.2% among 26 - 35 years age group. These variations may be attributed to hormonal and physiological variations. In this study, there was statistical significance between age and VVC occurrence (P = 0.042). Hedayati et al. [10], Konadu et al. [25], Aalei and Touhidi [37] reported no significance.

The study showed that 49.2% of the pregnant women had VVC. Some studies from Nigeria have reported lower prevalence of 41% [38], 40% [35], 38% [12]. Mucci et al. [39] and Sangre et al. [40] reported 24.8% and 22.7% from Argentina and Burkina Faso respectively. However, Akinbami et al. [41] reported a higher prevalence of 60% in Ogbomosho South West Nigeria. These observed differences may be as a result of diet, hygiene and sexual practices.

History of abortion and miscarriage was associated with VVC (P = 0.031) and bacterial vaginosis (P = 0.034) respectively. In a study by Konadu et al. [25], VVC and bacterial vaginosis were not associated with history of spontaneous abortion.

The study showed that bacterial vaginosis was the commonest cause of vaginal infection followed by VVC. This is consistent with findings from Tanzania, Yemen, South western Nigeria, Birgunj Nepal, Sudan [3] [7] [24] [27] [42]. Studies from Ethiopia, India, Brazil, observed that VVC was the commonest cause of vaginal infection [4] [5] [6]. The differences may be as a result of variations in method, study population, hygiene practices and educational status. In this study, 50.0% of the women had bacterial vaginosis only. This is higher than 27.2% reported among reproductive aged women seeking Primary Health Care in Yemen [7]. Bonneton et al. [43] also reported a lower prevalence of 18.6% in Senegal. Different studies in Nigeria have reported lower prevalence of bacterial vaginosis, 16.6% [20], 27% [21], 38% [23]. However, Udenze et al. [44] reported 74% while Enitan et al. [19] reported 65% and 85% prevalence by Nugent’s criteria and culture respectively in Ilara, Ogun state Nigeria. The observed variations in prevalence may be due to differences in study populations and techniques used for the test.

The prevalence of T. vaginalis (0.5%) is in agreement with reports from Sudan [42] but in contrast with the studies in Nepal where there was no positive case [27]. Higher prevalence of trichomoniasis have been reported in Kanchipuram India (4.0%) [45], Kogi state Nigeria (5.1%) [18] and Ibadan south western Nigeria (1.5%) [46]. T. vaginalis was found only in 31 - 35 years age group. Idakwo et al. [18] reported higher prevalence in age groups of 21 - 30 and 31 - 40 years while Tine et al. [47] reported 31 - 45 years age group. Studies from Egypt [48], Iran [49] reported that women in age group 25 - 45 years are at higher risk of T. vaginalis infection. There was no co-infection between VVC and T. vaginalis. This is in agreement with report by Idakwo et al. [18]. However, Mascarenhas et al. [6], Pondei et al. [34] reported co-infections by Candida species and T. vaginalis. Differences may be due to variations in methodology, level of awareness and poor personal hygiene. The low T. vaginalis prevalence could be as a result of the wet mount method used in detection. Studies by Adjei et al. [50], Squire et al. [51], showed that direct wet-mount microscopy has low sensitivity in detecting T. vaginalis.

The commonest symptom for patients with bacterial vaginosis was vaginal discharge (95.3%). Majigo et al. [3] and Enitan et al. [19] reported vaginal discharge as the commonest symptom. There was a significant association between discharge and bacterial vaginosis (P < 0.001). This finding agrees with previous study by Ranjit et al. [52] in Nepal and Garba et al. [53] in North Central Nigeria. Itching was also statistically significant in patients with bacterial vaginosis (<0.001) but study by Ranjit et al. [52] registered no significant relationship between itching and bacterial vaginosis. However, itching was the commonest symptom in VVC patients (61.9%) [P = 0.035]. Hedayati et al. [10], Karmastaji et al. [54] reported erythema with itching in VVC patients as the commonest symptoms. Abdul-Aziz et al. [7] reported significant relationship between vaginal itching and VVC among reproductive aged women in Yemen though Habibipour [55] did not find any significant correlation. In this investigation, pregnancy was associated with bacterial vaginosis but study by Apalata et al. [56] reported no significant association.

The study has some limitations. Detection of T. vaginalis by wet mount may have reduced the actual prevalence. Other causes of abnormal discharge were not detected in the study. Some diseases that make VVC to thrive were not taken into consideration.

5. Conclusion

Findings from this study reveal high burden of bacterial vaginosis and vulvovaginal candidiasis among reproductive age women with history of abortion and miscarriage as potential risk factors. There is need for strategy that will improve reproductive health education especially among women of age 25 years and below.

Conflicts of Interest

The authors declare no conflicts of interest regarding the publication of this paper.

References

[1] World Health Organization (2021) Sexually Transmitted Infections (STIs). Key Facts. World Health Organization, Geneva.
[2] World Health Organization (2013) Report on Global Sexually Transmitted Infection Surveillance. World Health Organization, Geneva.
[3] Majigo, M.V., Kashindye, P., Mtulo, Z. and Joachim, A. (2021) Bacterial Vaginosis, the Leading Cause of Genital Discharge among Women Presenting with Vaginal Infection in Dares Salaam, Tanzania. African Health Sciences, 21, 531-537.
https://doi.org/10.4314/ahs.v21i2.7
[4] Mulu, W., Yimer, M., Zenebe, Y. and Abera, B. (2015) Common Causes of Vaginal Infections and Antibiotic Susceptibility of Aerobic Bacterial Isolates in Women of Reproductive Age Attending at Felegehiwot Referral Hospital , Ethiopia: A Cross Sectional Study. BMC Women’s Health, 15, Article No. 42.
https://doi.org/10.1186/s12905-015-0197-y
[5] Narayankhedkar, A., Hodiwala, A. and Mane, A. (2015) Clinicoetiological Characterization of Infectious Vaginitis amongst Women of Reproductive Age Group from Navi Mumbai, India. Journal of Sexually Transmitted Diseases, 2015, Article ID: 817092.
https://doi.org/10.1155/2015/817092
[6] Mascarenhas, R.E.M., Machado, M.S.C., Borges da Costa e Silva, B.F., Pimentel, R.F.W., Ferreira, T.T., Leoni, F.M.S. and Grassi, M.F.R. (2012) Prevalence and Risk Factors for Bacterial Vaginosis and Other Vulvovaginitis in a Population of Sexually Active Adolescents from Salvador, Bahia, Brazil. Infectious Diseases in Obstetrics and Gynecology, 2012, Article ID: 378640.
https://doi.org/10.1155/2012/378640
[7] Abdul-Aziz, M., Mahdy, A.K., Abdul-Ghani, R., Alhilali, N.A., Al-Mujahed, L.K.A., Alabsi, S.A., Al-Shawish, F.A.M., Alsarari, N.J.M., Bamashmos, W., Abdulwali, S.J.H., Al Karawani, M. and Almikhlafy, A.A. (2019) Bacterial vaginosis, Vulvovaginal candidiasis and Trichomonal vaginitis among Reproductive-Aged Women Seeking Primary Healthcare in Sana’a City, Yemen. BMC Infectious Diseases, 19, Article No. 879.
https://doi.org/10.1186/s12879-019-4549-3
[8] Zullo, M.A., Schiavi, M.C., Di Pinto, A., Prata, G., Scudo, M., Luffarelli, P. and Oliva, C. (2020) Efficacy and Safety of Oral Administration of a Product Based on Hydroxytyrosol as Preventive Therapy for Recurrent Vulvo-Vaginal Candidosis: A Prospective Observational Pilot Study. European Review for Medical and Pharmacological Sciences, 24, 7427–7432.
[9] Arastehfar, A., Kargar, M.L., Mohammadi, S.R., Roudbary, M., Ghods, N., Haghighi, L., Daneshnia, F., Tavakoli, M., Jafarzadeh, J., Hedayati, M.T., Wang, H., Fang, W., Carvalho, A., Llkit, M., Perlin, D.S. and Lass-Florl, C. (2021) A High Rate of Recurrent Vulvovaginal Candidiasis and Therapeutic Failure of Azole Derivatives among Iranian Women. Frontiers in Microbiology, 12, Article ID: 655069.
https://doi.org/10.3389/fmicb.2021.655069
[10] Hedayati, M.T., Taheri, Z., Galinimoghadam, T., Aghili SR Cherati, J.Y. and Mosayebi, E. (2015) Isolation of Different Species of Candida in Patients with Vulvovaginal Candidiasis from Sari Iran. Jundishapur Journal of Microbiology, 8, Article ID: e15992.
https://doi.org/10.5812/jjm.8(4)2015.15992
[11] Nwadioha, S.I., Egah, D.Z., Alao, O.O., Iheanacho, E. (2010) Risk Factors for Vaginal Candidiasis among Women Attending Primary Health Care Centres of Jos Nigeria. Journal of Clinical Medicine and Research, 2, 110-113.
[12] Sule-Odu, A.O., Akadri, A.A., Oluwole, A.A., Osinupebi, O.A., Andu, B.A., Akiseku, A.K. and Lawal, A.I. (2020) Vaginal Candida Infection in Pregnancy and Its Implications for Fetal Well-Being. African Journal of Reproductive Health, 24, 33-40.
[13] Chavoustie, S.E., Eder, S.E., Koltun, W.D., Lemon, T.R., Mitchell, C., Nyirjesy, P., Sobel, J.D., Sobel, R. and Villanueva, R. (2017) Experts Explore the State of Bacterial Vaginosis and the Unmet Needs Facing Women and Providers. International Journal of Gynecology & Obstetrics, 137, 107-109.
https://doi.org/10.1002/ijgo.12114
[14] Klebanoff, M.A., Schwebke, J.R., Zhang, J., Nansel, T.R., Yu, K.F. and Andrews, W.W. (2004) Vulvovaginal Symptoms in Women with Bacterial Vaginosis. Obstetrics & Gynecology, 104, 267-272.
https://doi.org/10.1097/01.AOG.0000134783.98382.b0
[15] Bilardi, J., Walker, S., Mooney-Somers, J., Temple-Smith, M., McNair, R., Bellhouse, C., Fairley, C., Chen, M. and Bradshaw, C. (2016) Women’s Management of Recurrent Bacterial Vaginosis and Experiences of Clinical Care: A Qualitative Study. PLOS ONE, 11, Article ID: e0151794.
https://doi.org/10.1371/journal.pone.0151794
[16] Kissinger, P. (2015) Trichomonas vaginalis: A Review of Epidemiologic, Clinical and Treatment Issues. BMC Infectious Diseases, 15, Article No. 307.
https://doi.org/10.1186/s12879-015-1055-0
[17] Arbabi, M., Delavari, M., Fakhrieh-Rashan, Z. and Hooshyar, H. (2018). Review of Trichomonas vaginalis in Iran Based on Epidemiological Situation. Journal of Reproduction & Infertility, 19, 82-88.
[18] Idakwo, J., Yaro, C.A., Akoh, Q.P. and Raji, R.O. (2020) A Study of Trichomonas vaginalis and Risk Factors in Women of Reproductive Age Attending Health Facilities in Okene Metropolis, Kogi State, Nigeria. Journal of Clinical and Scientific Research, 9, 213-217.
[19] Enitan, S.S., Ihongbe, J.C., Ochei, J.O., Otuneme, G.O., Itodo, G.E. and Kalejaiye, O.S. (2018) Prevalence of Bacterial Vaginosis and Associated Risk Factors among Non-Pregnant Women in Ilara Community of Ogun State, Nigeria. International Journal of Public Health Research, 6, 35-46.
[20] Abdullateef, R.M., Ijaiya, M.A., Abayomi, F., Adeniran, A.S. and Idris, H. (2017) Bacterial Vaginosis: Prevalence and Associated Risk Factors among Non-Pregnant Women of Reproductive Age Attending a Nigerian Tertiary Hospital. Malawi Medical Journal, 29, 290-293.
https://doi.org/10.4314/mmj.v29i4.2
[21] Edet, U.O., Mboto, C.I., Mbim, E.N., George, U.E., Umego, C.F. and Okon, J. (2017) Prevalence of Bacterial Vaginosis amongst Female Students of the University of Calabar, Calabar, Cross River State. Asian Journal of Research in Medical and Pharmaceutical Sciences, 2, 1-8.
https://doi.org/10.9734/AJRIMPS/2017/36127
[22] Wariso, K.T., Oboro, I.L. and Igumna, J.A. (2017) Prevalence and Clinical Manifestations of Candidiasis among Patients with Vulvovaginitis in a Tertiary Institution in Southern Nigeria. Cross River Journal of Medicine, 1, 10-17.
[23] Cheesbrough, M. (2000) District Laboratory Practice in Tropical Countries Part 2. Cambridge University Press, Cambridge, 38, 92, 244.
[24] Olowe, O.A., Makanjuola, O.B., Olowe, R. and Adekanle, D.A. (2014) Prevalence of Vulvovaginal candidiasis, Trichomoniasis and Bacterial vaginosis among Pregnant Women Receiving Antenatal Care in South Western Nigeria. European Journal of Microbiology and Immunology, 4, 193-197.
https://doi.org/10.1556/EUJMI-D-14-00027
[25] Konadu, D.G., Owusu-Ofori, A., Yidana, Z., Boadu, F., Iddrisu, L.F., Adu-Gyasi, D., Dosoo, D., Awuley, R.L., Owusu-Agyei, S. and Asante, K.P. (2019) Prevalence of Vulvovaginal candidiasis, Bacterial vaginosis and Trichomoniasis in Pregnant Women Attending Antenatal Clinic in the Middle Belt of Ghana. BMC Pregnancy and Childbirth, 19, Article No. 341.
https://doi.org/10.1186/s12884-019-2488-z
[26] Payne, V.K., Cécile, T.T.F., Cedric, Y., Nadia, N.A.C. and Jose, O. (2020) Risk Factors Associated with Prevalence of Candida albicans, Gardnerella vaginalis, and Trichomonas vaginalis among Women at the District Hospital of Dschang, West Region, Cameroon. International Journal of Microbiology, 2020, Article ID: 8841709.
https://doi.org/10.1155/2020/8841709
[27] Gupta, R.S., Bhargav, D. and Deep, J.P. (2021) Common Types of Vaginitis (Bacterial vaginosis, Vulvovaginal candidiasis, Trichomoniasis) and Their Association with Urinary Tract Infection among Women Visiting NMCTH, Birgunj. International Journal of Current Microbiology and Applied Sciences, 10, 996-1010.
https://doi.org/10.20546/ijcmas.2021.1001.121
[28] Kadir, M.A., Sulymaz, M.A., Dawood, I.S. Cambridge Shams-Eldin, S. (2014) Trichomonas Vaginalis and Associated Microorganisms in Women with Vaginal Discharge in Kerkuk-Iraq. Ankara Medical Journal, 14, 91-99.
[29] Masand, D.L., Patel, J. and Gupta, S. (2015) Utility of Microbiological Profile of Symptomatic Vaginal Discharge in Rural Women of Reproductive Age Group. Journal of Clinical and Diagnostic Research, 9, QC04-QC07.
https://doi.org/10.7860/JCDR/2015/12161.5623
[30] Swaminathan, K.R., Devi, M., Gerald, S., Prakesh, S.C. and Thomas, B.M. (2017) Prevalence of Vulvovaginal Candidiasis in the Women of the Reproductive Age in Rural India. International Journal of Clinical Obstetrics and Gynaecology, 1, 37-39.
[31] Makanjuola, O., Adedokun, B., Fayemiwo, S. and Bakare, R. (2016) Correlates of Vulvovaginal Candidiasis among Attendees of a Special Treatment Clinic in Nigeria. International STD Research & Reviews, 4, 1-7.
https://doi.org/10.9734/ISRR/2016/27811
[32] Emeribe, A.U., Nasir, I.A., Onyia, J. and Ifunanya, A.L. (2015) Prevalence of Vulvovaginal Candidiasis among Non Pregnant Women Attending Tertiary Health Care Facility in Abuja Nigeria. Research and Reports in Tropical Medicine, 6, 37-42.
https://doi.org/10.2147/RRTM.S82984
[33] Akafyi, D.E., Oko, J.O., Umar, M., Obafemi, A. and Michael, R. (2016) Prevalence of Bacterial, Trichomonas and Candidal Vaginosis among Females in Angwan-Fulani, Palladan in Zaria, Nigeria. Journal of Applied Life Sciences International, 5, 1-6.
https://doi.org/10.9734/JALSI/2016/25649
[34] Pondei, K., Jeremiah, I., Lawani, E. and Nsikak, E. (2017) The Prevalence of Symptomatic Vulvovaginal Candidiasis and Trichomonas Vaginalis Infection and Associated Risk Factors among Women in the Niger Delta Region of Nigeria. International STD Research & Reviews, 5, 1-10.
https://doi.org/10.9734/ISRR/2017/32057
[35] Uzoh, C.V., Iheukwumere, I.H., Umezuruike, K.C. and Onyewenjo, S.C. (2017) Prevalence of Candida Albicans among Women Attending Federal Medical Centre Asaba, Delta State, Nigeria. International Journal of Biochemistry and Biotechnology, 6, 735-739.
[36] Sahoo, S., Mohanty, I., Parida, B. and Patnaik, S. (2018) Prevalence of Vulvovaginal Candidiasis in Sexually Active Females with Antifungal Susceptibility Patterns of the Isolates. International Journal of Clinical and Biomedical Research, 4, 38-41.
[37] Aalei, B.S.H. and Touhidi, A. (2000) Prevalence of Candida Vaginitis among Symptomatic Patients in Kerman. The Journal of Qazvin University of Medical Sciences, 4, 42-48.
[38] Ibrahim, S.M., Bukar, M., Mohammed, Y., Audu, B.M. and Ibrahim, H.M. (2013) Prevalence of Vaginal Candidiasis among Pregnant Women with Abnormal Vaginal Discharge in Maiduguri. Nigerian Journal of Medicine, 22, 138-142.
[39] Mucci, M.J., Cuestas, M.L., Landanburu, M.F. and Mujica, M.T. (2017) Prevalence of Candida albicans, Candida dubliniensis and Candida africana in Pregnant Women Suffering from Vulvovaginal Candidiasis in Argentina. Revista Iberoamericana de Micología, 34, 72-76.
https://doi.org/10.1016/j.riam.2016.09.001
[40] Sangare, I., Sirima, C., Bamba, S., ZidaA, Cissé, M., Bazié, W.W., Sanou, S., Dao, B., Menan, H. and Guiguemdé, R.T. (2018) Prevalence of Vulvovaginal Candidiasis in Pregnancy at Three Health Centers in Burkina Faso. Journal de Mycologie Médicale, 28, 186-192
https://doi.org/10.1016/j.mycmed.2017.08.006
[41] Akinbami, N.A., Babalola, G.O., Shittu, M.O., Tijani, A.M. and Adekola, S.A. (2015) Detection and Epidemiology of Vulvovaginal Candidiasis among Asymptomatic Pregnant Women Attending a Tertiary Hospital in Ogbomoso, Nigeria. International Journal of Biomedical Research, 6, 518-523.
https://doi.org/10.7439/ijbr.v6i7.2242
[42] Abdelaziz, Z.A., Ibrahim, M.E., Bilal, N.E. and Hamid, M.E. (2014) Vaginal Infections among Pregnant Women at Omdurman Maternity Hospital in Khartoum, Sudan. The Journal of Infection in Developing Countries, 8, 490-497.
https://doi.org/10.3855/jidc.3197
[43] Bonneton, M., Huynh, B., Seck, A., Bercion, R., Sarr, F.D., Delarocque-Astagneau, E. and Vray, M. (2021) Bacterial Vaginosis and Other Infections in Pregnant Women in Senegal. BMC Infectious Diseases, 21, Article No. 1090.
https://doi.org/10.1186/s12879-021-06767-4
[44] Udenze, C.L., Achi, O.K., Obeagu, E.I. and Elemchukwu, Q. (2014) Prevalence of bacterial Vaginosis among Female Students of Michael Okpara University of Agriculture Umudike, Abia State, Nigeria. IOSR Journal of Pharmacy and Biological Sciences, 9, 39-52.
https://doi.org/10.9790/3008-09523952
[45] Nagajothi, A. and Muthulakshmi, K. (2018). Prevalence of Trichomonas vaginalis Using Parasitological Methods in Kanchipuram. International Journal of Scientific Research, 7, 63-64.
[46] Okonko, I.O., Akinpelu, A.O. and Okerentugba, P.O. (2012) Prevalence of Sexually Transmitted Infections (STIs) among Attendees of AFRH Centre in Ibadan, Southwestern Nigeria. Middle-East J Scientific Research, 11, 24-31.
[47] Tine, R.C., Sylla, K., Ka, R., Dia, L., Sow, D., Lelo, S., Diallo, K., Faye, B., Dieng, T., Ndour, C.T. and Sow, A.Y. (2019) A Study of Trichomonas vaginalis Infection and Correlates in Women with Vaginal Discharge Referred at Fann Teaching Hospital in Senegal. Journal of Parasitology Research, 2019, Article ID: 2069672.
https://doi.org/10.1155/2019/2069672
[48] Mahmoud, A., Sherif, N.A., Abdella, R., El-Genedy, A.R., El Kateb, A.Y. and Askalani, A.N. (2015) Prevalence of Trichomonas vaginalis Infection among Egyptian Women Using Culture and Latex Agglutination: Cross-Sectional Study. BMC Women’s Health, 15, Article No. 7.
https://doi.org/10.1186/s12905-015-0169-2
[49] Azambakhtiar, A., Nikmanesh, B., Rezaeian, M., Dashti, N., Safari, F. and Zarebavani, M. (2018) The Prevalence of Trichomoniasis in Women Referred to Clinical Centers in South of Tehran, Iran during 2015-2016. Iranian Journal of Parasitology, 13, 108-113.
[50] Adjei, C., Boateng, R., Dompreh, A., Okyere, B. and Owiredu, E. (2019) Prevalence and the Evaluation of Culture, Wet Mount, and ELISA Methods for the Diagnosis of Trichomonas vaginalis Infection among Ghanaian Women Using Urine and Vaginal Specimens. Tropical Medicine and Health, 47, Article No. 33.
https://doi.org/10.1186/s41182-019-0162-9
[51] Squire, D.S., Lymbery, A.J., Walters, J., Ahmed, H., Asmah, R.H., Thompson, R.C.A. (2019) Trichomonas vaginalis Infection in Southern Ghana: Clinical Signs Associated with the Infection. Transactions of the Royal Society of Tropical Medicine and Hygiene, 113, 359-369.
https://doi.org/10.1093/trstmh/trz019
[52] Ranjit, E., Raghubanshi, B.R., Maskey, S. and Pramila, P. (2018) Prevalence of Bacterial Vaginosis and Its Association with Risk Factors among Non-Pregnant Women: A Hospital Based Study. International Journal of Microbiology, 2018, Article ID: 8349601.
https://doi.org/10.1155/2018/8349601
[53] Garba, D.J., Zabaze, S.S., Tabitha, S., James, G. and Makshwar, K. (2014) Microbiological Diagnosis of Bacterial Vaginosis in Pregnant Women in a Resource Limited Setting in North Central Nigeria. American Journal of Life Sciences, 2, 356-360.
https://doi.org/10.11648/j.ajls.20140206.15
[54] Karmastaji, A., Khajeh, F.G.H. and Amirian, M. (2005) Comparison between Clinical and Laboratory Diagnosis of Vaginitis. Hormozgan Medical Journal, 9, 131-136.
[55] Habibipour, R. (2016) Prevalence Rate of Vulvovaginal Candidiasis and Identification of Candida Species in Women Referred to Hamedan Hospitals 2013-2014, West of Iran. Zahedan Journal of Research in Medical Sciences, 18, Article No. e6250.
https://doi.org/10.17795/zjrms-6250
[56] Apalata, T., Nojaholo, S., Seipone, I.D. and Nxasana, N. (2021) Characterizations of Bacterial Vaginosis among HIV Positive and HIV Negative Women in Rural Eastern Cape Province, South Africa. International Journal of Microbiology, 2021, Article ID: 9913878.
https://doi.org/10.1155/2021/9913878

Copyright © 2024 by authors and Scientific Research Publishing Inc.

Creative Commons License

This work and the related PDF file are licensed under a Creative Commons Attribution 4.0 International License.