Etiological agents of Vulvovaginitis amongst women complaining of genital tract infection in Soran City, Kurdistan, Iraq

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Etiological agents of Vulvovaginitis amongst women complaining of genital tract infection in Soran City, Kurdistan, Iraq

Bushra Hussain Shnawa, Taban Mohammed Ali, Azhin Ismael Khadhr
Int. J. Biosci.12( 3), 265-279, March 2018.
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Vulvovaginitis is one of the commonest reproductive tract infections in women worldwide. There are three types of infectious vaginitis including, bacterial vaginosis, valvovaginal candidiasis, and trichomoniasis. The present study aimed to characterize the causative agents of vulvovaginitis among women attending Soran Obstetrics and Gynecology hospital. Host -related and some behavioral risk factors which proposed as predisposing factors for this disease were also investigated. A pair of high vaginal swabs was collected from 97 vulvovaginitis women aged 18-52 years. Trichomoniasis was detected by wet and stained smears. Candidiasis was identified by direct examination and culturing on both Sabouraud dextrose agar and Chromagar medium. Bacterial infection was confirmed by Nugent scoring method after Gram staining. The present results showed that 85 (87.6%) cases were positive for etiologic agents and 12(12.3%) with nonpathogenic agents. Among the positive patients, the commonest organisms was bacteria 45%, followed by Candida species 15%, Trichomniasis as 7%, and mixed infection with these three agents in 33%. Moreover, infection with non- albicans Candida like C. galabrata, C. krusei, and C.dubliensis were also detected. Pregnant women showed high percentage of infection with trichomoniasis and candidiasis .Women that used IUD as contraceptive methods, as well as those of non- contraceptive users were more susceptible to bacterial infection than the other. High percentage of women was infected with the etiological agents that responsible for vulvovaginitis particularly with bacteria. Routine culturing of vaginal discharge must be performed for these patients; also antibiotics susceptibility of bacterial isolates should be determined. In addition, comprehensive healthcare education plan is needed to manage the disease.


Adad SJ, de Lima RV, Sawan ZT, Silva ML, de Souza MA, Saldanha JC, Falco VA, da Cunha AH, Murta EF. 2001. Frequency of Trichomonas vaginalis, Candida spp. and Gardnerella vaginalis in cervical-vaginal smears in four different decades. Sao Paulo Med J. 1;119(6), 200-205.

Afolabi BB, Olusanjo Moses, Oyinlola E, Oduyebo O. 2016. Bacterial Vaginosis and Pregnancy Outcome in Lagos, Nigeria Infect Dis. 2016 Jan (3), 1-17. DOI: 10.1093/ofid/ofw030,

Agnew KJ, Hillier SL. 1995. The effect of treatment regimens for vaginitis and cervicitis on vaginal colonization with lactobacilli. Sex Transm Dis 22, 269-273.

Al- Kaisi AAR. 2008 Trichomoniasis among females with vaginal discharge in Baghdad Medical City. J. Fac. Med. Baghdad, 2008, 50, 37- 41.

Al-akeel RA, El-kersh TA, Al-Sheikh YA, Al-Ahmadey ZZ. 2013. Prevalence and comparison for detection methods of Candida species in vaginal specimens from pregnant and non-pregnant Saudi women. Afr J Microbiol Res 7(1), 56-65. DOI: 10.5897/AJMR12.1979.

Al-Attraqhchi AAF, Abbas N, Al-jeboori M. 2013. Detection of Candida spp. responsible for vulvovaginitis in women with contraceptives. Journal of genetic and environmental resources conservation 1(3), 254-261.

Alcaide ML, Feaster DJ, Duan R, Cohen S, Diaz C, Castro JG, Golden MR, Henn S, Colfax GN, Metsch LR. 2015. The incidence of Trichomonas vaginalis infection in women attending nine sexually transmitted diseases clinics in the USA. Sex Transm Infect. DOI: 10.1136/sextrans-2015-052010

Alli JAO, Okonko IO, Odu NN, Kolade AF, Nwanze JC. 2011. Detection and prevalence of Candida isolates among patients in Ibadan, Southwestern Nigeria. J. Microb. Biotechnol. Res 1, 176-184.

Allsworth JEPeipert JF. 2007. Prevalence of bacterial vaginosis: 2001-2004 National Health and Nutrition Examination Survey data. Obstet Gynecol 109(1), 114-120.

Alo MN, Anyim C, Onyebuchi AK, Okonkwo EC. 2012. Prevalence of asymptomatic Co Infection of Candidiasis and Vaginal Trichomoniasis among Pregnant Women in Abakaliki, South-Eastern Nigeria. J. Nat. Sci. Res (2), 87-91.

Al-Saeed WM. 2011. Detection of Trichomonas vaginalis by different methods in women from Dohok province, Eastern Mediterranean Health Journal 17(9), 706-709.

Amsel R, Totten PA, Spiegel CA, Chen KCEschenbach DHolmes KK. 1983. Nonspecific vaginitis. Diagnostic criteria and microbial and epidemiologic associations. Am J Med 74(1), 14-22.

Anderson MR, Klink K, Cohrssen A. 2004. Evaluation of vaginal complaints. JAMA 291(11), 1368-79.

Anorlu R, Imosemi D, Odunukwe N, Abudu O, Otuonye M. 2004. Prevalence of HIV among women with vaginal discharge in a gynecological clinic. J Natl Med Assoc. 2004 Mar 96(3), 367-71.

Babic M, Hukic M. 2010. Candida albicans and non-albicans species as etiological agent of vaginitis in pregnant and non-pregnant women. Bosn J Basic Med Sci 10(1), 89-97.

Bahram A, Hamid B, ZohreT. 2009. Prevalence of bacterial vaginosis and impact of genital hygiene practices in non-pregnant women in Zanjan, Iran, Oman Medical Journal 24(4), 288-293.

Bassisa CM, Allsworth JE, Wahl HN, Sack DE, Young VB, Bell JD. 2017. Effects of intrauterine contraception on the vaginal microbiota. Contraception 96, 189-195.

Bitew A,  Abebaw Y,  Bekele D,  Mihret A. 2017. Prevalence of bacterial vaginosis and associated risk factors among women complaining of genital tract infection. Int. J. Microbial 1-8. DOI: ORG/10.1155/ 2017/4919404

Bonyadpour B, Akbarzadeh M, Mohagheghzadeh A. 2016. A Descriptive study on the prevalence of vulvovaginal infections and species-specific distribution of vulvovaginal candidiasis in married women of the south of Iran. J. Midwifery & Reproductive health 4(4), 741-747.

Boyle DC, Smith JR. 1999. Infection and cervical intraepithelial neoplasia. Int J Gynecol Cancer 9, 177-186. pmid:11240764e

Calzolari E, Masciangelo R, Milite V, Verteramo R. 2000. Bacterial vaginosis and contraceptive methods. Int J Gynecol Obstet 70, 341-6.

Carey JC, Klebanoff MA. 2005. Is a change in the vaginal flora associated with an increased risk of preterm birth? Am J Obstetr Gynecol 192(4), 1341-1346.

Cheesbrough M. 2006. District laboratory practice in tropical countries. 2nd edition, part 2, 243. Cambridge university press.

Emeribe AU, Nasir IA, Onyia J, Ifunanya AL. 2015. Prevalence of Vulvovaginal candidiasis among nonpregnant women attending a tertiary health care facility in Abuja, Nigeria. Research and Reports in Tropical Medicine 6, 37-42.

Gallo MF, Macaluso M,Warner L, Fleenor ME, Hook III EW, Brill I, et al. 2012. Bacterial vaginosis, gonorrhea, and chlamydial infection among women attending a sexually transmitted disease clinic: a longitudinal analysis of possible causal links. Ann Epidemiol 22(3), 213-20.

Garcia LS, Ash LR. 1979. Diagnostic parasitology. 2nd edition, Mosby Company.

Geiger AM, Foxman B, Sobel JD. 1995. Chronic vulvovaginal candidiasis: characteristics of women with Candida albicansC glabrata and no Candida. Genitourin Med 71, 304-307.

Gerbase AC, Rowley JT, Heyman HL, Berkley SFB, Piot P. 1998. Global prevalence and incidence estimates of selected curable STDs. Sex Trans Inf 74, S12-S16.

Goncalves B, Ferreira C, Alves CT, Henriques M, Azeredo J, Silva S. 2016. Vulvovaginal candidiasis: Epidemiology, microbiology and risk factors. Crit Rev Microbiol 42(6), 905-927. DOI: 10.3109/1040841X.2015.1091805.

Gram IT, Macaluso M, Churchill J, Stalsberg H. 1992. Trichomonas vaginalis (TV) and human papillomavirus (HPV) infection and the incidence of cervical intraepithelial neoplasia (CIN) grade III. Cancer Causes Control 3, 231-236.

Gupta K, Stapleton AEHooton TMRoberts PLFennell CLStamm WE. 1998. Inverse association of H2O2-producing lactobacilli and vaginal Escherichia coli colonization in women with recurrent urinary tract infections. J Infect Dis 178, 446-450.

Hillier SL. 1993. Diagnostic microbiology of bacterial vaginosis. Am J Obstet Gynecol 169, 455e9.

Hirt RP, Sherrard J. 2015. Trichomonas vaginalis origins, molecular pathobiology and clinical considerations. Curr Opin Infect Dis 28, 72-79.

Horowitz BJ, Edelstein SW, Lippman L. 1985. Candida tropicalis vulvovaginitis .Obstet Gynecol 66, 229-232.

Iwueze MO, Ezeanyanwu LN, Okafor FC, Nwaorgu OC, Ukibe SC. 2014. Prevalence of Trichomonas vaginalis infection among women attending hospitals/health centres in Onitsha community, Onitsha North Local Government Area of Anambra State. Bioscientist 2, 54-64.

Kadir MA, Fattah COD. 2010. Trichomonas vaginalis among women in Sulaimania Governorate-Iraq. Tikrit J pharmaceutical .science 6, 1-9.

Kadir MA, Jerjis KJ. 1999. Incidence of trichomoniasis in Kirkuk city. Journal of the Faculty of Medicine, Baghdad 28(2), 75-79. 15.

Kadir MA, Salehy A, Hamed EE. 1996. Studies on Trichomonas vaginalis in Erbil teaching hospital. Journal of the Faculty of Medicine, Baghdad 23(1), 83-88. 16.

Kadir MA, Sulyman MA, Dawood IS, Shams-Eldin S. 2014. Trichomonas vaginalis and associated microorganisms in women with vaginal discharge in Kerkuk-Iraq. Ankara Medical journal 14(3), 91-99. DOI: 10.17098/amj.47284.

Kharofa WA. 1999. An epidemiological study and cultivation of Trichomonas vaginalis in Mosul city MSc thesis. Department of Microbiology, College of Medicine, University of Mosul, Mosul, Iraq.

Klebanoff SJ, Hillier SL, Eschenbach DA,  Waltersdorph DA. 1991. Control of the microbial flora of the vagina by H202-Generating Lactobacilli. J Infect Dis 164, 94-100.

Lai SK,  Hida K,  Shukair S,  Wang Y-Y,  Figueiredo A,  Cone R,  Hope TJ,  Hanes J. 2009. Human immunodeficiency virus type 1 is trapped by acidic but not by neutralized human cervicovaginal mucus. J Virol 83(21), 11196-11200. DOI: 10.1128/JVI.01899-08

Loose DS, Stevens D, Schurman DJ, Feldman D. 1983. Distribution ofa corticosteroid-binding protein inCandida and other fungal genera.J Gen Microbiol 129, 2379-85.

Loveless M, Myiant O. 2018. Vulvovaginitis- presentation of more common problems in pediatric and adolescent gynecology. 48,14-27. DOI: 10.1016/j.bpobgyn.

Madden T, Grentzer JM, Secura GM, Allsworth JE, Peipert JF. 2012. Risk of bacterial vaginosis in users of the intrauterine device: a longitudinal study. Sexually Transmitted Diseases 39,217–222

Malone MA. 2017. Vulvovaginitis in: Bope ET, Kellerman RD, (Eds.), Conn’s Current Therapy. Elsevier, USA pp.1092.

Maroszyńska M, Kunicka-Styczyńska A, Rajkowska K, Maroszyńska I. 2013. Antibiotics sensitivity of Candida clinical and food-borne isolates. Acta Biochim Pol 60, 719-724.

Martin HL, Richardson BANyange PMLavreys LHillier SLChohan BMandaliya KNdinya-Achola JOBwayo JKreiss J. 1999 .Vaginal lactobacilli, microbial flora, and risk of human immunodeficiency virus type 1 and sexually transmitted disease acquisition. J Infect Dis 180, 1863-1868.

Mbim EN, Mboto CI, George UE, Umego CF, Edet UO, Orajiaka NA. 2017. Prevalence of Vaginal Candidiasis among Female Students of a Hostel in the University of Calabar, Calabar. J Applied Life Sciences International 13(3), 1-7.

Mc Cormack WM, Augenbraun MH. 2015. Vulvovaginitis and Cervicitis. Mandell, Douglas, and Bennett’s Principles and Practice of Infectious Diseases, Updated Edition 110, 1358-1371.

Meites E. 2013. Trichomoniasis .The “Neglected” Sexually Transmitted Disease. Infect Dis Clin North Am 27(4), 755-764. DOI: 10.1016/j.idc.2013.06.003

Mercer F, Diala FGI, Chen YP, Molgora BM, Ng SH, Johnson PJ. 2016. Leukocyte Lysis and Cytokine Induction by the Human Sexually Transmitted Parasite Trichomonas vaginalis. PloS Negl Trop Dis 10, 1-19. DOI: 10.1371/journal.pntd.0004913

Mills BB. 2017. Vaginitis: Beyond the Basics. Obstet Gynecol Clin N Am 44, 159-177. DOI: j.ogc.2017.02.010.

Mulley AG. 2000. Approach to the patient with a vaginal discharge. In: Goroll AH, Mulley AG, editors. Primary Care medicine: office evaluation and management of the adult patient. Philadelphia: Lippincott Williams & Wilkins p. 702-7.

Narayankhedar A,  Hodiwala A,  Mane A. 2015. Clinicoetiological Characterization of Infectious Vaginitis amongst Women of Reproductive Age Group from Navi Mumbai, India. J Sex Transm Dis 817092. DOI: 10.1155/2015/817092

Nelson M, Wanjiru W, Margaret MW. 2013. Prevalence of vaginal candidiasis and determination of the occurrence of Candida species in pregnant women attending the antenatal clinic of Thika District Hospital, Kenya. Open J Med Microbiol 3, 264-72.

Nouraddin AS, Alsakee HM. 2015 . Prevalence Of Trichomonas Vaginalis Infection Among Women In Erbil Governorate, Northern Iraq: An Epidemiological Approach. European Scientific Journal August 2015 edition vol. 11, No. 24.243-254.

Nugent RP, Krohn MA, Hillier SI. 1991. Reliability of diagnosing bacterial vaginosis is improved by a standardized method of Gram stain interpretation. J Clin Microbiol 29, pp. 297-301.

Nwadioha SI, Egah DZ, Alao OO, Iheanacho E. 2010. Risk factors for vaginal candidiasis among women attending primary health care centers of Jos, Nigeria. J Clin Med Res 2, 110-13.

Nyirjesy P, Seeney SM, Grody MH, Jordan CA, Buckley HR. 1995 .Chronic fungal vaginitis: the value of cultures. Am J Obstet Gynecol 173, 820-3.

Nyirjesy P. 2008. Vulvovaginal candidiasis and bacterial vaginosis. Infect Dis Clin North Am 22, 637-52, vi.

Nyirjesy P. 2014. Management of persistent vaginitis. Obstet Gynecol 124(6),1135-46.

Nzomo J, Waiyaki P, Waihenya R. 2013. Bacterial vaginosis and correlates in women of reproductive age in Thika, Kenya. Advances in Microbiol, 2013, 3, 249-254.

Okungbowa FI, Isikhuemhen OS, Dede APO. 2003. The distribution frequency of Candida species in the genitourinary tract among symptomatic individuals in Nigerian cities. Rev Iberoam Micol 20, 60-3.

Olowe O, Makanjuola O, Olowe R, Adekanle D. 2014. Prevalence of vulvovaginal candidiasis, trichomoniasis and bacterial vaginosis among pregnant women receiving antenatal care in Southwestern Nigeria. European Journal of Microbiology and immunology 4(4), 193-197. DOI: 10.1556/EUJMI-D-14-00027.

Pham AT, Kives S, Merovitz L, Nitsch R, Tessler K, Yudin MH, et al. 2012. Screening for bacterial vaginosis at the time of intrauterine contraceptive device insertion. J Obstet Gynaecol Can 34, 179-185.

Phukan N, Parsamand T, Brooks AE, Nguyen TN, Simoes-Barbosa A. 2013. The adherence of Trichomonas vaginalis to host ectocervical cells is influenced by lactobacilli. Sex Transm Infect 89, 455-459. DOI: 10.1136/sextrans-2013-051039 

Powell BL, Frey CL, Drutz DJ. 1984. Identification of a 17b-estradiol binding protein in Candida albicans and Candida (Torulopsis) glabrata. Exp Mycol 8, 304-13.

Ravel J, Gajer P, Abdo Z, Schneider GM, Koenig SSK, McCulle SL et al. 2011. Vaginal microbiome of reproductive-age women. Proc Natl Acad Sci US A 108, 4680-4687.

Ray D, Goswami R, Banerjee U, et al. 2007. Prevalence of Diabetes Care 30, pp. 312-317.

Satterwhite CLTorrone EMeites EDunne EFMahajan ROcfemia MCSu JXu FWeinstock H. 2013. Sexually transmitted infections among US women and men: prevalence and incidence estimates. Sex Transm Dis 40(3), 187-93. DOI: 10.1097/OLQ.0b013e318286bb53

Schwebke JR, Burgess D. 2004. Trichomoniasis. Clin Microbiol Rev 17, 794-803.

Secor WE, Meites E, Star MC, Workowski KA. 2014. Neglected Parasitic Infections: Trichomoniasis. Am J Trop Med Hyg 90, 800-804.

Skowronski R, Feldman D. 1989. Characterization of an estrogen-binding protein in the yeast Candida albicans. Endocrinology 124, 1965-1972.

Sobel JD. 2007. Vulvovaginal candidosis. Lancet 369, 1961-1971.

Spinillo A, Capuzzo E, Gulminetti R, Marone PColonna LPiazzi G. 1997Prevalence of and risk factors for fungal vaginitis caused by non-albicans species. Am J Obstet Gynecol 176, 138-141.

Taha TE, Hoover DR, Dallabetta GA, Kumwenda NIMtimavalye LAYang LPLiomba GNBroadhead RLChiphangwi JDMiotti PG. 1998. Bacterial vaginosis and disturbances of vaginal flora: association with increased acquisition of HIV. AIDS 12(13), 1699-1706.

Tamura NKNegri MFBonassoli LA, Svidzinski TI. 2007. Virulence factors for Candida spp recovered from intravascular catheters and hospital workers hands. Rev Soc Bras Med Trop. Jan-Feb 40(1), 91-93.

Tellapragada C, Eshwara VK, Bhat P, Kamath A, Aletty S, Mukhopadhyay C. 2017. Screening of vulvovaginal infections during pregnancy in resource constrained settings: Implications on preterm delivery. J Infect Public Health. 2017; 10(4), 431-437. DOI: 10.1016/j.jiph.2016.06.003.

Toua V, Djaouda M, Gaké B, Menye DE, Christie EA, Tambe E, Akindoh VV, Njiné T. 2013. Prevalence of Vulvovaginal candidiasis amongst pregnant women in Maroua (Cameroon) and the sensitivity of Candida albicans to extracts of six locally used antifungal plants. International Research Journal of Microbiology (IRJM) 4, 89-97.

Vaginitis. 2006. ACOG Practice Bulletin No. 72. American College of Obstetricians and Gynecologists. Obstet Gynecol 107, pp. 1195-1206.

Wagner RD, Johnson SJ. 2012. Probiotic Lactobacillus and estrogen effects on vaginal epithelial gene expression responses to Candida albicans. J Biomed Sci 19, 58. DOI: 10.1186/1423-0127-19-58.

Wei Y, Feng J, Luo Z. 2010. Isolation and genotyping of vaginal non-albicans Candida spp. in women from two different ethnic groups in Lanzhou China. Int J Gynecol Obstetrics 110, 227-230.

Wiesenfeld HC, Hillier SL, Krohn MA, Landers DV, Sweet RL. 2003. Bacterial vaginosis is a strong predictor of Neisseria gonorrhoeae and Chlamydia trachomatis infection. Clinical Infect Dis 36, 663-668.

Wondemagegn M, Yimer M, Zenebe Y, 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(42), 1-9.

Workowski KA, Bolan GA. 2015. Centers for Disease Control and Prevention: Sexually transmitted diseases treatment guidelines, MMWR Recomm Rep 64, 1-137.

Yadav K, Prakash S. 2016. Prevalence of vulvovaginal candidiasis in pregnancy. Glob. J. Med. Med. Sci 4(1), 108-116.

Yazar S, Dagci H,Aksoy U, Ustun S, Akisu C, Mucide AK, Daldal N. 2002. Frequency of Trichomonas vaginalis among women having vaginal discharge in Izmir, Turkey. Inonu. Univ. Tip. Fakut. Derg 9, 159-161.

Yudin MHMoney DM. 2017. Screening and Management Bacterial Vaginosis in Pregnancy. J Obstet Gynaecol Can Aug 39(8), e184-e191. DOI: 10.1016/j.jogc.2017.04.018