Abstract
A close association between Trichomonas vaginalis (TV) infection and bacterial vaginosis (BV) has been reported. Some other studies have found association is stronger with intermediate Nugent score than BV. Most studies have used wet mount microscopy, a relatively insensitive method, to detect TV infection. We wanted to study the association of TV infection with BV and with intermediate Nugent score. We undertook a cross-sectional hospital-based study of 1110 non-pregnant women from Odisha state, India, aged between 18 and 45 years, collecting vaginal swabs for diagnosis of BV by Nugent score (NS) criteria and TV by PCR analysis. TV infection was found in 13.3% of women with intermediate Nugent score (NS 4–6) and 13.6% with BV (NS 7–10). Before adjustment, TV infection was associated with BV, intermediate Nugent, vaginal pH ≥ 4.5, and age group between 26 and 35 years. Multivariate analysis confirmed that TV infection was more likely to have raised vaginal pH, either BV or intermediate Nugent. Proportion of TV cases increased sequentially with the increase in Nugent score up to NS 6, after which a decline was observed. Vaginal pH was higher in the TV-infected group than the uninfected group in women with intermediate Nugent, but no difference was noticed in women with BV. TV infection was equally prevalent in women with intermediate Nugent as well as BV. In the intermediate Nugent group women, TV infection was found only when vaginal pH was raised, indicating a crucial role of vaginal pH in determining TV infection.
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Abbai NS, Reddy T, Ramjee G (2016) Prevalent bacterial vaginosis infection - a risk factor for incident sexually transmitted infections in women in Durban, South. Africa. Int J STD AIDS 27:1283–1288
Allsworth JE, Ratner JA, Peipert JF (2009) Trichomoniasis and other sexually transmitted infections: results from the 2001–2004 National Health and Nutrition Examination Surveys. Sex Transm Dis 36:738–744
Balkus JE, Richardson BA, Rabe LK, Taha TE, Mgodi N, Kasaro MP, Ramjee G, Hoffman IF, Abdool Karim SS (2014) Bacterial vaginosis and the risk of Trichomonas vaginalis acquisition among HIV-1 negative women. Sex Transm Dis 41:123–128
Bochner AF, Baeten JM, Rustagi AS, Nakku-Joloba E, Lingappa JR, Mugo NR, Bukusi EA, Kapiga S, Delany-Moretlwe S, Celum C, Barnabas RV, Partners in Prevention HSV (2017) HIV transmission study and partners PrEP study teams. Sex Transm Infect 93:520–529
Brotman RM, Klebanoff MA, Nansel TR, Yu KF, Andrews WW, Zhang J, Schwebke JR (2010) Bacterial vaginosis assessed by gram stain and diminished colonization resistance to incident gonococcal, chlamydial, and trichomonal genital infection. J Infect Dis 202:1907–1915
Conrad M, Zubacova Z, Dunn LA, Upcroft J, Sullivan SA, Tachezy J, Carlton JM (2011) Microsatellite polymorphism in the sexually transmitted human pathogen Trichomonas vaginalis indicates a genetically diverse parasite. Mol Biochem Parasitol 175:30–38
Fichorova RN (2009) Impact of T. vaginalis infection on innate immune responses and reproductive outcome. J Reprod Immunol 83:185–189
Fichorova RN, Buck OR, Yamamoto HS, Fashemi T, Dawood HY, Fashemi B, Hayes GR, Beach DH, Takagi Y, Delaney ML, Nibert ML, Singh BN, Onderdonk AB (2013) The villain team-up or how Trichomonas vaginalis and bacterial vaginosis alter innate immunity in concert. Sex Transm Infect 89:460–466
Freeman AH, Katz KA, Pandori MW, Rauch LM, Kohn RP, Liska S, Bernstein KT, Klausner JD (2010) Prevalence and correlates of Trichomonas vaginalis among incarcerated persons assessed using a highly sensitive molecular assay. Sex Transm Dis 37:165–168
Fule SR, Fule RP, Tankhiwale NS (2012) Clinical and laboratory evidence of Trichomonas vaginalis infection among women of reproductive age in rural area. Indian J Med Microbiol 30:314–316
Hillier SL, Holmes KK, Marrazzo JM (2008) Sexually transmitted diseases. Health Professions Division; Bacterial Vaginosis, New York: McGraw- Hill pp. 737–68
Hillier SL, Nugent RP, Eschenbach DA, Krohn MA, Gibbs RS, Martin DH, Cotch MF, Edelman R, Pastorek JG 2nd, Rao AV et al (1995) Association between bacterial vaginosis and preterm delivery of a low-birth weight infant. The Vaginal Infections and Prematurity Study Group. N Engl J Med 333:1737–1742
Hillier SL, Krohn MA, Nugent RP, Gibbs RS (1992) Characteristics of three vaginal flora patterns assessed by gram stain among pregnant women. Vaginal Infections and Prematurity Study Group. Am J Obstet Gynecol 166:938–944
Hillier SL, Martius J, Krohn M, Kiviat N, Holmes KK, Eschenbach DA (1988) A case-control study of chorioamnionic infection and histologic chorioamnionitis in prematurity. N Engl J Med 319:972–978
Josey WE, Schwebke JR (2008) The polymicrobial hypothesis of bacterial vaginosis causation: a reassessment. Int J STD AIDS 19:152–154
Kaur S, Khurana S, Bagga R, Wanchu A, Malla N (2008) Trichomoniasis among women in North India: a hospital based study. Indian J Sex Transm Dis 29:76–81
Kengne P, Veas F, Vidal N, Rey JL, Cuny G (1994) Trichomonas vagnialis: repeated DNA target for highly sensitive and specific polymerase chain reaction diagnosis. Cell Mol Biol 40:819–831
Kissinger P, Adamski A (2013) Trichomoniasis and HIV interactions: a review. Sex Transm Infect 89:426–433
Klinger EV, Kapiga SH, Sam NE, Aboud S, Chen CY, Ballard RC, Larsen U (2006) A community-based study of risk factors for Trichomonas vaginalis infection among women and their male partners in Moshi urban district, northern Tanzania. Sex Transm Dis 33:712–718
Lai SK, Hida K, Shukair S, Wang YY, Figueiredo A, Cone R, Hope TJ, Hanes J (2009) Human immunodeficiency virus type 1 is trapped by acidic but not by neutralized human cervico-vaginal mucus. J Virol 83:11196–11200
Madhivanan P, Bartman MT, Pasutti L, Krupp K, Arun A, Reingold AL, Klausner JD (2009) Prevalence of Trichomonas vaginalis infection among young reproductive age women in India: implications for treatment and prevention. Sex Health 6:339–334
Madhivanan P, Krupp K, Chandrasekaran V, Karat C, Arun A, Cohen CR, Reingold AL, Klausner JD (2008) Prevalence and correlates of bacterial vaginosis among young women of reproductive age in Mysore, India. Indian J Med Microbiol 26:132–137
Martin DH, Zozaya M, Lillis RA, Myers L, Nsuami MJ, Ferris MJ (2013) Unique vaginal microbiota that includes an unknown mycoplasma-like organism is associated with Trichomonas vaginalis infection. J Infect Dis 207:1922–1931
Martin HL, Richardson BA, Nyange PM, Lavreys L, Hillier SL, Chohan B, Mandaliya K, Ndinya-Achola JO, Bwayo J, Kreiss 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
Mgone CS, Lupiwa T, Yeka W (2002) High prevalence of Neisseria gonorrhoeae and multiple sexually transmitted diseases among rural women in the Eastern Highlands Province of Papua New Guinea detected by polymerase chain reaction. Sex Transm Dis 29:775–779
National Health Profile (2016) Ministry of Health and Family Welfare, Government of India
Nugent RP, Krohn MA, Hillier SL (1991) Reliability of diagnosing bacterial vaginosis is improved by a standardized method of Gram stain interpretation. J Clin Microbiol 29:297–301
O’Hanlon DE, Moench TR, Cone RA (2013) Vaginal pH and microbicidal lactic acid when lactobacilli dominate the microbiota. PLoS One 8:e80074
O’Hanlon DE, Moench TR, Cone RA (2011) In vaginal fluid, bacteria associated with bacterial vaginosis can be suppressed with lactic acid but not hydrogen peroxide. BMC Infect Dis 11:200
Pauletic AJ, Hawes SE, Geske JA (2004) Experience with routine vaginal pH testing in a family practice setting. Infect Dis Obstet Gynecol 12:63–68
Petrin D, Delgaty K, Bhatt R, Garber G (1998) Clinical and microbiological aspects of Trichomonas vaginalis. Clin Microbiol Rev 2:300–317
Rathod SD, Krupp K, Klausner JD, Arun A, Reingold AL, Madhivanan P (2011) Bacterial vaginosis and risk for Trichomonas vaginalis infection: a longitudinal analysis. Sex Transm Dis 38:882–886
Silver BJ, Guy RJ, Kaldor JM, Jamil MS, Rumbold AR (2014) Trichomonas vaginalis as a cause of perinatal morbidity: a systematic review and meta-analysis. Sex Transm Dis 41:369–376
Silver HM, Sperling RS, St Clair PJ, Gibbs RS (1989) Evidence relating bacterial vaginosis to intra amniotic infection. Am J Obstet Gynecol 161:808–812
Simpson P, Higgins G, Qiao M, Waddell R, Kok T (2007) Real-time PCRs for detection of Trichomonas vaginalis b-tubulin and 18S rRNA genes in female genital specimens. J Med Microbiol 56:772–777
Sivaranjini R, Jaisankar T, Thappa DM, Kumari R, Chandrasekhar L, Malathi M, Parija S, Habeebullah S (2013) Spectrum of vaginal discharge in a tertiary care setting. Trop Parasitol 3:135–139
Sutton M, Sternberg M, Koumans EH, McQuillan G, Berman S, Markowitz L (2007) The prevalence of Trichomonas vaginalis infection among reproductive-age women in the United States, 2001–2004. Clin Infect Dis 45:1319–1326
Wangnapi RA, Soso S, Unger HW, Sawera C, Ome M, Umbers AJ, Ndrewei N, Siba P, Wai L, Suen CS, Vallely A, Wapling J, Ryan C, Mueller I, Rogerson SJ (2015) Prevalence and risk factors for chlamydia trachomatis, Neisseria gonorrhoeae and Trichomonas vaginalis infection in pregnant women in Papua New Guinea. Sex Transm Infect 91:194–200
World Health Organization (2008) Global incidence and prevalence of selected curable. Sex Transm Infect
World Health Organization (2001) Global prevalence and incidence of selected curable sexually transmitted infections: overviews and estimates. In: WHO/HIVAIDS. Edited by Organization WH. Geneva
Acknowledgements
We thank Prof Jane Carlton (Center for genomics and system biology, New York University, New York, USA) for providing TV positive isolates. We express our appreciation for the support from study participants, and hospital nurses for assisting in this project.
Funding
This work was supported by the UK Department for International Development through the Sanitation and Hygiene Applied Research for Equity (SHARE) consortium and intramural support from Asian Institute of Public Health (AIPH), Bhubaneswar, Odisha, India. However, the funding agencies had no involvement in study design, data collection, data analysis, and data interpretation, and the views expressed here do not necessarily reflect those of SHARE or AIPH.
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PD, BT, PP designed the study and data collection instruments. PD managed and coordinated the study. PD, TS, JRM and SS did the laboratory work. Bijaya Panda (BP) and AN are the gynecologists responsible for recruitment of cases and collection of vaginal samples, PD and Bijay Padhi (BP) conducted data analysis, PD, OC, BT, and PP were involved in conceptualizing the manuscript. All authors had intellectual input during the study period and contributed to drafting the manuscript.
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The authors declare that they have no competing interests.
Ethical approval
The study was approved by the Institutional Review Board of Asian Institute of Public health (AIPH) (AIPH ethics ref.: ERC/ No: 2014–16) and the Ethical Committee of Department of Health, Government of Odisha (Ethics ref.: 237/SHRMU). Only those who provided written informed consent to participate in the study were included.
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The data is available from the first author—pdas@aiph.ac.in and corresponding author—ppanigrahi@unmc.edu
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Das, P., Swain, T., Mohanty, J.R. et al. Higher vaginal pH in Trichomonas vaginalis infection with intermediate Nugent score in reproductive-age women—a hospital-based cross-sectional study in Odisha, India. Parasitol Res 117, 2735–2742 (2018). https://doi.org/10.1007/s00436-018-5962-z
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DOI: https://doi.org/10.1007/s00436-018-5962-z