Reliability of conventional Papanicolaou smear in diagnosing bacterial vaginosis among women with clinical genital infection

Kavita Vivek Anand; Sharmila Anil Pimple; Gauravi A. Mishra; Rupali V. Sahare; Saleem Pathuthara; Kedar K. Deodhar; Surendra S. Shastri

doi:10.4103/sajc.sajc_421_18

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ORIGINAL ARTICLE: Epidemiology of Cancer and Cancer Screening

09 (

); 13-16

doi:

10.4103/sajc.sajc_421_18

Reliability of conventional Papanicolaou smear in diagnosing bacterial vaginosis among women with clinical genital infection

Kavita Vivek Anand¹, Sharmila Anil Pimple^1,, Gauravi A. Mishra¹, Rupali V. Sahare², Saleem Pathuthara³, Kedar K. Deodhar⁴, Surendra S. Shastri⁵

1 Department of Preventive Oncology, Tata Memorial Centre, Affliliated to Homi Bhabha National Institute, Mumbai, Maharashtra

2 Department of Microbiology, R. N. Cooper General Hospital, Tata Memorial Hospital, Mumbai, Maharashtra

3 Department of Cytopathology, Tata Memorial Hospital, Mumbai, Maharashtra

4 Department of Pathology, Tata Memorial Hospital, Mumbai, Maharashtra

5 Department of Health Disparities Research, Division of Cancer Prevention and Population Science, MD Anderson Cancer Centre, Houston

*Corresponding author: Dr. Sharmila Anil Pimple. drsharmilapatil@yahoo.com

Published: 2020-12-14

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Abstract

Objective: Bacterial vaginosis (BV) is a common reproductive tract infection (RTI) reported among Indian women. BV can influence the persistence of high-risk oncogenic human papillomavirus, a causative factor for cervical cancer. BV and cervical cancer are major public health issues in a developing country like India. It becomes important for a resource-constrained country like India with poor healthcare access to implement control measures to screen and treat RTI in an attempt to prevent the risk for cervical cancer. Papanicolaou (Pap) smear is an established screening tool for cervical cancer and the diagnosis of RTIs, forms a part of its evaluation. The present study explores the validity of conventional Pap smear in diagnosing BV. Methodology: Pap smear and Gram stain smear were collected for 254 women with clinically evident cervicitis/cervicovaginitis (genital infection). Using the Nugent score on Gram stain as a gold standard, we determined the sensitivity and specificity of Pap smear to diagnose BV. Results: The overall prevalence of BV in the study population was 44% using the Nugent score. Pap smear showed sensitivity and specificity of 70.9%. (CI- 61.5% - 79.2%) and 56.8% (CI – 48.2%–65.2%), respectively. The positive predictive value of Pap smear to diagnose BV was 56.5% (CI – 47.8%–64.9%), and the negative predictive value was 71.2% (CI – 61.8%–79.4%). Conclusion: In the present study, conventional Pap smear demonstrates good accuracy to detect BV. Pap testing for cervical cancer screening can additionally serve as an effective screening tool for diagnosing BV among women with genital infection in healthcare settings.

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References

National AIDS Control Organisation. Report on Mid-Term Review of Sexually Transmitted Infection Services; 2009. Available from: http://www.naco.gov.in/sites/default/STI%20RTI%20MONOGRAPH%20NACP-III-pdf. [Last accessed on 2015 Aug 28].
Centre for Disease Control and Prevention. Bacterial Vaginosis; 2015. Available from: https://www.cdc.gov/std/tg2015/bv. [Last accessed on 2018 Jun 19].
Sodhani P, Garg S, Bhalla P, Singh MM, Sharma S, Gupta S. Prevalence of bacterial vaginosis in a community setting and role of the pap smear in its detection. Acta Cytol 2005;49:634-8.
Marrazzo JM, Wiesenfeld HC, Murray PJ, Busse B, Meyn L, Krohn M, et al. Risk factors for cervicitis among women with bacterial vaginosis. J Infect Dis 2006;193:617-24.
Paavonen J, Critchlow CW, DeRouen T, Stevens CE, Kiviat N, Brunham RC, et al. Etiology of cervical inflammation. Am J Obstet Gynecol 1986;154:556-64.
Peipert JF, Montagno AB, Cooper AS, Sung CJ. Bacterial vaginosis as a risk factor for upper genital tract infection. Am J Obstet Gynecol 1997;177:1184-7.
Woodman CB, Collins SI, Young LS. The natural history of cervical HPV infection: Unresolved issues. Nat Rev Cancer 2007;7:11-22.
Nam KH, Kim YT, Kim SR, Kim SW, Kim JW, Lee MK, et al. Association between bacterial vaginosis and cervical intraepithelial neoplasia. J Gynecol Oncol 2009;20:39-43.
Gillet E, Meys JF, Verstraelen H, Verhelst R, De Sutter P, Temmerman M, et al. Association between bacterial vaginosis and cervical intraepithelial neoplasia: Systematic review and meta-analysis. PLoS One 2012;7:e45201.
Williams VM, Filippova M, Soto U, Duerksen-Hughes PJ. HPV-DNA integration and carcinogenesis: Putative roles for inflammation and oxidative stress. Future Virol 2011;6:45-57.
International Agency for Research on Cancer. Human papillomaviruses. IARC Monographs on the Evaluation of Carcinogenic Risks to Humans. Vol. 64. International Agency for Research on Cancer; 1995.
Walboomers JM, Jacobs MV, Manos MM, Bosch FX, Kummer JA, Shah KV, et al. Human papillomavirus is a necessary cause of invasive cervical cancer worldwide. J Pathol 1999;189:12-9.
Nayar R, Wilbur DC. The pap test and Bethesda 2014. “The reports of my demise have been greatly exaggerated.” (after a quotation from mark Twain). Acta Cytol 2015;59:121-32.
GLOBOCAN Cancer Fact Sheet Cervix Cancer. Available from: http://www.globocan.iarc.fr/Default.aspx. [Last accessed on 2018 Jul 24].
Prey M. Routine pap smears for the diagnosis of bacterial vaginosis. Diagn Cytopathol 1999;21:10-3.
Eriksson K, Forsum U, Bjørnerem A, Platz-Christensen JJ, Larsson PG. Validation of the use of pap-stained vaginal smears for diagnosis of bacterial vaginosis. APMIS 2007;115:809-13.
Davis JD, Connor EE, Clark P, Wilkinson EJ, Duff P. Correlation between cervical cytologic results and gram stain as diagnostic tests for bacterial vaginosis. Am J Obstet Gynecol 1997;177:532-5.
Tokyol C, Aktepe OC, Cevrioǧlu AS, Altindiş M, Dilek FH. Bacterial vaginosis: Comparison of pap smear and microbiological test results. Mod Pathol 2004;17:857-60.
Karani A, De Vuyst H, Luchters S, Othigo J, Mandaliya K, Chersich MF, et al. The pap smear for detection of bacterial vaginosis. Int J Gynaecol Obstet 2007;98:20-3.
Greene JF 3rd, Kuehl TJ, Allen SR. The Papanicolaou smear: Inadequate screening test for bacterial vaginosis during pregnancy. Am J Obstet Gynecol 2000;182:1048-9.
Wang J. Bacterial vaginosis. Prim Care Update Ob Gyns 2000;7:181-5.
Nugent RP, Krohn MA, Hillier SL. Reliability of diagnosing bacterial vaginosis is improved by a standardized method of gram stain interpretation. J Clin Microbiol 1991;29:297-301.
Money D. The laboratory diagnosis of bacterial vaginosis. Can J Infect Dis Med Microbiol 2005;16:77-9.
Platz-Christensen JJ, Larsson PG, Sundström E, Wiqvist N. Detection of bacterial vaginosis in wet mount, Papanicolaou stained vaginal smears and in gram stained smears. Acta Obstet Gynecol Scand 1995;74:67-70.
Vardar E, Maral I, Inal M, Ozgüder O, Tasli F, Postaci H. Comparison of gram stain and pap smear procedures in the diagnosis of bacterial vaginosis. Infect Dis Obstet Gynecol 2002;10:203-7.
Siddig EE, Albari RF, Mohamed MA, Elamin BK, Edris AM. Bacterial vaginosis in Khartoum state, Sudan: Comparison of gram stain with pap test procedures. Afr J Microbiol Res 2017;11:644-8.
Luff RD. The Bethesda system for reporting cervical/vaginal cytologic diagnoses. Report of the 1991 Bethesda workshop. Am J Clin Pathol 1992;98:152-4.
Larsen B, Monif GR. Understanding the bacterial flora of the female genital tract. Clin Infect Dis 2001;32:e69-77.
Giacomini G, Paavonen J, Rilke F. Microbiologic classification of cervicovaginal flora in Papanicolaou smears. Acta Cytol 1989;33:276-8.
Giacomini G, Schnadig VJ. The cervical Papanicolaou smear: Bacterial infection and the Bethesda system. Acta Cytol 1992;36:109-10.
Kharsany AB, Hoosen AA, Moodley J, Bagaratee J, Gouws E. The association between sexually transmitted pathogens and cervical intra-epithelial neoplasia in a developing community. Genitourin Med 1993;69:357-60.

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[1] National AIDS Control Organisation. Report on Mid-Term Review of Sexually Transmitted Infection Services; 2009. Available from: http://www.naco.gov.in/sites/default/STI%20RTI%20MONOGRAPH%20NACP-III-pdf. [Last accessed on 2015 Aug 28].

[2] Centre for Disease Control and Prevention. Bacterial Vaginosis; 2015. Available from: https://www.cdc.gov/std/tg2015/bv. [Last accessed on 2018 Jun 19].

[3] Sodhani P, Garg S, Bhalla P, Singh MM, Sharma S, Gupta S. Prevalence of bacterial vaginosis in a community setting and role of the pap smear in its detection. Acta Cytol 2005;49:634-8.

[4] Marrazzo JM, Wiesenfeld HC, Murray PJ, Busse B, Meyn L, Krohn M, et al. Risk factors for cervicitis among women with bacterial vaginosis. J Infect Dis 2006;193:617-24.

[5] Paavonen J, Critchlow CW, DeRouen T, Stevens CE, Kiviat N, Brunham RC, et al. Etiology of cervical inflammation. Am J Obstet Gynecol 1986;154:556-64.

[6] Peipert JF, Montagno AB, Cooper AS, Sung CJ. Bacterial vaginosis as a risk factor for upper genital tract infection. Am J Obstet Gynecol 1997;177:1184-7.

[7] Woodman CB, Collins SI, Young LS. The natural history of cervical HPV infection: Unresolved issues. Nat Rev Cancer 2007;7:11-22.

[8] Nam KH, Kim YT, Kim SR, Kim SW, Kim JW, Lee MK, et al. Association between bacterial vaginosis and cervical intraepithelial neoplasia. J Gynecol Oncol 2009;20:39-43.

[9] Gillet E, Meys JF, Verstraelen H, Verhelst R, De Sutter P, Temmerman M, et al. Association between bacterial vaginosis and cervical intraepithelial neoplasia: Systematic review and meta-analysis. PLoS One 2012;7:e45201.

[10] Williams VM, Filippova M, Soto U, Duerksen-Hughes PJ. HPV-DNA integration and carcinogenesis: Putative roles for inflammation and oxidative stress. Future Virol 2011;6:45-57.

[11] International Agency for Research on Cancer. Human papillomaviruses. IARC Monographs on the Evaluation of Carcinogenic Risks to Humans. Vol. 64. International Agency for Research on Cancer; 1995.

[12] Walboomers JM, Jacobs MV, Manos MM, Bosch FX, Kummer JA, Shah KV, et al. Human papillomavirus is a necessary cause of invasive cervical cancer worldwide. J Pathol 1999;189:12-9.

[13] Nayar R, Wilbur DC. The pap test and Bethesda 2014. “The reports of my demise have been greatly exaggerated.” (after a quotation from mark Twain). Acta Cytol 2015;59:121-32.

[14] GLOBOCAN Cancer Fact Sheet Cervix Cancer. Available from: http://www.globocan.iarc.fr/Default.aspx. [Last accessed on 2018 Jul 24].

[15] Prey M. Routine pap smears for the diagnosis of bacterial vaginosis. Diagn Cytopathol 1999;21:10-3.

[16] Eriksson K, Forsum U, Bjørnerem A, Platz-Christensen JJ, Larsson PG. Validation of the use of pap-stained vaginal smears for diagnosis of bacterial vaginosis. APMIS 2007;115:809-13.

[17] Davis JD, Connor EE, Clark P, Wilkinson EJ, Duff P. Correlation between cervical cytologic results and gram stain as diagnostic tests for bacterial vaginosis. Am J Obstet Gynecol 1997;177:532-5.

[18] Tokyol C, Aktepe OC, Cevrioǧlu AS, Altindiş M, Dilek FH. Bacterial vaginosis: Comparison of pap smear and microbiological test results. Mod Pathol 2004;17:857-60.

[19] Karani A, De Vuyst H, Luchters S, Othigo J, Mandaliya K, Chersich MF, et al. The pap smear for detection of bacterial vaginosis. Int J Gynaecol Obstet 2007;98:20-3.

[20] Greene JF 3rd, Kuehl TJ, Allen SR. The Papanicolaou smear: Inadequate screening test for bacterial vaginosis during pregnancy. Am J Obstet Gynecol 2000;182:1048-9.

[21] Wang J. Bacterial vaginosis. Prim Care Update Ob Gyns 2000;7:181-5.

[22] Nugent RP, Krohn MA, Hillier SL. Reliability of diagnosing bacterial vaginosis is improved by a standardized method of gram stain interpretation. J Clin Microbiol 1991;29:297-301.

[23] Money D. The laboratory diagnosis of bacterial vaginosis. Can J Infect Dis Med Microbiol 2005;16:77-9.

[24] Platz-Christensen JJ, Larsson PG, Sundström E, Wiqvist N. Detection of bacterial vaginosis in wet mount, Papanicolaou stained vaginal smears and in gram stained smears. Acta Obstet Gynecol Scand 1995;74:67-70.

[25] Vardar E, Maral I, Inal M, Ozgüder O, Tasli F, Postaci H. Comparison of gram stain and pap smear procedures in the diagnosis of bacterial vaginosis. Infect Dis Obstet Gynecol 2002;10:203-7.

[26] Siddig EE, Albari RF, Mohamed MA, Elamin BK, Edris AM. Bacterial vaginosis in Khartoum state, Sudan: Comparison of gram stain with pap test procedures. Afr J Microbiol Res 2017;11:644-8.

[27] Luff RD. The Bethesda system for reporting cervical/vaginal cytologic diagnoses. Report of the 1991 Bethesda workshop. Am J Clin Pathol 1992;98:152-4.

[28] Larsen B, Monif GR. Understanding the bacterial flora of the female genital tract. Clin Infect Dis 2001;32:e69-77.

[29] Giacomini G, Paavonen J, Rilke F. Microbiologic classification of cervicovaginal flora in Papanicolaou smears. Acta Cytol 1989;33:276-8.

[30] Giacomini G, Schnadig VJ. The cervical Papanicolaou smear: Bacterial infection and the Bethesda system. Acta Cytol 1992;36:109-10.

[31] Kharsany AB, Hoosen AA, Moodley J, Bagaratee J, Gouws E. The association between sexually transmitted pathogens and cervical intra-epithelial neoplasia in a developing community. Genitourin Med 1993;69:357-60.

Reliability of conventional Papanicolaou smear in diagnosing bacterial vaginosis among women with clinical genital infection

Abstract

Abstract

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