Bacterial vaginosis – diagnostic dilemma and implications

  • Sonja Atanasievska Military Medical Academy, Institute of Microbiology
  • Dane Nenadić Military Medical Academy, Center for Gynecology and Human Reproduction
  • Slaviša Stanković University of Belgrade, Faculty of Biology
  • Vesna Protić-Đokić Military Medical Academy, Institute of Microbiology
  • Elizabeta Ristanović Military Medical Academy, Institute of Microbiology
Keywords: diagnostic techniques, obstetrical and gynecological;, microscopy;, vaginal diseases;, vaginal smears;, vaginosis, bacterial

Abstract


Background/Aim. Bacterial vaginosis (BV) is one of the most common microbial dysbiosis, characterized by a decrease of Lactobacillus spp. with an increase of other anaerobic bacteria species [Gardnerella (G.) vaginalis, Atopobium (A.) vaginae, Prevotella spp, Mobiluncus spp, etc.] causing serious gynecological and obstetric complications. Therefore, it is particularly important to have accurate and reliable diagnostic standards. The aim of this study was to compare the results of various diagnostic methods for detecting BV, such as Amsel, Nugent, and Ison and Hay criteria, as well as multiplex quantitative real-time polymerase chain reaction (mqRT-PCR) test. Methods. This study involved vaginal swabs from 235 patients of reproductive age. Nugent criteria were used as the ‘gold standard’ compared with Amsel and Ison/Hay criteria as well as mqRT-PCR test based on the detection and quantification of G. vaginalis, A. vaginae, Lactobacillus spp., and total concentration of bacterial DNA. The kappa coefficient was employed to measure agreement between tests. Results. Our analysis demonstrated excellent agreement between Ison/Hay criteria and Nugent scores (kappa = 0.95), good agreement between Amsel and Nugent criteria (kappa = 0.78), while between Nugent criteria and mqRT-PCR test agreement was moderate (kappa = 0.59). Total agreements of Ison/Hay, Amsel, and mqRT-PCR against Nugent scores were 94.9%, 90.2%, and 74%, respectively. Nugent methods classified the highest number of intermediate patients - 60 (25.2%). The largest number of BV patients was detected by the mqRT-PCR method, while the largest number of healthy patients was detected by Amsel criteria. Conclusion. The mqRT-PCR is the best choice for BV diagnosis because it is more efficient at differentiating patients with intermediate results. Compared to Amsel and Nugent methods that group patients into 2 or 3 categories, the mqRT-PCR method recognizes other conditions of vaginal flora important for correct diagnoses and application of better therapeutic approaches, as well as preventing possible clinical consequences of this dysbiosis.

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1.      Amabebe E, Anumba DOC. The Vaginal Microenvironment: The Physiologic Role of Lactobacilli. Front Med (Lausanne) 2018; 5: 181.

2.      Van de Wijgert JHHMJespers V. The global health impact of vaginal dysbiosis. Res Microbiol 2017; 168(9‒10): 859‒64.

3.      Huang B, Fettweis JM, Brooks JP, Jefferson KK, Buck GA. The changing landscape of the vaginal microbiome. Clin Lab Med 2014; 34(4): 747‒61.

4.      Nelson TM, Borgogna JL, Brotman RM, Ravel J, Walk ST, Yeoman CJ. Vaginal biogenic amines: biomarkers of bacterial vaginosis or precursors to vaginal dysbiosis?. Front Physiol 2015; 6: 253.

5.      Gibbs RS. Asymptomatic bacterial vaginosis: is it time to treat? Am J Obstet Gynecol 2007; 196(6): 495‒6.

6.      Ma B, Forney LJ, Ravel J. Vaginal microbiome: rethinking health and disease. Ann Rev Microbiol 2012; 66: 371‒89.

7.      Redelinghuys MJ, Geldenhuys J, Jung H, Kock MM. Bacterial Vaginosis: Current Diagnostic Avenues and Future Opportunities. Front Cell Infect Microbiol 2020; 10: 354.

8.      Donders GGG, Ravel J, Vitali B, Netea MG, Salumets A, Unemo M. Role of Molecular Biology in Diagnosis and Characterization of Vulvo-Vaginitis in Clinical Practice. Gynecol Obstet Invest 2017; 82(6): 607‒16.

9.      Nasioudis D, Linhares IM, Ledger WJ, Witkin SS. Bacterial vaginosis: a critical analysis of current knowledge. BJOG 2017; 124(1): 61‒9.

10.   Ison CA, Hay PE. Validation of a simplified grading of Gram stained vaginal smears for use in genitourinary medicine clinics. Sex Transm Infect 2002; 78(6): 413‒5.

11.   Sycuro LK, Fredricks DN. Microbiota of the genitourinary tract. In: Fredricks DN, editor. The human microbiota. How microbial communities affect health and disease. Hoboken, New Jersey:  John Wiley & Sons, Inc; 2013. p. 168‒99.

12.   Onderdonk ABDelaney ML, Fichorova RN. The Human Microbiome during Bacterial Vaginosis. Clin Microbiol Rev 2016; 29(2): 223‒38.

13.   Altman DG. Practical statistics for medical research. London: Chapman and Hall; 1991.

14.   Chawla R, Bhalla P, Chadha S, Grover S, Garg S. Comparison of Hay's criteria with Nugent's scoring system for diagnosis of bacterial vaginosis. Biomed Res Int 2013; 2013: 365194.

15.   Mohammadzadeh F, Dolatian M, Jorjani M, Alavi Majd H. Diagnostic value of Amsel's clinical criteria for diagnosis of bacterial vaginosis. Glob J Health Sci 2014; 7(3): 8‒14.

16.   Mahajan G, Mahajan A, Chopra S, Chand K. Comparison of Different Diagnostic Methods of Bacterial Vaginosis – Amsel’svs Nugent. Int J Curr  Microbiol App Sci 2017; 6(5): 1442‒8.

17.   Sha BE, Chen HY, Wang QJ, Zariffard MR, Cohen MH, Spear GT. Utility of Amsel criteria, Nugent score, and quantitative PCR for Gardnerella vaginalis, Mycoplasma hominis, and Lactobacillus spp. for diagnosis of bacterial vaginosis in human immunodeficiency virus-infected women. J Clin Microbiol 2005; 43(9): 4607‒12.

18.   Amit AR, Parmjit S, Sharma V. Comparison of the Amsel's composite clinical criteria and Nugent's criteria for diagnosis of BV: A step towards preventing mis-diagnosis. J Adv Res Biol Sci 2013; 5(1): 37–44.

19.   Verstraelen H, Verhelst R. Bacterial vaginosis: an update on diagnosis and treatment. Expert Rev Anti Infect Ther 2009; 7(9): 1109‒24.

20.   Forsum U, Larsson PG, Spiegel C. Scoring vaginal fluid smears for diagnosis of bacterial vaginosis: need for quality specifications. APMIS 2008; 116(2): 156‒9.

21.   Verhelst R, Verstraelen P, Cools P, Lopes dos Santos Santiago G ,. Temmerman M, Veneechoutte M. Garnderella. In: Liu D, editor. Molecular detection of human bacterial pathogens. Boca Raton: Press Taylor & Fracis Group; 2011; p. 81‒95.

22.   Diop K, Dufour JC, Levasseur A, Fenollar F. Exhaustive repertoire of human vaginal microbiota. Human Microbiome J 2019; 11: 100051.

23.   van den Munckhof EHA, van Sitter RL, Boers KE, Lamont RF, Te Witt R, le Cessie S, et al. Comparison of Amsel criteria, Nugent score, culture and two CE-IVD marked quantitative real-time PCRs with microbiota analysis for the diagnosis of bacterial vaginosis. Eur J Clin Microbiol Infect Dis 2019; 38(5): 959‒66.

24.   Dhiman N, Yourshaw CJ, Chintalapudi MR, Turner C, Murphy E. Diagnostic Evaluation of a Multiplex Quantitative Real-Time PCR Assay for Bacterial Vaginosis. J Women’s Health Care 2016; 5: 1‒3.

Published
2023/02/13
Section
Original Paper