RESEARCH ARTICLE

https://doi.org/10.5005/jp-journals-10045-00234
The Journal of Medical Sciences
Volume 9 | Issue 1–4 | Year 2023

Cross-sectional and Prospective Study of Aerobic Vaginitis and Its Outcomes in Pregnant Women Attending a Rural Teaching Hospital, Telangana

Kalpana Basany¹, Meera Rajgopal², Mahathi Nadella³, Kiranmai Sannithi⁴ https://orcid.org/0000-0002-6449-4834

^1–3Department of Obstetrics & Gynecology, MediCiti Institute of Medical Sciences, Ghanpur, Hyderabad, Telangana, India

⁴Department of Microbiology, MediCiti Institute of Medical Sciences, Hyderabad, Telangana, India

Corresponding Author: Kiranmai Sannithi, Department of Microbiology, MediCiti Institute of Medical Sciences, Hyderabad, Telangana, India, Phone: +91 9885511234, e-mail: kiranmai_microb@mims.edu.in

Received: 21 December 2022; Accepted: 15 September 2023Published on: 19 October 2023

ABSTRACT

Aims and background: Aerobic vaginitis (AV) is an alteration in vaginal bacterial flora. AV has drawn attention because of its threat to women’s reproductive health and pregnancy. If AV is not diagnosed early and treated correctly, it can diffuse in the genital apparatus and during pregnancy can cause abnormal outcomes like preterm birth, premature rupture of membrane (PROM) chorioamnionitis, etc. Little is known about the treatment’s success in reducing adverse pregnancy outcomes in mothers with AV infection. The study aims to report the prevalence of AV in pregnant women and to provide evidence of the threat of AV on pregnancy outcomes.

Materials and methods: Vaginal swab specimens were obtained from females attending the obstetric outpatient department (OPD) from June 2021 to May 2022. Swab samples were immediately sent to the laboratory for Gram stain, AV scoring, and culture and sensitivity. All participants were followed up to evaluate pregnancy outcomes.

Results: A total of 197 pregnant women enrolled in the study, 21 (10.7%) women were having AV. The majority of the isolates belong to the Staphylococcus species (47.9%, 11/23) followed by Escherichia coli (E. coli) (26.1%, 6/23). Antibiotic resistance has shown to be minimal.

Conclusion: Screening of all pregnant women for infections like AV contributes to the improvement of pregnancy outcomes.

Clinical significance: Knowing the incidence of the infection and its outcomes improves the standard of care among pregnant women.

How to cite this article: Basany K, Rajgopal M, Nadella M, et al. Cross-sectional and Prospective Study of Aerobic Vaginitis and Its Outcomes in Pregnant Women Attending a Rural Teaching Hospital, Telangana. J Med Sci 2023;9(1–4):00234.

Keywords: Aerobic vaginitis scoring, Follow-up, Pregnancy outcomes, Vaginitis

INTRODUCTION

Aerobic vaginitis (AV) is an opportunistic infection of endogenous origin due to disruption of the normal vaginal flora. AV was first named by Donders et al. in the year 2002. It is characterized by infection with aerobic bacteria leading to vaginal inflammation and the presence of parabasal epitheliocyte.¹

The AV has drawn attention because of its threat to women’s reproductive health and pregnancy. The presence of abnormal microbial flora in the vagina of pregnant women is to be considered a major risk factor for preterm delivery, preterm labor, premature rupture of membranes (PROM), ascending chorioamnionitis, fetal funisitis, and low birth weights (LBWs).²^–⁵

The AV is a disturbance in the vaginal flora that is different from bacterial vaginosis (BV). AV is characterized by an increased inflammation and immune response, unlike the suppressed immune response seen in BV. In AV, reduction in hydrogen peroxide-producing lactobacilli and multiplication of aerobic bacteria, like gram-negative bacilli, Escherichia coli (E. coli) or gram-positive cocci Staphylococcus aureus (S. aureus), group B Streptococcus and Enterococci. An increased pH and signs of inflammation with leukocyte infiltration are also seen.¹^,²^,⁶^–⁸ Inflammatory markers like interleukin-1 (IL-1), IL-6, and IL-8 are raised in AV. The fivefold rise in IL-6 is observed in AV.⁶^,⁹ IL-6 is an important marker of bacterial amnionitis and preterm delivery.⁹ Significant rise in IL-8 is observed in neonatal infections and the first 24 hours of severe necrotizing enterocolitis (NEC).¹⁰

Signs and symptoms of AV include inflamed vaginal mucosa, vaginal itching or burning sensation, dyspareunia, sticky yellow discharge, absence of fishy odor, vaginal pH >4.5 and increased leukocytes.¹^,²^,⁸ The appearance of parabasal cells and modification of vaginal epithelial cells morphology to rounded is seen in moderate or severe AV.¹¹

Four criteria for diagnosis of AV are:

Lactobacillary grading.
Proportional number of leukocytes.
Background flora.
Epithelial cells.

A composite scoring system called AV score is used for grading AV as mild AV (0), moderate AV (1), or severe AV (2) similar to the nugent scoring system for BV.²^,⁸ Light microscope with high power objective is used to calculate the AV score.

The AV is transmitted by sexual contact prevalently; habits like personal hygiene have a significant role in the pathogenesis of AV. If treatment and diagnosis of AV are not done promptly, it can disseminate in the genital apparatus and affect pregnancy.¹² Asymptomatic genital infection is predominantly seen during pregnancy as reported in the literature.¹³ There is a clear indication that even an asymptomatic AV may be a risk factor for preterm delivery¹⁴^,¹⁵ and other abnormal pregnancy outcomes.²^,⁴^,⁵ Maternal and fetal complications of intrauterine infections are inflammation of the fetal membranes, prostaglandin synthesis, and metalloprotease release. As the chorionic membrane and amniotic membranes weaken, stimulation of uterine contractions and ripening of cervix is induced leading to premature birth and preterm delivery.¹⁶

Treatment with broad-spectrum antibiotics like aminoglycosides, kanamycin and quinolones, and moxifloxacin are proven effective for AV. AV responds better with conventional treatment than metronidazole, as in BV. In pregnant women with AV, clindamycin is a better alternative. Women with abnormal vaginal flora may benefit from tropical preparations and the use of probiotics.¹⁷^–¹⁹

No proven evidence of success is reported in preventing the adverse outcomes of pregnancy on the treatment of AV, but it is suspected that treatment failure is leading to the emerging drug resistance in bacteria causing AV. No standard treatment is available to address the adverse pregnancy outcomes in AV-infected pregnant women.²⁰ Antibiotic sensitivity pattern of vaginal pathogens causing AV which can to a great extent aid in the proper management of AV and substantially bring down the morbidity and mortality of both mother and newborn.

To study the relationship between pregnancy outcomes and AV infection and AV infection of mothers, a better understanding of the rate of infections is required to formulate the strategies. Early diagnosis and prompt treatment of AV may significantly decrease the risk of adverse pregnancy outcomes. More studies are required to relate AV with adverse pregnancy outcomes, emphasizing the need for the study of AV in pregnancy.

AIMS AND OBJECTIVES

The aim of the present study is to know the prevalence of AV in pregnant women, to know the most common bacteria and their sensitivity pattern in AV infection and to assess the effect of AV on adverse pregnancy outcomes.

MATERIALS AND METHODS

Samples

Vaginal swab specimens were obtained from pregnant women attending the Obstetric Outpatient Department (OPD) of MediCiti Institute of Medical Sciences (MIMS) for their regular prenatal visits in the third trimester of pregnancy from June 2021 to May 2022.

Sample Size

The prevalence of AV in pregnant females ranges from 4.5 to 9.2%. With a precision of 0.04 and a z-score of 1.96, the sample size is calculated as 197.

Study Design

Cross-sectional and prospective study to know the prevalence of AV and its association with pregnancy outcomes along with the characterization of species and its sensitivity pattern.

Inclusion Criteria

Intrauterine pregnancy.
Singleton pregnancy.
Third trimester (>24 weeks) of pregnancy.
And intact fetal membranes.

Exclusion Criteria

Use of antibiotics in the past 1 week.
Congenital genital tract deformities.
Presence of comorbid diseases [diabetes mellitus (DM), hypertension, etc].
Bad obstetric history.
Women with pregnancy complications like placenta previa, antepartum hemorrhage (APH), gestational DM (GDM), etc.

Human Subjects’ Protection

Written informed consent was obtained from participants. We have used unique identification numbers for each participant to maintain confidentiality. Ethical board approval for the study was sought from MIMS.

Data Collection

Data was collected using a close-ended questionnaire administered to participants. A complete medical history was taken with reference to age, address, occupation, presenting complaints (type of discharge, odor, pain, itching, etc.), obstetric history, history, family history, treatment history, and personal history was noted with the help of questionnaire.

Sample Collection and Transport

All participants have undergone gynecological examinations and vaginal swab collection. Sterile swabs were used for obtaining vaginal swab samples from the posterior fornix for vaginal pH measurements, microscopy, aerobic culture, and sensitivity. Two vaginal swab samples were collected from each participant. By speculum examination the following findings were noted:

The characteristics of vaginal discharge (color, quantity, appearance, and odor).
The appearance of vaginal mucosa (edema, ulcer, and erythema).
And the presence of inflammation in the cervix (redness and discharge).

These swab samples were immediately sent to the laboratory for further processing.

Sample Processing

The sample from the first swab was spread over two slides for microscopy. A discharge sample on one slide is used for wet mount and examined at 400× magnification with a compound microscope. Visual detection of leukocytes, lactobacilli (seen as long rods), background flora, epithelial cells etc. and AV score 1–2 was determined and graded as per Table 1. Diagnostic criteria of AV (400× magnification). AV score of <3 corresponds to no signs of AV, 3–4 to mild AV, 5–6 to moderate AV, and >6 to severe AV.

**Table 1:** Diagnostic criteria of AV (400× magnification)
AV score	Lactobacillary grades (LBG)	Number of leukocytes	Proportion of toxic leukocytes	Background flora	Proportion of parabasal epitheliocytes (PBCs)
0	I and IIa	≤10/hpf	None of sporadic	Unremarkable or cytolysis	None of ≤1%
1	IIb	>10/hpf and ≤10/epithelial cell	≤50% of leukocytes	Small coliform bacilli	≤10%
2	III	>10/epithelial cell	>50% of leukocytes	Cocci or chains	>10%

hpf, high power field (400 times magnification); LBGI, numerous pleomorphic lactobacilli, no other bacteria; LBGIIa, mixed flora, but predominantly lactobacilli; LBGIIb, mixed flora, proportion of lactobacilli severely decreased due to increased number of other bacteria; LBGIII, lactobacilli severely depressed or absent because of overgrowth of other bacteria

The second slide was Gram stained for determining the organisms.²¹ The other swab sample was used for culture and sensitivity. Samples were plated on blood agar, chocolate agar, and MacConkey agar²² and incubated at 37°C for 24–48 hours. The isolates were identified based on their Gram staining, colony and cultural characteristics, and biochemical reactions were performed as per the standard laboratory procedures.²³ The antibiotic susceptibility testing of the isolates was performed on Mueller Hinton agar plates by the Kirby–Bauer disk diffusion technique as per the Clinical and Laboratory Standards Institute guidelines.²⁴ The diameter of each zone of inhibition around the disk was measured and compared with the zone size interpretative chart and results were recorded.

Follow-up

All participants were followed up till delivery to assess the pregnancy outcomes and notes.

Diagnostic Criteria

Preterm births: Births that occur at a gestational age <37 weeks.²⁵
Stillbirth: No signs of life.²⁶
Low birth weight: Birth weight <2500 gm.²⁷
PROM: Premature rupture of membranes.²⁸
Neonatal asphyxia: If appearance, pulse, grimace, activity, and respiration (APGAR) score is recorded <7 after birth at 1/5 minutes, pH of umbilical artery <7.15 and other causes of a low score to be ruled out.²⁹

Statistical Analysis

Statistical analysis was performed by Statistical Package for the Social Sciences 20.0 software. Data represented in mean ± standard error of the mean. The p-value is used to calculate the strength of association between the factors. The p-value < 0.05 was considered statistically significant. The association between AV and pregnancy outcomes was done by univariate logistic regression analysis.

RESULTS

A total of 197 swab samples were collected from 197 pregnant women in their third trimester on their visit to the obstetrics and gynecology department for checkups. All the samples collected were sent to the microbiology lab for AV scoring and culture. Of the 197 pregnant women enrolled in the study, 21 (10.7%) women were having AV.

All the participants enrolled were of the age-group 18–40 years, and the mean age of participants was 22 ± 3.2 years. All these 197 pregnant women were successfully followed up for abnormal pregnancy outcomes. In the lab, the AV score was calculated for all 197 samples. Among the positive samples, 74% (17/21) had mild AV, 21.7% (5/21) had moderate AV and 4.3% (1/21) showed severe AV.

A total of 23 isolates were identified from 21 samples of pregnant women with AV. The majority of the isolates belonged to the Staphylococcus species (47.9%, 11/23) followed by E. coli (26.1%, 6/23). The distribution of bacterial isolates is depicted in Figure 1.

Fig. 1: Distribution of bacterial isolates

Antibiotic susceptibility was performed for all the isolates. Antibiotic resistance was shown to be minimal as only three (13%) isolates (two E.coli and one Klebsiella) were shown to be extended-spectrum β-lactamase producers. Others showed susceptibility to all the antibiotics except penicillins and macrolides.

Clinical characteristics of all the women including age, hygiene, obstetric history and history of vaginitis were recorded before delivery and PROM, delivery mode, APGAR score, stillbirth, and neonatal infections were recorded after delivery. Clinical characters and pregnancy outcomes of women are given in Table 2.

**Table 2:** Clinical characters and pregnancy outcomes
Risk factor	Pregnant women with AV (n = 21)	Pregnant women without AV (n = 176)	Odds ratio	p-value
Clinical characters
Age >25 years ≤25 years	10 11	71 105	1.34	0.52
Educational status Literate Illiterate	13 8	152 24	3.89	0.0065
Personal hygiene Maintained Not maintained	12 9	142 34	3.13	0.0175
History of vaginal infection Present Absent	11 10	90 86	1.0511	0.9141
Symptoms Discharge Itching Others Asymptomatic	4 1 8 8	8 1 32 135	5.35	0.0005
AV score 0 1 2	17 5 1	148 28 0	1.8655	0.2284
Pregnancy outcomes
Preterm	2	13	1.1941	0.8232
LBW	7	28	2.6428	0.0275
Intrauterine death (IUD)	1	1
Stillbirth	1	2
PROM	1	16	0.5	0.257
APGAR score <5 >5	2 21	8 162	1.928	0.212
Delivery mode Normal Cesarean section	7 14	69 107	0.775	0.301

A total of 199 neonates of 197 mothers (as two had twins) were followed up till the discharge from the hospital. Among them, 35 (17.6%) neonates had low birth weight. Among them, seven (3.5%) neonates had AV-positive mothers.

DISCUSSION

Aerobic vaginitis (AV) is a vaginal condition which is often wrongly treated as BV.¹ Though lactobacillary disruption is seen in both conditions, AV differs profoundly. The occurrence of AV in the current study 10.7% was consistent with the results of studies on AV in pregnancy the study by Zodzika et al.³⁰ was 10.79%, a study by Sangeetha et al.³¹ was 9.52% and in a study by Tang et al.³² on AV in late pregnancy, it was only 4.2%. The maximum number of cases in the study was diagnosed as mild AV, 80.9% which correlated with studies done by Zodzika et al., and Sangeetha et al., In developing countries like India, pregnant ladies maintain good personal hygiene may lead to the relatively low incidence of AV in pregnant individuals. Decreased sexual contact and risk of transmission from the partners is less during the pregnancy period. A high percentage of lactobacillus flora due to estrogen levels reduce the multiplication of pathogenic organisms and moreover, frequent visit to the gynecologist for antenatal checkup leads to early diagnosis and care of the patients.

In this study, Staphylococcus species was the prevalent pathogen followed by E. coli. In a study by Tempera et al. and Tempera et al., E. coli was the most frequently isolated pathogen³³ and a study by Fan et al. in 2013³⁴ showed Enterococcus faecalis, E. coli, and coagulase negative staphylococcus (CONS) were the most frequently isolated organisms. Antibiotic resistance shown was much less compared to the isolates from the clinical samples.

We have performed prospective follow-up to strengthen the evidence of an association between AV and adverse pregnancy outcomes. AV may be an independent risk factor associated with adverse pregnancy outcomes like PROM, neonatal asphyxia, low birth weight, preterm delivery, and others compared to others. In 2001, Donders et al. showed that AV is associated with preterm birth.¹ As AV has been established for increased inflammation leading to chorioamnionitis and funisitis, it may have other unknown complicated pathways causing these adverse pregnancy outcomes.²

CONCLUSION

In the pathogenesis of AV, personal hygiene habits play an important role. Screening of all pregnant women for infections like AV, BV, and VVC contributes to a decrease in adverse pregnancy outcomes. Antibiotic sensitivity-based treatment must be followed to not create multidrug resistance and disturb the normal flora.

*Clinical Significance

Knowing the incidence of the infection and its outcomes improves the standard of care among pregnant women.

DECLARATION

Ethics Approval and Patient Consent to Participate

Ethical approval is sought from the Institutional Ethical Approval Board MediCiti Institute of Medical Sciences (MIMS). Written informed consent was obtained from participants. We have used unique identification numbers for each participant to maintain confidentiality.

Author Contributions

Conceptualization, data curation, formal analysis, investigation, methodology, project administration, resources, supervision, validation, visualization and writing of the draft.

Availability of Data and Materials

Data and materials were collected by the authors.

ORCID

Kiranmai Sannithi https://orcid.org/0000-0002-6449-4834

REFERENCES

1. Donders GG, Vereecken A, Bosmans E, et al. Definition of a type of abnormal vaginal flora that is distinct from bacterial vaginosis: aerobic vaginitis. BJOG 2002;109(1):34–43. DOI: 10.1111/j.1471-0528.2002.00432.x

2. Donders G, Bellen G, Rezeberga D. Aerobic vaginitis in pregnancy. BJOG 2011;118(10):1163`–1170. DOI: 10.1111/j.1471-0528.2011.03020.x

3. Donders GG, Van Calsteren K, Bellen G, et al. Predictive value for preterm birth of abnormal vaginal flora, bacterial vaginosis and aerobic vaginitis during the first trimester of pregnancy. BJOG 2009;116(10):1315–1324. DOI: 10.1111/j.1471-0528.2009.02237.x

4. Rabiee S, Arab M, Yousefi MR. Epidemiologic pattern of vaginal colonization by group B Streptococcus in pregnant women in Hamadan, Central West of Iran. Iran J Med Sci 2006;31(2):106–108.

5. Najmi N, Jehan I, Sikandar R, et al. Maternal genital tract colonization by group-B Streptococcus: a hospital based study. J Pak Med Assoc 2013;63(9):1103–1107. http://ecommons.aku.edu/pakistan_fhs_mc_women_childhealth_obstet_gynaecol/47

6. Hemalatha R, Ramalaxmi BA, KrishnaSwetha G, et al. Cervicovaginal inflammatory cytokines and sphingomyelinase in women with and without bacterial vaginosis. Am J Med Sci 2012;344(1):35–39. DOI: 10.1097/MAJ.0b013e318235597b

7. MacPhee RA, Miller WL, Gloor GB, et al. Influence of the vaginal microbiota on toxic shock syndrome toxin 1 production by Staphylococcus aureus. Appl Environ Microbiol 2013;79(6):1835–1842. DOI: 10.1128/AEM.02908-12

8. Tansarli GS, Kostaras EK, Anthanasiou S, et al. Prevalence and treatment of aerobic vaginitis among non-pregnant women: evaluation of the evidence for an underestimated clinical entity. Eur J Clin Microbiol Infect Dis 2013;32(8):977–984. DOI: 10.1007/s10096-013-1846-4

9. Donati L, Di Vico A, Nucci M, Quagliozzi L, et al. Vaginal microbial flora and outcome of pregnancy. Arch Gynecol Obstet 2010;281(4):589–600. DOI: 10.1007/s00404-009-1318-3

10. Wang S, Hibberd ML, Pettersson S, et al. Enterococcus faecalis from healthy infants modulates inflammation through MAPK signaling pathways. PLoS One 2014;9(5):e97523. DOI: 10.1371/journal.pone.0097523

11. Donders GG. Definition and classification of abnormal vaginal flora. Best Pract Clin Obstet Gynaecol 2007;21(3):355–373. DOI: 10.1016/j.bpobgyn.2007.01.002

12. Zarbo G, Coco L, Leanza V, et al. Aerobic vaginitis during pregnancy. Res Obstet Gynecol 2013;2(2):7–11. DOI: 10.5923/j.rog.20130202.01

13. Akerele J, Abhulimen P, Okonofua F. Prevalence of asymptomatic genital infection among pregnant women in Benin City, Nigeria. Afr J Reprod Health 2002;6(3):93–97. DOI: 10.2307/3583261

14. Stojanovic N, Plecas D, Plesinac S. Normal vaginal flora, disorders and application of probiotics in pregnancy. Arch Gynecol Obstet 2012;286(2):325–332. DOI: 10.1007/s00404-012-2293-7

15. Honda H, Yokoyama T, Akimoto Y, et al. The frequent shift to intermediate flora in preterm delivery cases after abnormal vaginal flora screening. Sci Rep 2014;4:4799. DOI: 10.1038/srep04799

16. Goldenberg RL, Hauth JC, Andrews WW. Intrauterine infection and preterm delivery. N Engl J Med 2000;342(20):1500–1507. DOI: 10.1056/NEJM200005183422007

17. Heczko PB, Tomusiak A, Adamski P, et al. Supplementation of standard antibiotic therapy with oral probiotics for bacterial vaginosis and aerobic vaginitis: a randomised, doubleblind, placebo-controlled trial. BMC Womens Health 2015;15:115. DOI: 10.1186/s12905-015-0246-6

18. Tomusiak A, Strus M, Heczko PB, et al. Efficacy and safety of a vaginal medicinal product containing three strains of probiotic bacteria: a multicenter, randomized, double-blind, and placebo-controlled trial. Drug Des Devel Ther 2015;9:5345–5354. DOI: 10.2147/DDDT.S89214

19. Russo R, Edu A, De Seta F. Study on the effects of an oral lactobacilli and lactoferrin complex in women with intermediate vaginal microbiota. Arch Gynecol Obstet 2018;298(1):139–145. DOI: 10.1007/s00404-018-4771-z

20. Han C, Wu W, Fan A, et al. Diagnostic and therapeutic advancements for aerobic vaginitis. Arch Gynecol Obstet 2015;291(2):251–257. DOI: 10.1007/s00404-014-3525-9

21. Mackie TJ, McCartney JE. Laboratory strategy in the diagnosis of infective syndromes. In:Collee JG, Fraser AG, Marmion BP, Simmons A, (Eds). Practical Medical Microbiology, 14th edition. Edinburg: Churchill Livingstone; 2006. p. 796.

22. Forbes BA, Daniel FS, Alice SW. Baily and Scott’s Diagnostic Microbiology, 12th edition. USA: Mosby Elsevier Company; 2007. p. 867.

23. Allen SD, Janda WM, Koneman EW, et al. Koneman’s Color Atlas and Textbook of Diagnostic Microbiology, 6th edition. Philadelphia: Lippincott; 2005. pp. 1443–1535.

24. CLSI - Clinical and Laboratory Standards Institute 2013. Performance standards for antimicrobial susceptibility testing. Twenty-third informational supplement. Wayne, PA, USA: CLSI; 2013. pp. M100-S23.

25. Slattery MM, Morrison JJ. Preterm delivery. Lancet 2002;360(9344):1489–1497. DOI: 10.1016/S0140-6736(02)11476-0

26. Blencowe H, Cousens S, Jassir FB, et al. National, regional, and worldwide estimates of stillbirth rates in 2015, with trends from 2000: a systematic analysis. Lancet Glob Health 2016;4(2):e98–e108. DOI: 10.1016/S2214-109X(15)00275-2

27. World Health Organization. International statistical classification of diseases and related health problems, 10th revision, Fifth edition, 2016. World Health Organization. 2015. http://www.who.int/iris/handle/10665/246208

28. Committee on Practice Bulletins-Obstetrics. ACOG practice bulletin no. 188: prelabor rupture of membranes. Obstet Gynecol 2018;131(1):e1–e14. DOI: 10.1097/AOG.0000000000002455

29. Chen ZL, Liu J. Interpretation of the experts’ consensus on the criteria for the diagnosis and grading of neonatal asphyxia in China. Transl Pediatr 2013;2(2):59–63. DOI: 10.3978/j.issn.2224-4336.2013.04.02

30. Zodzika J, Jermakowa I, Rezeberga D, et al. Factors related to elelvated vaginal pH in the first trimester of pregnancy. Acta Obstet Gynecol Scand 2011;90(1):41–46. DOI: 10.1111/j.1600-0412.2010.01011.x

31. Sangeetha KT, SarojGolia, Vasudha CL. A study of aerobic bacterial pathogens associated with vaginitis in reproductive age group women (15-45 years) and their sensitivity pattern. Int J Res Med Sci 2015;3(9):2268–2273. DOI: 10.18203/2320-6012.ijrms20150615

32. Tang Y, Yu F, Hu Z, et al. Characterization of aerobic vaginitis in late pregnancy in a Chinese population: a STROBE-compliant study. Medicine 2020;99(25):e20732. DOI: 10.1097/MD.0000000000020732

33. Tempera G, Bonfiglio G, Cammarata E, et al. Microbiological/clinical characteristics and validation of topical therapy with kanamycin in aerobic vaginitis: a pilot study. Int J Antimicrob Agents 2004;24(1):85–88. DOI: 10.1016/j.ijantimicag.2003.12.013

34. Fan A, Yue Y, Geng N, et al. Aerobic vaginitis and mixed infections: comparison of clinical and laboratory findings. Arch Gynecol Obstet 2013;287(2):329–335. DOI: 10.1007/s00404-012-2571-4

________________________
© The Author(s). 2023 Open Access This article is distributed under the terms of the Creative Commons Attribution 4.0 International License (https://creativecommons.org/licenses/by-nc/4.0/), which permits unrestricted use, distribution, and non-commercial reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated.