Clinical correlation and laboratory diagnosis of bacterial vaginosis.
Bacterial vaginosis is characterised by a heavy overgrowth of gram-negative and gram-positive anaerobes with no signs of inflammation and regarded as a microbiological and immunological enigma. (1) It occurs in up to 25% of the general population with more than half of the women being asymptomatic.2. Although, its exact aetiology is unknown. It has been linked to high-risk sexual behaviours such as lack of condom use and multiple sex partners. (3,4) The chief complaint is a malodorous vaginal discharge. (2,5,6,7,8) It has a polymicrobial aetiology that includes Gardnerella vaginalis, Mycoplasma hominis, and various obligate anaerobes like Bacteroides, Prevotella, Porphyromonas, Peptostreptococcus, Peptococcus, Veillonella, Eubacterium, Mobiluncus, (5,6,8,9) Peptoniphilus, and Fusobacterium. (10) Many clinicians empirically diagnose the aetiology of a vaginal discharge without the aid of laboratory tests and this often leads to a misdiagnosis. (11,12) In view of this, the present study was done to identify the causative organisms from clinically suspected cases of BV among non-pregnant women compare the utility of various methods for the diagnosis of this condition and correlate the association with other associated sexually transmitted infections.
MATERIAL AND METHODS
This prospective study involving total 600 non-pregnant women with abnormal vaginal discharge attending the Gynaecology OPD at a tertiary care hospital was done over a period of one year.
Young non-pregnant sexually active females with excessive vaginal discharge in the reproductive age group of 15-45 years.
Age below 15 years, age older than 45 years, pregnant, menstruating, history of antibiotics, and/or topical vaginal creams within seven days prior to the date of examination.
The Institutional Ethics Committee approval was taken. Informed consent of the participants was obtained. Participants were asked about their symptoms, past illness, and previous treatment before undergoing gynaecological examination. In the gynaecological OPD, after assuring the patient, a clean unlubricated Cusco's vaginal speculum was passed into the vagina to examine the condition of the vaginal wall, cervix, and characteristics of the discharge [with respect to amount, odour, and type of discharge, which was described as normal (Mucoid or floccular), purulent, curdy, or thin and homogenous. The following samples were collected from each subject: Three vaginal swabs and one blood sample (5 mL). The vaginal sample was collected by swabbing the posterior and lateral vaginal fornices with a cotton-tipped sterile swab. Three vaginal swabs were taken and immediately sent to the microbiology laboratory for processing. After aseptic precautions, 5 mL blood was collected from cubital vein, for serological diagnosis of Hepatitis B and C and the patient was directed to ICTC Centre for HIV and VDRL testing. In the laboratory, the processing was as follows: For the 3 vaginal swabs: 1. First swab was immediately processed by inoculating on Brucella blood agar with Hemin and Vitamin K1 supplement for anaerobes, (13) Human Blood Bilayer (HBT) agar for detection of Gardnerella vaginalis, New York City agar for Neisseria gonorrhoeae, and Sabouraud dextrose agar for Candida. 2. A second swab was used to inoculate a tube of thioglycollate broth by gently introducing the swab into the lower half of the tube and rubbing it against the wall of the tube. The swab was subsequently mixed with two drops of sterile saline on a clean glass slide and a coverslip was placed over it. This wet mount was immediately examined using bright field microscopy under high power objective (x40) for clue cells and jerking motility of Trichomonas vaginalis. 3. Third swab was used for smear, pH test, whiff test, and KOH mount the swab was then mixed with 2 drops of 10% potassium hydroxide on a slide and immediately held close to nose to detect the fishy odour associated with volatile amines (Whiff amine test). A diagnosis of BV was made using Amsel's clinical criteria (5), if three of the following four criteria were present: A thin, homogenous discharge with milk-like consistency tending to adhere to the vaginal vault, Vaginal pH >4.5, positive whiff amine test, and presence of clue cells. For diagnosis by Nugent's Gram stain criteria: Morphotypes were scored as the average number seen per oil immersion field. A total of 100 fields were examined for each slide. Total score-Lactobacillus+Gardnerella and Bacteroides spp. + curved rods. (14) Women who had a score of 7 or higher were considered to have BV, score of 4-6 were termed as intermediate vaginal flora and 0-3 as normal flora. For detection of yeast, Gram stain was screened for the presence of gram-positive budding yeast cells, and pseudohyphae. The presence of intracellular gram-negative diplococci within the polymorphonuclear leucocytes was presumptively diagnosed as Neisseria gonorrhoeae. For culture identification of anaerobes, Brucella blood agar with Hemin and Vitamin [K.sub.1] supplement was incubated for 48 hours and examined for growth. The plates were kept for 7 days before final examination and then discarded. The thioglycollate broth was kept for 7 days at 370[degrees]C. If no anaerobes were isolated from the primary plates after 7 days incubation, then the broth was subcultured onto Brucella blood agar with Hemin and Vitamin K1 supplement plates. For identification of anaerobes: Each distinct anaerobe colony was examined and its morphology noted. A portion of the colony was Gram stained and inoculated onto the following media: 1) Chocolate agar plate incubated in a candle jar for 48 hours to test the isolate for aerotolerance. 2) Brucella blood agar with Hemin and Vitamin [K.sub.1] supplement for the antibiotic identification test. 1 mg kanamycin disc, 5 ng vancomycin disc, and 10 [micro]g Colistin disc were placed well separated from each other. The plate was incubated anaerobically for 48 hours at 37[degrees]C. A zone diameter of [less than or equal to] 10 mm indicated resistance while a zone diameter >10 mm indicated sensitivity. For Gardnerella vaginalis: Human Blood Bilayer with Tween (HBT) agar with selective supplement (From HiMedia) and New York City (NYC) agar with NYC supplement (From HiMedia) were inoculated. Sodium polyanethole sulfonate (SPS) disc indicator was used. Both HBT and NYC agar plates were incubated at 370[degrees]C for 48 hrs. and 72 hrs. respectively in a C[O.sub.2] enriched humid atmosphere achieved by using candle jar. The blood sample was kept in room temperature for a minimum 1 hr and the serum was used for the following tests: ELISA for anti-HCV detection (3rd generationSD Bioline) and ELISA for HBsAg detection (Sun Pharma).
In this prospective study involving a total of 600 non-pregnant women with abnormal vaginal discharge, 142/600 (23.7%) had BV. The distribution of cases based on Nugent's score was as follows: normal group: 223 followed by intermediate: 161 and BV: 142 (Table 1). Based on aetiology, it was seen that mixed infection occurred in 42/600 cases: Vulvovaginal candidiasis (VVC)+Intermediate in 24, BV+VVC in 16 and BV+ Trichomoniasis in 2 (Table 2). BV was commonly seen in 36-45 yrs. age group: 55/135(40.7%), which was statistically significant p value (<0.05). Married women comprised 593/600(98.8%); BV occurred in 140/593(23.6%) of them. Recurrent vaginal discharge occurred in 259/600 of which 92(35.5%) were associated with BV. This association was significant with Pearson chi-square ([chi square]) 35.405, continuity correction 34.305, df-1 and p-value of 4.71E-09. Abnormal discharge was most commonly seen (193/600) in women who had not used any contraceptives. Majority of the women with BV were sterilised with TL (55/142); very few used OC pills (1/142), condom (10/142), and other methods (10/142) such as diaphragm, sponge, spermicidal jelly/foam, etc. Foul smelling discharge was more in BV patients as compared to pain, itching, and burning micturition, which was more common in NBV, and was statistically significant p value (<0.05 ). Clue cells were seen in a total of 19/142 (13.3%) BV patients of which majority i.e. 13/19 had Nugent's score of 8 followed by 4/19 with Nugent's score of 7 and one each with Nugent's score of 9 and 10. Amsel's criteria were able to detect BV in 167/600 (27.8%) [Table 3]. Of these, Nugent's Gram stain criteria was negative in 50. On the contrary, 25 patients who did not satisfy the Amsel's clinical criteria were positive by Nugent's Gram stain. The inter-rater agreement statistic (Kappa) was determined between the Amsel's criteria and Nugent's score (Kappa=0.674). Majority of anaerobes i.e. 100/136 (73.5%) were found in BV patients. This association of anaerobes in BV was found to be significant with p-value (<0.05). Curved gram-negative rods suggestive of Mobiluncus spp. were most commonly seen microscopically in BV cases (30.3%) followed by Peptostreptococcus spp. (27.5%) and Bacteroides spp. (21.8%). Gardnerella vaginalis was not isolated. Yeast was grown in 105/600 (17.5%), 16/105 (11.3%) were significantly associated with BV (p<0.05). In our study, HIV infection was seen in 0.7%, HBV infection occurred in 0.3%, and HCV occurred in 0.2%.
(In the present study, BV was diagnosed in 23.7% based on Nugent's criteria).
*N=Non-pregnant; P=Pregnant; SAW=Sexually active women.
For diagnosis by Nugent's Gram stain criteria14: Morphotypes were scored as the average number seen per oil immersion field. A total of 100 fields were examined for each slide. Total score = Lactobacillus + Gardnerella and Bacteroides spp.+curved rods. Women who had a score of 7 or higher were considered to have BV, score of 4-6 were termed as intermediate vaginal flora, and 0-3 as normal flora.
In our study involving 600 non-pregnant women with abnormal vaginal discharge, BV was diagnosed in 23.7% (Based on Nugent's criteria). Among the Indian studies, Adamson et al (15) Modak et al (16) Uma et al (17) and Kosambiya et al (18) reported similar results (Fig. 1). Higher rate have been reported by Becker et al (19) Thulkar et al (20) and Aggrawal et al (21) Slightly lower rate was reported by Indu et al (22) Madhivanan et al (4) Patel et al (23) whereas very low infection was noted by Mania et al (24) Shethwala et al (25) and Ray et al (26) Highest number (68%) was noted in a study by Aggrawal et al (21) where Amsel's clinical criteria was used as standard. Also, a meta-analysis by Gillet et al (27) showed a higher rate (32%). In our study, Vulvovaginal Candidiasis (VVC) was noted in 14.8%; similar findings were reported 14% by Kosambiya et al (18) in Surat, India and 15.7% River et al (28) in USA. Higher rate of VVC, 17.4% was noted by Esim et al (29) and Xiao et al (3021.87%) in China. Indu et al (22) reported 9%, which was low. In our study, 2.27% cases had mixed infection of BV/VVC, which was close to 4.4% reported by River et al (28) 3% by Indu et al (22) in North India and 4.2% by Mania et al (24) in Mumbai; slightly less (1.36%) was found by Xiao et al. (30) In our study, Trichomoniasis was seen in 9/600 (1.5%) and mixed infection of BV/Trichomoniasis in 2/600 (0.3%). Similar reports from India are: 1.4% by Sunita et al (31) 1.2% by Patel et al (23) 1.18% by Rao et al (32) 1.2% by Ray et al. (26) Reports by Shethvala et al (25) (2%), Bhalla et al (33) 2.8%, Thulkar et al (20) 6.74%, Adamson et al 8.5%, (15) Bogearts et al 2%, (34) and Kosambiya et al 22% (18) showed higher number of cases. Studies from China reported lower infection 1.7% Youngin et al (35) and 0.67% Liu et al. (36) In the present study, majority of women with abnormal discharge 240/600 (40%) belonged to the 26-35 yrs. age group among them BV occurred in 66/240 (27.5%). Older age group (36-45 yrs.) comprised 135/600 (22.5%) and BV occurred in 55/135 (40.7%) of them. Sumati et al (37) noted that 60.11% patients were between 26 to 40 years of age and BV occurred in 52% in this age group. The mean SD (Standard deviation) and median age (Yrs.) of all cases are 29.59, 6.97, and 29 respectively whereas in BV it was 32.46, 6.10, and 33 respectively. This difference was significant with p-value 1.59 E-09 (<0.05). Modak et al (16) found the mean SD and median of overall cases to be 30.7, 10.46, and 30 almost similar to us; however, in BV cases these were 28. (33), 7.90, and 29.5 respectively, which is less compared to us. In our study, married women were 593/600 (98.8%) and 7 were widowed, which is similar to Madhivanan et al4 and Modak et al (16) Abnormal discharge was higher among women who had not used any contraceptives (193/600). Maximum women associated with BV had undergone sterilization with TL (55/142). Patel et al (23) reported similar findings. We noted that abdominal pain, itching, and burning micturition, all three inflammatory signs were less in BV compared to NBV, which was significant. In present study, 36.62% of BV patients had abdominal pain whereas it was higher (58.52%) in NBV patients. Bhalla et al (33) reported abdominal pain in 24.3% BV patient and Patel et al (23) in only 18.6%. Itching was noted in 247/600 (41.2%) of total patients and 17/142 (11.97%) of BV cases. Kosambiya et al (18) reported itching in 10/42 (23.8%) patients with discharge and Patel et al (23) in 19.3% of BV cases. In present study, burning micturition was seen in 241/600 and 30/241 (12.4%) had BV, which was lower than 20.4% by Patel et al (23) In our study, 88.03% BV cases had foul-smelling discharge compared to 18.12% in NBV, which was similar to 68.6% and 100% by Figueiredo et al (38) and Hapsari et al (39) in BV. The present study showed that grey thin homogenous discharge was more common in BV patients (71.12%) similar to 84% seen by Aggrawal et al (21) Grey thin homogenous discharge had sensitivity, specificity, positive, and negative predictive values of 71.13%, 74.02%, 45.91%, and 89.21% respectively similar to Modak et al (16) (66.67%, 71.05%, 42%, and 87% respectively). Whiff test in present study had sensitivity, specificity, positive and negative predictive value of 87.32%, 84.50%, 63.59%, and 95.56% (Table 3). Modak et al (46) findings have shown sensitivity, specificity, positive, and negative predictive value of 41.67%, 100%, 100%, and 84% respectively; sensitivity being lower. Aggrawal et al (21) reported sensitivity of 68% while Hainer et al (40) observed a sensitivity and specificity of 77% and 93% respectively. Clue cells found in our study was 19/600 (3.2%) similar to 1.07% by Sunita et al. (31) The presence of clue cells was the most specific of all the criteria (Specificity=100%). It also had the highest predictive value of a positive test (100%). But, presence of clue cells was not found to be very sensitive (Sensitivity=13.38%) and gave a large number of false negative cases (86.6%) with negative predictive value of 78.82%. In our study, pH >4.5 had sensitivity, specificity, positive, and negative predictive values of 88.73%, 73.58%, 51.01%, and 95.47% respectively. Modak et al (16) noted similar findings: 83.33%, 86.84%, 67%, and 94% respectively. 88% of sensitivity was also observed by Aggrawal et al (21) Ultimately, pH seemed to be the best indicator of bacterial vaginosis, if all sensitivity, specificity, positive, and negative predictive values are taken into consideration. It was found to be most sensitive and had the best predictive value of a negative test. Furthermore, it is the one, which could be objectively measured at the bedside. In this study, the Amsel's criteria had a sensitivity of 82.39%, specificity of 89.08%, positive and negative predictive values of 70.06% and 94.23% respectively when compared to the Nugent's criteria. Modak et al (16) also found sensitivity, specificity, positive, and negative predictive values 66.67%, 94.47%, 80%, and 90% respectively. Similar parameters were reported by Schwebke et al (41) with 70.40%, 94.40%, 89%, and 83.10% respectively. Gallo et al (42) found the sensitivity and specificity of Amsel's criteria as 60% and 90% respectively; sensitivity being less compared to present study. Schwebke et al (41) compared Amsel's clinical criteria with Nugent's criteria and showed that the Nugent criteria had a higher sensitivity of 89% and Amsel's criteria had a higher specificity of 94%. It is suggested by many reports to consider Nugent's score as standard criteria as the comparatively low sensitivity of Amsel's criteria results in the decrease of true positive cases causing ineffective treatment. (16,24,20,15,43,44) Pus cells were seen in 32/142(22.5%) of BV patients compared to 104/161(64.6%) of intermediate and 108/297(50.2%) of normal group suggestive of non-inflammatory characteristic of BV. Sachdeva et al (45) also observed that "vaginal discharge of patients with BV is notable for its lack of (Polymorphs) PMNs' typically 1 or less than 1 PMN per vaginal epithelial cell." Distribution of anaerobes was as follows: curved gram-negative rods suggestive of Mobiluncus spp. were most commonly seen microscopically in BV cases (30.3%) followed by Peptostreptococcus spp. (27.5%) and Bacteroides spp. (21.8%). Evidence of association of anaerobic bacteria with BV is mounting. Aggrawal et al (21) reported Peptostreptococcus spp. (53.30%) as most common followed by Bacteroides spp. (16.7%). Rao et al (32) found Peptostreptococcus spp. and Prevotella spp. to be common among the anaerobes isolated. Sumati et al (37) found Bacteroides spp. to be more common followed by Peptococcus spp. Curved gram-negative rods were also noted by Rao et al in 8.45% BV cases. In present study' Gardnerella vaginalis was not isolated. This may be due to inadvertent error in transport or inhibition by high concentration of NACl in the Columbia base agar used in the culture medium (Catnil et al) (9) Various studies have reported isolation of Gardnerella vaginalis ranging from 10.2% Esin et al (29) 7.32% Rao et al (32) 2 8% Khan et al (46) to as high as 96.8% Figueiredo et al38 Among the STIs in our study' gonorrhea occurred in 0.3%, which was less compared to 0.5% of Bogaerts et al (34) 1.9% of Patel et al (23) 1% of Bhalla et al (33) 1.7% of Youngin et al (35) 15.8% of Wang et al (47) and 16.11% of Liu et al. (36) In our study, HIV infection was seen in 0.7%' which was less than 0.87% of Sunita et al (31) 11.6% of Shethwala et al (25) and 0.95% of Bhalla et al.33 In the present study' HBV infection occurred in 0.3%, which was low compared to 3.33% by Shethwala et al (25) (India), 0.9% by Wang et al (47) (China), 0.67% by Liu et al (114) (China) and highest 35% reported by Bogaerts et al. (34) In our study, HCV occurred in 0.2%, which was low compared to 0.5% by Wang et al (47) (China), 0.67% by Liu et al (36) (China), and 0.9% reported by Bogaerts et al (34) The limitation of the study was that we could not include Herpes and Chlamydia due to lack of funds. Further studies are required especially for detection of HBV and HCV infection in BV.
India has a high burden of reproductive morbidity and bacterial vaginosis has been documented as a risk factor for both adverse birth outcomes and HIV. Proper diagnosis of BV is challenging. It is often misdiagnosed using clinical criteria alone because the components are subjective. Many studies have suggested that the Gram stain be considered the gold standard for diagnosis of BV. Recently, although, newer diagnostic molecular methods have been devised, Nugent's and Amsel methods remain the most practical, viable, and economic option especially in developing countries.
We acknowledge the cooperation of the faculty and staff of Obstetrics and Gynaecology and Microbiology Department, TN Medical College and BYL Nair Hospital, Mumbai.
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Kirti Malpekar , Kumar Vivek , Jayanthi Shastri 
 Associate Professor, Department of Microbiology, Topiwala National Medical College, Nair Hospital, Mumbai.
 Senior Registrar, Department of Microbiology, Topiwala National Medical College, Nair Hospital, Mumbai.
 Professor and HOD, Department of Microbiology, Topiwala National Medical College, Nair Hospital, Mumbai.
Financial or Other, Competing Interest: None.
Submission 29-06-2016, Peer Review 12-07-2016, Acceptance 19-07-2016, Published 26-07-2016.
Corresponding Author: Dr. Kirti Malpekar, #404, Audumber So, 3rd Akkalkot Lane, Khadilkar Road, Girgaum, Mumbai-400004.
Table 1: Distribution Based on Nugent's Score Criteria * Diagnosis (3 Groups) No. Percentage BV 142 23.7% Intermediate 161 26.8% Normal 297 49.5% Total 600 100.0% * Nugent's score: BV 7-10; Intermediate-4-6; Normal 0-3. Table 2: Distribution of Cases of RTIs (Reproductive Tract Infections) Diagnosis No. Percentage Intermediate * 137 22.8% BV (Bacterial Vaginosis) * 124 20.7% VVC (Vulvovaginal candidiasis) 65 10.8% VVC+I nte rmediate 24 4.0% BV+VVC 16 2.7% Trichomoniasis 7 1.2% BV+Trichomoniasis 2 0.3% Gonorrhea 2 0.3% Normal * 223 37.2% Total 600 100.0% Table 3: Based on Amsel's Clinical Criteria: (Cases With and Without BV) Clinical Sign BV NBV Total Chi-Square Tests Thin Grey No. 101 119 220 Pearson Chi-Square Homogenous Discharge % 71.1% 26.0% 36.7% Continuity Correction pH >4.5 No. 126 121 247 Pearson Chi-Square % 88.7% 26.4% 41.2% Continuity Correction Whiff Test No. 124 71 195 Pearson Chi-Square % 87.3% 15.5% 32.5% Continuity Correction Clue Cells No. 19 0 19 Pearson Chi-Square % 13.4% 0.0% 3.2% Continuity Correction Clinical Sign Value Df p-Value Association is- Thin Grey No. 95.127 1 1.79E-22 Significant Homogenous Discharge % 93.193 1 4.74E-22 Significant pH >4.5 No. 173.777 1 1.11E-39 Significant % 171.214 1 4.02E-39 Significant Whiff Test No. 254.875 1 2.25E-57 Significant % 251.612 1 1.16E-56 Significant Clue Cells No. 63.286 1 1.79E-15 Significant % 58.997 1 1.58E-14 Significant Fig. 1: Bacterial Vaginosis in Different Cities/States in India INDIAN SCENARIO BV Prevalance (%) BV (%) 68 20.5 24 25 11.3 BV Diagnosis Amsel Nugent Nugent Nugent Nugent Age ranges 15-44 15-49 (Years) P/N/5AW N SAW SAW SAW SAW No. of cases 100 505 51 457 78,617 enrolled City/ State Amritsar Manipal Surat Chennai Delhi Authors Aggra- Rao Kosa- Uma Ray wal et al et al mbiya et al et al et al Years 2003 2004 2005 2006 2006 Reference p B p 38 w 121 w 68 p 29 BV (%) 17.8 19.1 13.33 14.1 53.8 BV Diagnosis Nugent Nugent Nugent Age ranges 18-50 15-30 (Years) P/N/5AW SAW SAW N SAW SAW No. of cases 2436 B63 300 * 510 400 enrolled City/ State Goa Mysore Surat Mumbai Delhi Authors Patel Madhi- Sheth- Mania Thulkar et al vahan et al wala et al et al et al Years 2006 2008 2008 2009 2010 Reference p 93 p 74 w 125 W 59 w 117a BV (%) 40 20.5 24 22.1 BV Diagnosis Amsel Nugent Nugent Age ranges 15-30 (Years) P/N/5AW SAW P SAW SAW No. of cases 412 200 50 397 enrolled City/ State Kamataka North India Kolkata Mysore Authors Becker Indu Modak Paul et al et al et al et al Years 2010 2010 2011 2011 Reference W 117b w 75 P 39 w 89
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|Title Annotation:||Original Article|
|Author:||Malpekar, Kirti; Vivek, Kumar; Shastri, Jayanthi|
|Publication:||Journal of Evolution of Medical and Dental Sciences|
|Date:||Jul 28, 2016|
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