ph-balanced tampons: do they effectively control vaginal ph?
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1 DOI: /j x General gynaecology ph-balanced tampons: do they effectively control vaginal ph? L Melvin, a A Glasier, a R Elton, b ST Cameron c a Family Planning and Well Woman Clinic, Edinburgh, UK b Department of Statistics, University of Edinburgh, Edinburgh, UK c Department of Obstetrics and Gynaecology, Royal Infirmary of Edinburgh, Edinburgh, UK Correspondence: Dr L Melvin, Family Planning and Well Woman Clinic, 18 Dean Terrace, Edinburgh EH4 1NL, UK. louise.melvin@virgin.net Accepted 28 December Objective To determine if tampons lubricated with ph-balanced gel are effective at maintaining normal vaginal ph. Design Randomised controlled trial. Setting Urban family planning clinic and teaching hospital. Population Healthy volunteers using the combined oral contraceptive pill. Methods Women were randomised to use an existing lubricating gel (ph 5.1) or a lactic acid-buffered gel (ph ) with regular size, non-applicator tampons. In the preceding control cycle, women used identical tampons without gel. Main outcome measures Vaginal ph 4.5, microbiology (candida and bacterial vaginosis [BV]) and colposcopic appearance within 72 hours of tampon use, subject acceptability and symptoms. Results Eighty-one out of 98 (83%) women completed the study. No significant difference was observed between tampons with the standard gel formulation, the ph-balanced gel and nonlubricated tampons in terms of vaginal ph, microbiological evidence of candida or BV, or colposcopic appearance. Acceptability scores were significantly higher for lubricated tampons compared with nonlubricated tampons (P < 0.05), although there was no difference in reported symptoms. Conclusions Tampons lubricated with ph-balanced gel do not control vaginal ph. There was no evidence of measurable health benefits of lubricated tampons, but women preferred tampons without lubrication. Keywords Menstruation, tampons, vaginal ph. Please cite this paper as: Melvin L, Glasier A, Elton R, Cameron S. ph-balanced tampons: do they effectively control vaginal ph? BJOG 2008;115: Introduction Vulvovaginal symptoms such as discharge, itch, odour and discomfort are common complaints of women attending general practice, gynaecology and sexual health clinics. 1 These symptoms occur most commonly during and shortly after menstruation, at a time when the vaginal ph tends to be elevated compared with other times in the cycle. 2 The reason for the rise in ph is unclear, but there is evidence of a temporary disturbance of the vaginal microflora and an increased incidence of bacterial vaginosis (BV) and candidal infection around the time of menstruation. 2,3 Lactobacillus-dominant flora is associated with vaginal ph in the range This is generally considered the normal vaginal ph in women of reproductive age. Elevated vaginal ph greater than 4.5 is associated with BV (characterised by overgrowth of anaerobic bacteria), which is in turn associated with vaginal discharge symptoms, preterm birth, increased transmission of sexually transmitted infections and pelvic inflammatory disease. 5 Thus, it seems that maintaining a low ph in the vagina could potentially reduce the incidence of troublesome symptoms and infection of the genital tract. Vaginal tampons have been used for menstrual protection for over 70 years. Although tampons offer the advantage of being more discrete and comfortable to wear than pads, some women find them uncomfortable to insert. There is evidence that tampons can cause minor trauma to the vaginal mucosa. 6 8 Use of tampons has also been associated with infection, including life-threatening toxic shock syndrome. 9 Over the years, manufacturers have modified tampon materials and designed to ease insertion and minimise trauma and infection. Lubricated tampons have been commercially available in the UK since 2003 (Lil-lets Extra Comfort Ò ; Accantia Health and Beauty Ltd, Birmingham, UK). This product consists of a two-sachet system, one sachet containing a regular ª 2008 The Authors Journal compilation ª RCOG 2008 BJOG An International Journal of Obstetrics and Gynaecology 639
2 Melvin et al. size, non-applicator tampon (Lil-lets Regular Ò ) and the other containing 1 g of aqueous gel with a ph of 5.1. A ph-balanced gel was developed for use as a novel tampon lubricant. The gel contains a lactic acid buffer designed to maintain vaginal ph between 3.8 and 4.2 for 8 hours (Data on file, Accantia Health and Beauty Ltd). Our study aimed to investigate the potential for using tampons in conjunction with ph-balanced gel to maintain a vaginal ph of 4.5. Secondary outcomes were vaginal microbial disturbance (BV and candidosis), integrity of the lower genital tract mucosa as assessed by colposcopic appearance, lower genital tract symptoms and user acceptability of tampon products. Methods Participants Ethical approval was obtained from Lothian Research Ethics Committee. Women were healthy volunteers, aged years, using the combined oral contraceptive pill. Women were recruited from the general public, hospital staff and family planning clinic patients in Edinburgh from February 2004 to April We chose to recruit women on the combined oral contraceptive pill to sample a homogeneous group with regular, predictable bleeds. Unlike some other contraceptive methods, use of the combined pill does not appear to alter vaginal ph or the incidence of BV or candidal infection. 10 Women were excluded from the study if they had an abnormal cervical smear in the previous 5 years or at pre-entry screening. Other exclusion criteria included recurrent urinary tract infection or abnormal vaginal bleeding. Eligible women were screened by general physical and gynaecological examination, cervical cytology, Chlamydia trachomatis nucleic acid amplification test (Lcx; Abbott, Queenborough, UK), high vaginal swab (Gram stain microscopy and culture) and vaginal ph (ph control strip number 3060, range in increments of 0.5; Precision Labs Inc., West Chester, OH, USA). Women who were tested positive for candida, BV or chlamydia were treated prior to entry into the study. Study entry was delayed for 1 month after antibiotic treatment for chlamydia. We asked women to avoid using other sanitary products, vaginal hygiene products or douching during the study. There was no restriction on sexual intercourse. The length of time since last intercourse was recorded at each examination. Statistics and randomisation Based on existing literature on vaginal ph, 10 power calculations estimated that 50 women in each treatment group (total 100 women) would give 90% power to detect a statistically significant decrease in the incidence of abnormal ph of >4.5 from 28% after menstruation to 6% after ph-balanced tampon use. Randomisation was conducted in blocks of ten using a computer algorithm. Regular size, non-applicator tampons with ph-balanced gel and standard gel were packaged identically and labelled by the manufacturer (Accantia Health and Beauty Ltd) with sequential subject numbers according to the randomisation code. Subjects and investigators were blinded to the type of lubricated tampon used in the treatment cycle of the study. There was no blinding in the initial control cycle in which all women used identical nonlubricated tampons. Statistical analyses were performed by R.E. Association between categorised variables was tested by chi-square test using Yate s correction for 2 2 tables and tests for linear trend for ordinal variables. Wilcoxon signed-rank tests were used to test for changes over time within treatment groups. Follow up and outcome measures Women were monitored over two pill cycles. They kept a daily diary of vaginal symptoms (dryness, itch, redness, burning, odour, discharge and bleeding), subjectively graded as mild, moderate or severe. In the first cycle, women acted as their own control by using the non-applicator tampon without lubricant (Lil-lets Regular Ò ; Accantia Health and Beauty Ltd). In the second cycle, they used the same tampon with lubricating gel: either standard gel (Lil-lets Extra Comfort Ò ) or ph-balanced gel. Women attended for follow up after each withdrawal bleed (within 72 hours of using the last tampon) and underwent speculum examination as follows. Colposcopic visualisation of the vulva, vagina and cervix was performed using a SOM 52 cold light colposcope (Karl Kaps, Asslar, Germany) at 10 magnification. The study doctor was trained in colposcopy and recorded epithelial findings according to the World Health Organization/Contraceptive Research and Development Program protocol. 11 Vaginal ph testing was performed using a dry cotton swab from the lateral fornix, applied to narrow range ( ) ph indicator paper (ph control strip no. 3060, Precision Labs, Inc.). We validated our ph recordings by laboratory testing of the Precision ph paper against standard ph solutions and by introducing a second brand of ph paper for verifying the in vivo ph measurements (Whatman narrow range ph paper , Middlesex, UK). A high vaginal swab was taken for microbiological assessment by the hospital laboratory, Royal Infirmary of Edinburgh. Microbiological evidence of candidal infection was defined as moderate or large yeasts (>5 yeast per 400 magnification field) on microscopy or positive culture. Evidence of BV was defined as the presence of clue cells on microscopy (wet film and Gram stain). Acceptability of tampon products was assessed by selfadministered questionnaire in which women graded their overall satisfaction with each type of tampon on a scale of 0 10 (minimum to maximum). Symptom diaries were analysed using a scoring system corresponding to the intensity of the symptom (1 = mild, 2 = moderate and 3 = severe) on each 640 ª 2008 The Authors Journal compilation ª RCOG 2008 BJOG An International Journal of Obstetrics and Gynaecology
3 ph-balanced tampon study day of tampon use. The symptom index was expressed as the total score for each symptom per woman per day of tampon use. Results Out of 121 women screened, 23 were excluded from the study (Figure 1). Of the 98 women randomised, 81 (83%) completed the study. There were no significant physical or socio-demographic differences between the groups allocated to standard gel or ph-balanced gel at baseline or on completion of the study (Table 1). Vaginal ph Vaginal ph recordings taken within 72 hours of tampon use ranged from 4.5 to 6.0. The majority of women had a vaginal ph elevated above 4.5, regardless of tampon type (Figure 2). Although the prevalence of vaginal ph of 4.5 tended to be higher after the treatment cycle compared with the control (nonlubricated tampon) cycle for all women, the difference was not statistically significant (Table 2). Nor was there any significant difference in the prevalence of ph 4.5 after use of the standard gel tampon compared with the ph-balanced gel tampon. The only statistically significant ph change was a decrease in the prevalence of elevated ph of >4.5 in women using the standard gel tampon compared with the use of nonlubricated tampons in the control cycle (P < 0.01). No significant correlation was observed between vaginal ph and time since sexual intercourse or evidence of candida or BV. There was, however, a statistically significant correlation between vaginal ph and time since last tampon use, with higher ph levels being recorded the more recently the last tampon had been used (P < 0.05). We re-analysed our data using ph recordings obtained with a different brand of ph paper (Whatman, narrow range ). There was a tendency for Whatman paper ph recordings to be lower by a ph increment of 0.5, but there was no statistically significant difference in ph results (results not shown). Infection The number of swabs showing microbiological evidence of BV (clue cell positivity) was generally very low with only two women testing positive at screening (Table 1) and one woman after the control cycle. No clue cells was detected after the use of gel tampons, and no statistical differences in clue cell positivity was observed between control and gel tampon cycles. Microbiological evidence of candida was observed in 13.4% (11/82), 9.8% (4/41) and 2.5% (1/40) of women after the control, standard gel and ph-balanced gel tampon cycles, respectively. The prevalence of candidosis after each tampon type was not significantly different. Colposcopic inspection On colposcopic assessment, a total of 126 epithelial changes were observed during 162 inspections. The most frequently recorded epithelial change was erythema (noted on 99 [61%] of inspections), and the sites most commonly affected by erythema were the cervix (29 inspections) and vagina (28 inspections). Petechiae, abrasions and oedema were noted on 19, 5 and 3 inspections, respectively. It was not possible to control for iatrogenic epithelial change due to trauma from speculum insertion, but it was estimated that up to 75 (60%) of the recorded changes (i.e. those affecting the cervix and vaginal fornices) may have been secondary to the examination rather than tampon use or other trauma. The incidence of epithelial changes did not differ significantly with use of each tampon type. Acceptability and symptom scores When asked to grade overall satisfaction with tampon products on a scale of 0 10, women gave significantly higher mean scores for both types of lubricated tampon (8.55 and 8.40 for standard gel and ph-balanced gel groups, respectively, compared with 6.63 and 7.15 [P < 0.05] for use of nonlubricated tampons by each group). There was no significant difference in mean acceptability scores between standard gel and phbalanced gel tampons. There were no significant differences in the symptom scores for dryness, itch, redness, burning, odour or discharge experienced while using the control tampon, standard gel or ph-balanced gel tampons. Discussion We aimed to recruit 120 women and anticipated a drop-out rate of 20%. Although these targets were met, higher than anticipated numbers were excluded at screening. Thus, 98 women (rather than the target 100) entered the study, resulting in the trial being slightly underpowered. The study s main outcome measure was vaginal ph. Measurements of vaginal ph were higher than expected, with the majority of recordings (85% of subjects after standard gel and 83% after ph-balanced gel tampons) lying above 4.5, the upper limit of normal. There are a number of possible explanations for these high ph recordings. As previously discussed, vaginal ph tends to rise around the time of menses, 2 and the presence of any residual blood in the vagina may also increase ph recordings. This would explain our finding of lower ph levels with greater time elapsed since tampon use. One previous study of combined pill users demonstrated that 28% of women had elevated vaginal ph following withdrawal bleeds. 10 A more recent study of young women in a genitourinary medicine setting reported that 60% of vaginal ph recordings taken at random times in the cycle were above ª 2008 The Authors Journal compilation ª RCOG 2008 BJOG An International Journal of Obstetrics and Gynaecology 641
4 Melvin et al. Enrolled, n = 121 Screening Eligible subjects, n = 98 Randomisation Control arm, n = 50 Treatment arm, n = 48 First month Nonlubricated tampon First assessment, n = 43 (lost to follow-up, n = 7) First assessment, n = 39 (lost to follow up/excluded, n = 8, defaulted, n = 1) Second month Second month Control gel tampon ph-balanced gel tampon Second assessment, n = 41 (lost to follow up, n = 2) Second assessment, n = 40 Completion rate 81/98 (82.7%) Figure 1. CONSORT study profile. 642 ª 2008 The Authors Journal compilation ª RCOG 2008 BJOG An International Journal of Obstetrics and Gynaecology
5 ph-balanced tampon study Table 1. Baseline demographics of study population Characteristics Standard gel tampon group (n 5 50) ph-balanced gel tampon group (n 5 48) Age (years) 28.8 [6.6] 26.7 [4.4] Body mass index 23.6 [4.4] 23.5 [4.2] Ethnic group Caucasian 50 (100) 44 (91.7) Black 0 (0) 1 (2.1) Asian 0 (0) 1 (2.1) Other 0 (0) 2 (4.2) Current smoker 14 (28.0) 9 (18.8) Chlamydia infection 1 (2.0) 0 (0) Candida infection 12 (24.0) 8 (16.7) BV 2 (4.0) 0 (0) PH (46.0) 21 (43.8) (54.0) 27 (56.2) Values are presented as mean [SD] or n (%). The ph-balanced (ph ) gel was no more effective at maintaining vaginal ph of 4.5 than the standard (ph 5.1) gel. The standard gel was associated with a statistically significant reduction in elevated vaginal ph (>4.5) compared with control tampons, but this was not the primary outcome Percentage of women 40.0% 30.0% 20.0% 10.0% 0.0% ph Gel 5.50 No gel Standard gel ph-balanced gel Figure 2. Vaginal ph measurements after tampon use measure, and a falsely significant result may have arisen from multiple statistical testing. Our study may have failed to demonstrate any significant effect of ph-balanced gel on vaginal ph for a number of reasons. First, the sample size was relatively small and the study was slightly underpowered. Moreover, had we anticipated the low incidence of what is considered normal ph we could perhaps have powered the study more accurately or used a more sensitive primary outcome measure. It could be argued that the testing of vaginal ph from a single swab within 72 hours of menstruation may not be representative of the impact of tampons on vaginal ph. However, this is the time in the cycle when symptoms are most common and when any clinically relevant ph changes are most likely to occur. Another limitation of the study could be inadequate delivery of gel to the vagina. The buffering capacity of the phbalanced gel had previously only been tested in vitro, and the volume required to buffer vaginal fluid and menstrual blood had not been determined. The lubricated tampon products were packaged as a two-sachet system connected by a thin seal. One sachet contains 1 g of gel and the other contains a dry tampon. Prior to insertion, the tampon is pushed through the seal into the gel sachet, coated with gel and then inserted digitally into the vagina. A variable quantity of gel remains in the sachet and some is left on the vulva. Thus, the exact quantity of gel reaching the vagina is unknown and is certainly less than 1 g. In contrast, other products for vaginal acidification have been formulated in higher doses with applicators for insertion directly into the vagina. Examples include Acijel Ò (5 ml acetic acid gel, twice daily dose), 13 BuffergelÔ (5 g once daily) 14 and MiphilÔ(2.5 g once daily). 15 Interestingly, Acijel s effects on vaginal ph have also been disappointing, which may be due to the inferior buffering capacity of acetic acid compared with lactic acid. 13 Given the strong association between high vaginal ph and BV, we were surprised to detect only two cases with microbiological evidence of BV (2% prevalence) at screening and only one case during the control cycle. The prevalence of BV is known to vary according to the population studied and the diagnostic criteria employed, with rates of between 4.9 and 50% quoted in the literature. 5 In the few studies of asymptomatic, nonpregnant women, the prevalence rates in American, British and Swedish women were 4, 9 and 10%, respectively The majority of studies have used either composite clinical and microbiological criteria (Amsel s criteria) 19 or Gram stain scoring systems (Nugent s criteria) 20 as a determinant of BV, while our study used only the presence of clue cells on wet film and Gram stain. We used clue cells because it is a relatively simple method with reasonable sensitivity and specificity (figures in the range 81 98% sensitivity and 94 95% specificity reported). 21 It is also the criterion used in the local hospital laboratory and this allowed ª 2008 The Authors Journal compilation ª RCOG 2008 BJOG An International Journal of Obstetrics and Gynaecology 643
6 Melvin et al. Table 2. Prevalence of vaginal ph 4.5 after tampon use Vaginal ph Standard gel tampon group ph-balanced gel tampon group Control cycle (n 5 43) Treatment cycle (n 5 41) Control cycle (n 5 39) Treatment cycle (n 5 40) (4.65) 7 (17.1) 3 (7.69) 6 (15.0) (95.3)* 34 (82.9)* 36 (92.3) 34 (85.0) Values are presented as n (%). *P, 0.01 (use of nonlubricated tampon versus standard gel tampon). comparison of our results with local prevalence rates. In the 12 months, from August 2003 to 2004, the laboratory received over high vaginal swabs from symptomatic women, of which 4.5% were positive for clue cells (Dr FXS Emmanuel, Medical Microbiology Laboratory, Royal Infirmary of Edinburgh, pers. comm.). In light of this figure, the observed number of BV cases in our population of healthy volunteers is not surprising. Determination of BV by the presence of clue cells alone may not be as specific as Amsel s criteria 22 or as reproducible as Nugent s method, 20 and our study could perhaps be criticised for not using a more rigorous diagnostic method. Furthermore, clue cells correlate poorly with intermediate grades of flora. 23 The use of Nugent s criteria to identify women with intermediate scores may have revealed more subtle effects on vaginal flora, which may be clinically relevant in the context of vaginal discharge symptoms. Colposcopic evaluation of the vaginal mucosa suggests that epithelial changes are common after tampon use. Our findings are consistent with those of other studies of tampon users in which a high incidence of vaginal mucosal alteration was observed during tampon use, followed by spontaneous resolution. 6,8 Fraser et al. 7 performed colposcopy on healthy sexually active volunteers and found that epithelial changes were strongly associated with sexual intercourse in the last 24 hours and with tampon use. Lower genital tract infection can also alter the appearance of the vaginal and cervical mucosa. 24 Thus, a proportion of our findings may have been due to intercourse, trauma from speculum insertion or infection, but a significant number are likely to be secondary to tampon use. The clinical significance of such epithelial changes is unclear. We can at least be reassured that the majority of changes were superficial and rarely involved disruption of the epithelial surface (5 abrasions observed in 162 inspections). While the lubricating gels did not appear to reduce epithelial trauma, they were not associated with deleterious effects on vaginal mucosa. Women did not express any preference for the phbalanced gel tampon over the standard gel tampon, and there was no apparent difference in symptoms with use of any of the tampon products. However, both types of lubricated tampon were rated as more acceptable to use than the nonlubricated control tampon. Conclusion Previously published tampon research has tended to focus on minimising the adverse effects of tampon use. This is one of the few studies exploring potential health benefits of a tampon product. Although the study did not demonstrate any major benefits of tampon lubrication with a ph-balanced gel, it does provide reassuring data on the safety and the acceptability of lubricated tampons and adds to the limited volume of published literature on the effects of tampons on the vaginal milieu. If the product design could be modified to deliver a larger amount of gel to the vagina, it may be possible to control vaginal ph more effectively. Conflicts of interest The study was funded by a grant from Accantia Health and Beauty Ltd, the manufacturer of Lil-lets Ò tampon products. Acknowledgements We gratefully acknowledge the support provided by Accantia Health and Beauty Ltd, the contribution of Sister Helen Dewart, Prof Hilary Critchley and Dr Alan Brown and the cooperation of staff in the Family Planning and Well Woman Clinic, and Reproductive Health Outpatient Department, Edinburgh. j References 1 French P. Sorting out vaginal discharge. Trends Urol Gynaecol Sex Health 2004;9: Eschenbach DA, Thwin SS, Patton DL, Hooton TM, Stapleton AE, Agnew K, et al. Influence of the normal menstrual cycle on vaginal tissue, discharge, and microflora. Clin Infect Dis 2000;30: Keane F, Ison C, Taylor-Robinson D. A longitudinal study of the vaginal flora over a menstrual cycle. Int J STD AIDS 1997;8: Boskey ER, Telsch KM, Whaley KJ, Moench TR, Cone RA. Acid production by vaginal flora in vitro is consistent with the rate and extent of vaginal acidification. Infect Immun 1999;67: ª 2008 The Authors Journal compilation ª RCOG 2008 BJOG An International Journal of Obstetrics and Gynaecology
7 ph-balanced tampon study 5 Morris M, Nicoll A, Simms I, Wilson J, Catchpole M. Bacterial vaginosis: a public health review. BJOG 2001;108: Berkeley AS, Micha JP, Freedman KS, Hirsch JC. The potential of digitally inserted tampons to induce vaginal lesions. Obstet Gynecol 1985; 66: Fraser IS, Lahteenmaki P, Elomaa K, Lacarra M, Mishell DR Jr, Alvarez F, et al. Variations in vaginal epithelial surface appearance determined by colposcopic inspection in healthy, sexually active women. Hum Reprod 1999;14: Friedrich EG Jr, Siegesmund KA. Tampon-associated vaginal ulcerations. Obstet Gynecol 1980;55: Reingold AL. Toxic shock syndrome: an update. Am J Obstet Gynecol 1991;165: Eschenbach DA, Patton DL, Meier A, Thwin SS, Aura J, Stapleton A, et al. Effects of oral contraceptive pill use on vaginal flora and vaginal epithelium. Contraception 2000;62: WHO/CONRAD. Manual for the Standardization of Colposcopy for the Evaluation of Vaginal Products, Update Geneva, Switzerland: CONRAD/WHO, Brabin L, Roberts SA, Fairbrother E, Mandal D, Higgins SP, Chandiok S, et al. Factors affecting vaginal ph levels among female adolescents attending genitourinary medicine clinics. Sex Transm Infect 2005;81: Holley RL, Richter HE, Varner E, Pair L, Schwebke JR. A randomized, double-blind clinical trial of vaginal acidification versus placebo for the treatment of symptomatic bacterial vaginosis. Sex Transm Dis 2004;31: Harwell JI, Moench T, Mayer KH, Chapman S, Rodriguez I, Cu-Uvin S. A pilot study of treatment of bacterial vaginosis with a buffering vaginal microbicide. J Womens Health 2003;12: Fiorilli A, Molteni B, Milani M. Successful treatment of bacterial vaginosis with a policarbophil-carbopol acidic vaginal gel: results from a randomised double-blind, placebo-controlled trial. Eur J Obstet Gynecol 2005;120: Eschenbach DA, Hillier SL, Critchlow C, Stevens C, DeRouen T, Holmes KK. Diagnosis and clinical manifestations of bacterial vaginosis. Am J Obstet Gynecol 1988;158: Lamont RF, Morgan DJ, Wilden SD, Taylor-Robinson D. Prevalence of bacterial vaginosis in women attending one of three general practices for routine cervical cytology. Int J STD AIDS 2000;11: Larsson P, Platz-Christensen J, Sundstrom E. Is bacterial vaginosis a sexually transmitted disease? Int J STD AIDS 1991;2: Amsel R, Totten PA, Spiegel CA, Chen KC, Eschenbach D, Holmes KK. Nonspecific vaginitis: diagnostic criteria and microbial and epidemiologic associations. Am J Med 1983;74: 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: Thomason JL, Gelbart SM, Anderson RJ, Walt AK, Osypowski PJ, Broekhuizen FF. Statistical evaluation of diagnostic criteria for bacterial vaginosis. Am J Obstet Gynecol 1990;162: Gutman RE, Peipert JF, Weitzen S, Blume J. Evaluation of clinical methods for diagnosing bacterial vaginosis. Obstet Gynecol 2005;105: Taylor-Robinson D, Morgan DJ, Sheehan M, Rosenstein IJ, Lamont RF. Relation between Gram-stain and clinical criteria for diagnosing bacterial vaginosis with special reference to Gram grade II evaluation. Int J STD AIDS 2003;14: Georgijevic AV, Sisovic JR, Djukic SV, Bujko MJ. Colposcopic and cytologic findings among women with abnormal vaginal flora. J Low Genit Tract Dis 2002;6: ª 2008 The Authors Journal compilation ª RCOG 2008 BJOG An International Journal of Obstetrics and Gynaecology 645
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