The Threat of Aerobic Vaginitis to Pregnancy and Neonatal Morbidity

Eveline Kaambo, Charlene W J Africa

Abstract

Aerobic vaginitis (AV) is an endogenous opportunistic infection brought about by the disruption of the normal vaginal microbiota. Its early diagnosis and treatment during pregnancy may reduce the risk of negative pregnancy outcomes. The aim of this review was to report on the aerobic bacteria most prevalent in AV and to provide evidence of the threat of untreated AV on pregnancy outcomes. More than 300 papers on preterm delivery were extracted from several research domains and filtered to include only AV-associated bacteria such as Staphylococcus aureus, Enterococcus faecalis, Escherichia coli and Group B streptococci and their association with adverse pregnancy outcomes. Due to the diverse sample groups, study techniques and outcomes, a meta-analysis was not conducted. The review revealed that the association of AV with adverse pregnancy outcomes has not been as widely researched as bacterial vaginosis (BV) and needs further investigation. Furthermore, the frequent misdiagnosis of AV coupled with the emerging antimicrobial resistance associated with bacteria implicated in AV and neonatal nosocomial infections pose a problem for prophylaxis and treatment to reduce the risk of maternal and neonatal morbidity and mortality. (Afr J Reprod Health 2017; 21[2]: 109-118).

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References

Li J, McCormick J, Bocking A and Reid G. Importance of

vaginal microbes in reproductive health. Reproduct Sci 2012; 19(3): 235-242.

Shennan AH and Bewley S. Why should preterm births be rising - If a rise is confirmed, the implications are considerable. BMJ 2006; 332: 924.

Curzik D, Drazancic A and Hrgovic Z. Non-specific aerobic vaginitis and pregnancy. Fetal Diag Ther 2001; 16(3): 187-92.

Rezeberga D, Lazdane G, Kroica J, Sokolova L and Donders GG. Placental histological inflammation and reproductive tract infections in a low risk pregnant population in Latvia. Acta Obstet Gynecol Scand 2008; 87(3): 360-5

Donders G, Bellen G and Rezeberga D. Aerobic vaginitis

in pregnancy. BJOG 2011; 118(10): 1163-70.

Donders GG, Vereecken A, Bosmans E, Dekeersmaecker A, Salembier G and Spitz B. Definition of a type of abnormal vaginal flora that is distinct from bacterial vaginosis: aerobic vaginitis. BJOG 2002; 109(1): 34-43.

Hemalatha R, Ramalaxmi BA, KrishnaSwetha G, Kumar PU, Rao DM, Balakrishna N and Annapurna V. Cervicovaginal inflammatory cytokines and sphingomyelinase in women with and without bacterial vaginosis. Am J Med Sci 2012; 344(1): 35-9.

MacPhee RA, Miller WL, Gloor GB, McCormick JK, Hammond JA, Burton JP and Reid G. Influence of the vaginal microbiota on toxic shock syndrome toxin 1 production by Staphylococcus aureus. Appl Environ Microbiol 2013; 79(6): 1835-42.

Tansarli GS, Kostaras EK, Anthanasiou S and Falagas ME. Prevalence and treatment of aerobic vaginitis

among non – pregnant women: evaluation of the Clin Microbiol Infect Dis 2013; 32(8): 977–84.

Kumari G and Tempe A. Should abnormal vaginal flora in 2nd trimester of pregnancy be treated to prevent preterm labour? MAMC J Med Sci 2015; 1(2): 64-8.

Donders GG, Van Calsteren K, Bellen G, Reybrouck R, Van den Bosch T, Riphagen I and Van Lierde S. Predictive value for preterm birth of abnormal vaginal flora, bacterial vaginosis and aerobic vaginitis during the first trimester of pregnancy. BJOG 2009; 116(10): 1315-24.

Donders GG. Definition and classification of abnormal vaginal flora. Best Pract Clin Obstet Gynaecol 2007; 21(3): 355–73.

Donati L, Di Vico A, Nucci M, Quagliozzi L, Spagnuolo T, Labianca A, Bracaglia M, Ianniello F, Caruso AM and Paradisi G. Vaginal microbial flora and outcome of pregnancy. Arch Gynecol Obstet 2010; 281(4): 589-600.

Sangeetha K T, Golia S and Vasudha CL. The 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): 2268-73.

Wang ZL, Fu LY, Xiong ZA, Qin Q, Yu TH, Wu YT, Hua YY and Zhang YH. Diagnosis and microecological characteristics of aerobic vaginitis in outpatients based on preformed enzymes. Taiwan J Obstet Gynecol 2016; 55(1): 40-4.

Sobel JD, Reichman O, Misra D and Yoo W. Prognosis and treatment of desquamative inflammatory vaginitis. Obstet Gynecol 2011; 117(4): 850-5.

Tempera G, Bonfiglio G, Cammarata E, Corsello S and Cianci A. Microbiological/clinical characteristics and validation of topical therapy with kanamycin in aerobic vaginitis: a pilot study. Int J Antimicrob Agents 2004; 24(1): 85-8.

Han C, Wu W, Fan A, Wang Y, Zhang H, Chu Z, Wang C and Xue F. Diagnostic and therapeutic advancements for aerobic vaginitis. Arch Gynecol Obstet 2015; 291(2): 251-7.

Zarbo G, Coco L, Leanza V, Genovese F, Leanza G, D‘Agati A, Giannone TT, Giunta MR, Palumbo MA, Carbonaro A and Pafumi C. Aerobic vaginitis during pregnancy. Res Obstet Gynecol 2013; 2(2): 7-11.

Stojanovic N, Plecas D and Plesinac S. Normal vaginal flora, disorders and application of probiotics in pregnancy. Arch Gynecol Obstet 2012; 286(2): 325-32.

Honda H, Yokoyama T, Akimoto Y, Tanimoto H, Teramoto M and Teramoto H. The frequent shift to intermediate flora in preterm delivery cases after abnormal vaginal flora screening. Sci Rep 2014; 4: 4799.

Rabiee S, Arab M and 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): 106-8.

Najmi N, Jehan I, Sikandar R and Zuberi NF. Maternal genital tract colonization by Group-B Streptococcus:A hospital based study. J Pak Med Assoc 2013; 63(9): 1103-7.

Wang S, Hibberd ML, Pettersson S and Lee YK. Enterococcus faecalis from healthy infants modulates inflammation through MAPK signaling pathways. PLoS One 2014; 9(5): e97523.

Normann E, Fahlén A, Engstrand L and Lilja HE. Intestinal microbial profiles in extremely preterm infants with and without necrotizing enterocolitis. Acta Paediatr 2013; 102(2): 129– 36.

Hällström M, Eerola E, Vuento R, Janas M and Tammela O. Effects of mode of delivery and necrotising enterocolitis on the intestinal microflora in preterm infants. Eur J Clin Microbiol Infect Dis 2004; 23(6): 463-70.

Magne F, Suau A, Pochart P and Desjeux J. Fecal microbial community in preterm infants. J Pediatr Gastroenterol Nutr 2005; 41(4): 386-92.

Hornik CP, Fort P, Clark RH, Watt K, Benjamin DK Jr., Smith PB, Manzoni P, Jacqz-Aigrain E, Kaguelidou F and Cohen-Wolkowiez M. Early and late onset sepsis in very-low-birth-weight infants from a large group of neonatal intensive care units. Early Hum Dev 2012; 88(Suppl 2): S69–74.

Stoll BJ, Hansen NI, Higgins RD, Fanaroff AA, Duara S, Goldberg R, Laptook A, Walsh M, Oh W and Hale E. Very low birth weight preterm infants with early onset neonatal sepsis: the predominance of Gram-negative infections continues in the National Institute of Child Health and Human Development Neonatal Research Network, 2002–2003. Pediatr Infect Dis J 2005; 24(7): 635-9.

Chu A, Joseph R, Hageman JR, Schreiber M and Alexander K. Antimicrobial therapy and late onsetsepsis. NeoReviews 2012; 13(2): e94-102.

Schnarr J and Smaill F. Asymptomatic bacteriuria and symptomatic urinary tract infections in pregnancy. Eur J Clin Invest 2008; 38(S2):50-7.

Fatemi F, Chamani L, Pakzad P, Zeraati H, Rabbani H and Asgari S. Colonization rate of group B streptococcus (GBS) in pregnant women using GBS agar medium. Acta Medica Iranica 2009; 47(1): 25-30.

Taminato M, Fram D, Torloni MR, Belasco AG, Saconato H and Barbosa DA. Screening for group B Streptococcus in pregnant women: a systematic review and meta-analysis. Rev Lat Am Enfermagem. 2011; 19(6): 1470-8.

McDonald HM and Chambers HM. Intrauterine infection and spontaneous midgestation abortion: is the spectrum of microorganisms similar to that in preterm labor? Infect Dis Obstet Gynecol 2000; 8(5-6): 220-7.

Carey JC and Klebanoff MA. Is a change in the vaginal flora associated with an increased risk of preterm birth? Am J Obstet Gynecol 2005; 192(4): 1341-6.

Baltimore RS, Huie SM, Meek JI, Schuchat A and O‘Brien KL. Early-onset sepsis in the era of group B 1094-8.

Hyde TB, Hilger TM, Reingold A, Farley MM, O‘Brien KL and Schuchat A. Trends in incidence and antimicrobial resistance of early-onset sepsis: population-based surveillance in San Francisco and Atlanta. Pediatrics 2002; 110(4): 690-5.

Stroll BJ, Hansen N, Fanaroff AA, Wright LL, Carlo WA, Ehrenkranz RA, Lemons JA, Donovan EF, Stark AR, Tyson JE, Oh W, Bauer CR, Korones SB, Shankaran S, Laptook AR, Stevenson DK, Papile L and Poole WK. Changes in the pathogens causing early-onset sepsis in very-low-birth-weight infants. N Engl J Med 2002; 347(4): 240-7.

Towers CV and Briggs GG. Antepartum use of antibiotics and early-onset sepsis: the next 4 years. Am J Obstet Gynecol 2002; 187(2): 495-500.

Lin FY, Brenner RA, Johnson YR, Azimi PH, Philips JB, Regan JA, Clark P, Weisman LE, Rhoads GG, Kong F and Clemens JD. The effectiveness of risk-based intrapartum chemoprophylaxis for the prevention of early-onset neonatal group B streptococcal disease. Am J Obstet Gynecol. 2001; 184(6): 1204-10.

Cordero L, Rau R, Taylor D and Ayers LW. Enteric gram-negative bacilli bloodstream infections: 17 years‘ experience in neonatal intensive care unit. Am J Infect Control 2004; 32(4): 189-95.

Bizzarro MJ, Dembry LM, Baltimore RS and Gallagher PG. Changing patterns in neonatal Escherichia coli sepsis and ampicillin resistance in the era of intrapartum antibiotic prophylaxis. Pediatrics 2008; 121(4): 689-96.

Dermer P, Lee C, Eggert J and Few B. A history of neonatal group B streptococcus with its related morbidity and mortality rates in the United States. J Pediatr Nurs 2004; 19(5): 357-63.

Stronati M, Tzialla C and Lombardi G. Prevention of early-onset neonatal group B streptococcus infection. Ital J Pediatr 2004; 30(1): 39-48.

Domelier S, van der Mee-Marquet N, Grandet A, Mereghetti L, Rosenau A and Quentin R. Loss of catabolic function in Streptococcus agalactiae strains and its association with neonatal meningitis. J Clin Microbiol 2006; 44(9): 3245-50.

Van der Mee-Marquet N, Domelier AS, Mereghetti L, Lanotte P, Rosenau A, van Leeuwen W and Quentin R. Prophagic DNA Fragments in Streptococcus agalactiae strains and association with neonatal meningitis. J Clin Microbiol 2006; 44(3): 1049-58.

Milyani R and Rokbah RA. Factors affecting vaginal and rectal carriage rate of Streptococcus agalactiae among pregnant and nonpregnant Saudi women. Adv Schol Med 2011; 1(3): 37-44.

Konikkara KP, Baliga S, Shenoy SM and Bharati B. Comparison of various culture methods for isolation of Group B streptococcus from intrapartum vaginal colonization. J Lab Physicians 2013; 5(1): 42-5.

Varma R, Gupta JK, James DK and Kilby MD. Do screening-preventative interventions in asymptomatic pregnancies reduce the risk of preterm delivery-a critical appraisal of the literature. Eur J Obstet Gynecol Reprod Biol 2006; 127(2): 145-59.

Hiller JE, McDonald HM, Philip Darbyshire P and Crowther CA. Antenatal screening for group B streptococcus: a diagnostic cohort study. BMC Pregnancy Childbirth 2005; 5: 12.

Maghaddam MN. Recto-vaginal colonization of group B streptococcus in pregnant women referred to a hospital in Iran and its effect on Lactobacillus normal flora. J Biol Sci 2010; 10(2): 166-9.

Bohnsack FJ, Whiting A, Gottschalk M, Dunn MD, Weiss R, Azimi PH, Philips BJ, Weisman LE, Rhoads GG and Lin FY. Population structure of invasive and colonization strains of Streptococcus agalactiae from neonates of six U.S. Academic Centers from 1995 to 1999. J Clin Microbiol 2008; 46(4): 1285-91.

Ramaswamy SV, Ferrieri P, Flores AE and Paoletti LC. Molecular characterization of nontypeable Group B streptococcus. J Clin Microbiol 2006; 44(7): 2398-403.

Rocchetti TT, Marconi C, Rall VL, Borges VT, Corrente JE and Da Silva MG. Group B streptococci colonization in pregnant women: risk factors and evaluation of the vaginal flora. Arch Gynecol Obstet 2011; 283(4): 717-21.

Zhou X, Brotman RM, Gajer P, Abdo Z, Schüette U, Ma S, Ravel J and Forney LJ. Recent advances in understanding the microbiology of the female reproductive tract and the causes of premature birth. Infect Dis Obstet Gynecol 2010; Article ID: 737425.

Romero R, Chaiworapongsa T and Espinoza J. Micronutrients and intrauterine infection, preterm birth and the fetal inflammatory response syndrome. J Nutr 2003; 133(5 Suppl 2): 1668S–1673S.

Baltimore RS. Consequences of prophylaxis for group B streptococcal infections of the neonate. Semin Perinatol 2007; 31(1): 33-8.

Bergeron MG and Ke D. New DNA-based PCR approches forrapid real-time detection and prevention of group B streptococcal infections in newborns and pregnant women. Expert Rev Mol Med 2001; 3(27): 1-14.

Tsolia M, Psoma M, Gavrili S, Petrochilou V, Michalas S, Legakis N and Karpathios T. Group B streptococcus colonization of Greek pregnant women and neonates: prevalence, risk factors and serotypes.Clin Microbiol Infect 2003; 9(8): 832-8.

Berseng H, Bevanger L, Rygg M and Berg K. Real-time PCR targeting the sip gene for detection of group B streptococcus colonization in pregnant women at delivery. J Med Microbiol 2007;56(Pt 2): 223-8.

Rallu F, Barriga P, Scrivo C, Martel-Laferrière V and

Laferrière C. Sensitivities of antigen detection and PCR assays greatly increased compared to that of the standard culture method for screening for group B streptococcus carriage in pregnant women. J Clin Microbiol 2006; 44(3): 725-8.

Martins ER, Pessanha MA, Ramirez M and Melo-Cristino J. Analysis of group B streptococcal isolates from infants and pregnant women in Portugal revealing two lineages with enhanced invasiveness. J Clin Microbiol 2007; 45(10): 3224-9.

Mhaskar R, Sathyan S, Nadig S, Bhat S and Shamsundar R. Selective risk factor based screening of pregnant women for Group B streptococcal colonization in a teaching hospital in South India. J Obstet Gynecol India 2005; 55(4): 336-8.

Top KA, Buet A, Whittier S, Ratner AJ and Saiman L. Predictors of Staphylococcus aureus rectovaginal colonization in pregnant women and risk for maternal and neonatal infections. J Pediatric Infect Dis Soc 2012; 1(1): 7-15.

Bourgeois-Nicolaos N, Lucet JC, Daubié C, Benchaba F, Rajguru M, Ruimy R, Andremont A and Armand-Lefèvre L. Maternal vaginal colonization by Staphylococcus aureus and newborn acquisition at delivery. Pediatr Perinat Epidemiol 2010; 24(5): 488-91.

Grass B and Leone A. Severe complications in preterm infant with late – onset Staphylococcus aureus sepsis. Clinic for Neonatology (GB, LA), University Hospital of Zurich, Switzerland. Swiss Society of Neonatology, 2013; September: 3-15.

Seybold U, Halvosa JS, White N, Voris V, Ray SM and Blumberg HM. Emergence of and risk factors for methicillin-resistant Staphylococcus aureus of community origin in intensive care nurseries. Pediatrics 2008; 122(5): 1039-46.

Jimenez-Truque N, Tedeschi S, Saye EJ, McKenna BD, Langdon W, Wright JP, Alsentzer A, Arnold S, Saville BR, Wang W, Thomsen I and Creech CB. Relationship between maternal and neonatal Staphylococcus aureus colonization. Pediatrics 2012; 129(5): e1252-9.

Lazenby GB, Soper DE, Beardsley W and Salgado CD. Methicillin-resistant Staphylococcus aureus colonization among women admitted for preterm delivery. Am J Obstet Gynecol. 2012; 206(4): 329.e1-5.

Li J, McCormick J, Bocking A and Reid G. Importance of vaginal microbes in reproductive health. Reprod Sci 2012; 19(3): 235-42.

Chen KT, Huard RC, Della-Latta P and Saiman L. Prevalence of methicillin-sensitive and methicillin-resistant Staphylococcus aureus in pregnant women. Obstet Gynecol 2006; 108(3 Pt 1):482-7.

Andrews WW, Schelonka R, Waites K, Stamm A, Cliver SP and Moser S. Genital tract methicillin – resistant Staphylococcus aureus: risk of vertical transmission in pregnant women. Obstet Gynecol 2008; 111(1): 113-8.

Hufnagel M, Liese C, Loescher C, Kunze M, Proempeler H, Berner R and Krueger M. Enterococcal colonization of infants in a neonatal intensive care unit: associated predictors, risk factors and seasonal patterns. BMC Infect Dis 2007; 7: 107.

Al-Abbas MJA. Antimicrobial susceptibility of Enterococcus faecalis and a novel Planomicrobium isolate of bacterimia. Int J Med Med Sci 2012; 4(2): 19-27.

Akerele J, Abhulimen P and Okonofua F. Prevalence of asymptomatic genital infection among pregnant women in Benin City, Nigeria. Afr J Reprod Health 2002; 6(3): 93-7.

Coombs GW, Pearson JC, Daley DA, Le T, Robinson OJ, Gottlieb T, Howden BP, Johnson PD, Bennett CM, Stinear TP and Turnidge JD. Molecular epidemiology of enterococcal bacteremia in Australia. J Clin Microbiol 2014; 52(3): 897-905.

Ghasemi E, Mansouri S and Shahabinejad N. Vaginal colonization and susceptibility to antibiotics of enterococci during late pregnancy in Kerman City, Iran. Arch Clin Infect Dis 2016; 11(4): e35428.

Gaca AO, Abranches J, Kajfasz JK and Lemos JA. Global transcriptional analysis of the stringent response in Enterococcus faecalis. Microbiology 2012; 158(Pt 8): 1994–2004.

Cheng VC, Tai JW, Chen JH, So SY, Ng WC, Hung IF, Leung SS, Wong SC, Chan TC, Chan FH, Ho PL and Yuen KY. Proactive infection control measures to prevent nosocomial transmission of vancomycin-resistant enterococci in Hong Kong. J Formos Med Assoc. 2014;113(10):734-41.

Muratani T and Matsumoto T. Bacterial resistance to antimicrobials in urinary isolates. Int J Antimicrob Agents 2004; 24(Suppl 1): S28–31.

Seliga-Siwecka JP and Kornacka MK. Neonatal outcome of preterm infants born to mothers with abnormal genital tract colonisation and chorioamnionitis: a cohort study. Early Hum Dev 2013; 89(5): 271-5.

Subramaniam A, Abramovici A, Andrews WW and Tita TA. Antimicrobials for preterm birth prevention: an overview. Infect Dis Obstet Gynecol 2012; Article ID: 157159.

Ozkinay E, Terek MC, Yayci M, Kaiser R, Grob P and Tuncay G. The effectiveness of live lactobacilli in combination with low dose oestriol (Gynoglor) to restore the vaginal flora after treatment of vaginal infections. BJOG 2005; 112(2): 234-40.

Donders CG, van Bulck B, Van de Walle P, Kaiser RR, Pohlig G, Gonser S and Graf F. Effect of lypholized lactobacilli and 0.03 mg estriol (Gynoflor®) on vaginitis and vaginosis with disrupted vaginal microflora. A multicentre, randomised, single-blind, active controlled pilot study. Gynecol Obstet Invest 2010; 70(4): 264-72.

Mumtaz S, Ahmad M, Aftab I, Akhar N, ul Hassan M and Hamid A. Aerobic vaginal pathogens and their sensitivity patterns. J Ayub Med Coll Abbottabad

; 20(1): 113-7.

Nahar D, Soni G, Chand AE and Mourya S. Bacterial etiology and their antibiogram in aerobic vaginitis patients at Tertiary Care Hospital, Kota, Rajasthan. Int J Scien Stud 2016; 4(3): 103- 7.

Khan I and Khan UA. A hospital based study of frequency of aerobic pathogens in vaginal infections. RMJ 2004; 29(1): 22-5.

Tempera G, Bonfiglio G, Cammarata E, Corsello S and Cianci A. Microbiological/clinical characteristics and validation of topical therapy with kanamycin in aerobic vaginitis: a pilot study. Int J Antimicrob Agents 2004; 24(1): 85-8.

Tempera G, Abbadessa G, Bonfiglio C, Cammarata E, Cianci A, Corsello S, Raimondi A, Ettore G, Nicolosi D and Furneri PM. Topical kanamycin: an effective therapeutic option in aerobic vaginitis. J Chemother 2006; 18(4): 409-14.

Murphy R and Edwards L. Desquamative inflammatory

vaginitis: what is it? J Reprod Med 2008; 53(2): 124-8.

Fan A, Yue Y, Gang N, Zhang H, Wang Y and Xue F. Aerobic vaginitis and mixed infections: comparison of clinical and laboratory findings. Arch Gynecol Obstet 2013; 287(2): 329-35.

Ling C and Wang JY. The vaginal microflora of aerobic vaginitis and bacterial vaginosis. Chinese J Microbiol 2009; 21(2): 1107-9.

Razzak MSA, Al-Charrakh AH and Al-Greitty BH.

Relationship between lactobacilli and opportunistic bacterial pathogens associated with vaginitis. North Am J Med Sci 2011; 3(4): 185-92.

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