1921
Volume 92, Issue 6
  • ISSN: 0002-9637
  • E-ISSN: 1476-1645

Abstract

Abstract.

Interrelationships among bacteria, protozoa, helminths, and ectoparasites were explored in a cross-sectional survey of 213 pregnant and 99 lactating indigenous women. Prevalences in pregnancy and lactation, respectively, were: vaginitis (89.2%; 46.8%), vaginal trichomoniasis (75.3%; 91.1%), bacterial vaginosis (BV; 60.6%; 63.3%), hookworm (56.6%; 47.8%), asymptomatic bacteriuria/urinary tract infection (AB/UTI; 56.2%; 36.2%), cervicitis (33.3%; 6.3%), vaginal yeast (24.9%; 11.4%), (32.5%; 17.4%), vaginal diplococci (20.4%; 31.6%), caries (19.7%; 18.2%), scabies (17.4%; 8.1%), and (12.5%; 8.7%). Multiple regressions revealed positive associations during pregnancy (trichomoniasis and AB/UTI; diplococci and ) and lactation (yeast and scabies). Negative associations were detected in pregnancy (BV and trichomoniasis; hookworm and diplococci) and lactation (BV and yeast). Vaginal reduced odds of diplococci in pregnancy and lactation, but increased eggs per gram (epg) and odds of trichomoniasis in pregnancy and yeast in lactation. These associations raised a concern that treatment of one condition may increase the risk of another.

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2015-06-03
2017-11-22
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References

  1. Anderson MR, Klink K, Cohrssen A, , 2004. Evaluation of vaginal complaints. JAMA 291: 13681379.[Crossref]
  2. Ilkit M, Guzel AB, , 2011. The epidemiology, pathogenesis, and diagnosis of vulvovaginal candidosis: a mycological perspective. Crit Rev Microbiol 37: 250261.[Crossref]
  3. Schnarr J, Smaill F, , 2008. Asymptomatic bacteriuria and symptomatic urinary tract infections in pregnancy. Eur J Clin Invest 38 (Suppl 2): 5057.[Crossref]
  4. Larocque R, Casapia M, Gotuzzo E, Gyorkos TW, , 2005. Relationship between intensity of soil-transmitted helminth infections and anemia during pregnancy. Am J Trop Med Hyg 73: 783789.
  5. Kandan PM, Menaga V, Kumar RR, , 2011. Oral health in pregnancy (guidelines to gynaecologists, general physicians and oral health care providers). J Pak Med Assoc 61: 10091014.
  6. Matevosyan NR, , 2011. Periodontal disease and perinatal outcomes. Arch Gynecol Obstet 283: 675686.[Crossref]
  7. Feldmeier H, Heukelbach J, , 2009. Epidermal parasitic skin diseases: a neglected category of poverty-associated plagues. Bull World Health Organ 87: 152159.[Crossref]
  8. Afsar FS, , 2010. Skin infections in developing countries. Curr Opin Pediatr 22: 459466.[Crossref]
  9. Zhang D, Mi L, Yang H, , 2014. Incidence and factors influencing postpartum bacterial vaginosis: a controlled study. Chin Med J (Engl) 127: 586587.
  10. Adriaens LM, Alessandri R, Sporri S, Lang NP, Persson GR, , 2009. Does pregnancy have an impact on the subgingival microbiota? J Periodontol 80: 7281.[Crossref]
  11. Moodley D, Esterhuizen T, Reddy L, Moodley P, Singh B, Ngaleka L, Govender D, , 2011. Incident HIV infection in pregnant and lactating women and its effect on mother-to-child transmission in South Africa. J Infect Dis 203: 12311234.[Crossref]
  12. Selvaraj S, Paintsil E, , 2013. Virologic and host risk factors for mother-to-child transmission of HIV. Curr HIV Res 11: 93101.[Crossref]
  13. Schleiss MR, , 2006. Role of breast milk in acquisition of cytomegalovirus infection: Recent advances. Curr Opin Pediatr 18: 4852.
  14. Amir LH, Cullinane M, Garland SM, Tabrizi SN, Donath SM, Bennett CM, Cooklin AR, Fisher JR, Payne MS, , 2011. The role of micro-organisms (Staphylococcus aureus and Candida albicans) in the pathogenesis of breast pain and infection in lactating women: study protocol. BMC Pregnancy Childbirth 11: 54.[Crossref]
  15. Betzold CM, , 2012. Results of microbial testing exploring the etiology of deep breast pain during lactation: a systematic review and meta-analysis of nonrandomized trials. J Midwifery Womens Health 57: 353364.[Crossref]
  16. Elram T, Livne A, Oren A, Gross I, Shapiro M, Mankuta D, , 2008. Labor as a bacteriuric event—assessment and risk factors. J Matern Fetal Neonatal Med 21: 483486.[Crossref]
  17. Knowles S, O'Sullivan N, Meenan A, Hanniffy R, Robson M, , 2014. Maternal sepsis incidence, aetiology and outcome for mother and fetus: a prospective study. BJOG 121: 17541755.[Crossref]
  18. Muhangi L, Woodburn P, Omara M, Omoding N, Kizito D, Mpairwe H, Nabulime J, Ameke C, Morison LA, Elliott AM, , 2007. Associations between mild-to-moderate anaemia in pregnancy and helminth, malaria and HIV infection in Entebbe, Uganda. Trans R Soc Trop Med Hyg 101: 899907.[Crossref]
  19. Adegnika AA, Ramharter M, Agnandji ST, Ateba Ngoa U, Issifou S, Yazdanbahksh M, Kremsner PG, , 2010. Epidemiology of parasitic co-infections during pregnancy in Lambarene, Gabon. Trop Med Int Health 15: 12041209.[Crossref]
  20. Ivan E, Crowther NJ, Rucogoza AT, Osuwat LO, Munyazesa E, Mutimura E, Njunwa KJ, Zambezi KJ, Grobusch MP, , 2012. Malaria and helminthic co-infection among HIV-positive pregnant women: prevalence and effects of antiretroviral therapy. Acta Trop 124: 179184.[Crossref]
  21. Liabsuetrakul T, Chaikongkeit P, Korviwattanagarn S, Petrueng C, Chaiya S, Hanvattanakul C, Kongkitkul P, Sinthuuthai C, Kalong N, Ongsawang D, Ungsathapornpon S, Ameeroh A, Bavonnarongdet P, Buadung A, , 2009. Epidemiology and the effect of treatment of soil-transmitted helminthiasis in pregnant women in southern Thailand. Southeast Asian J Trop Med Public Health 40: 211222.
  22. Franklin TL, Monif GR, , 2000. Trichomonas vaginalis and bacterial vaginosis. Coexistence in vaginal wet mount preparations from pregnant women. J Reprod Med 45: 131134.
  23. Goto A, Nguyen QV, Pham NM, Kato K, Cao TP, Le TH, Hoang QK, Le TQ, Nguyen BT, Katsube M, Ishii S, Yasumura S, , 2005. Prevalence of and factors associated with reproductive tract infections among pregnant women in ten communes in Nghe An province, Vietnam. J Epidemiol 15: 163172.[Crossref]
  24. Romoren M, Sundby J, Velauthapillai M, Rahman M, Klouman E, Hjortdahl P, , 2007. Chlamydia and gonorrhoea in pregnant Batswana women: time to discard the syndromic approach? BMC Infect Dis 7: 27.[Crossref]
  25. Lello J, Knopp S, Mohammed KA, Khamis IS, Utzinger J, Viney ME, , 2013. The relative contribution of co-infection to focal infection risk in children. Proc Biol Sci 280: 20122813.[Crossref]
  26. Cauci S, Culhane JF, , 2007. Modulation of vaginal immune response among pregnant women with bacterial vaginosis by Trichomonas vaginalis, Chlamydia trachomatis, Neisseria gonorrhoeae, and yeast. Am J Obstet Gynecol 196: 133.e1133.e7.[Crossref]
  27. Allsworth JE, Peipert JF, , 2011. Severity of bacterial vaginosis and the risk of sexually transmitted infection. Am J Obstet Gynecol 205: 113.e1113.e6.[Crossref]
  28. Balkus JE, Richardson BA, Rabe LK, Taha TE, Mgodi N, Kasaro MP, Ramjee G, Hoffman IF, Abdool Karim SS, , 2014. Bacterial vaginosis and the risk of Trichomonas vaginalis acquisition among HIV-1-negative women. Sex Transm Dis 41: 123128.[Crossref]
  29. Ezenwa VO, Jolles AE, , 2011. From host immunity to pathogen invasion: the effects of helminth coinfection on the dynamics of microparasites. Integr Comp Biol 51: 540551.[Crossref]
  30. Friberg IM, Little S, Ralli C, Lowe A, Hall A, Jackson JA, Bradley JE, , 2013. Macroparasites at peripheral sites of infection are major and dynamic modifiers of systemic antimicrobial pattern recognition responses. Mol Ecol 22: 28102826.[Crossref]
  31. Getachew M, Tafess K, Zeynudin A, Yewhalaw D, , 2013. Prevalence of soil transmitted helminthiasis and malaria co-infection among pregnant women and risk factors in Gilgel Gibe Dam area, southwest Ethiopia. BMC Res Notes 6: 263.[Crossref]
  32. Hartgers FC, Yazdanbakhsh M, , 2006. Co-infection of helminths and malaria: modulation of the immune responses to malaria. Parasite Immunol 28: 497506.[Crossref]
  33. Supali T, Verweij JJ, Wiria AE, Djuardi Y, Hamid F, Kaisar MM, Wammes LJ, van Lieshout L, Luty AJ, Sartono E, Yazdanbakhsh M, , 2010. Polyparasitism and its impact on the immune system. Int J Parasitol 40: 11711176.[Crossref]
  34. Graham AL, Cattadori IM, Lloyd-Smith JO, Ferrari MJ, Bjornstad ON, , 2007. Transmission consequences of coinfection: cytokines writ large? Trends Parasitol 23: 284291.[Crossref]
  35. Fenton A, , 2013. Dances with worms: the ecological and evolutionary impacts of deworming on coinfecting pathogens. Parasitology 140: 11191132.[Crossref]
  36. Singer M, , 2013. Development, coinfection, and the syndemics of pregnancy in sub-Saharan Africa. Infect Dis Poverty 2: 26.[Crossref]
  37. Sistema de Naciones Unidas, Gobierno de la República de Panamá, 2009. Objetivos de desarrollo del Milenio, III Informe de Panamá, 2009, 1st Ed. Apartadó, República de Panamá: El PNUD en Panamá, 2736.
  38. Kuamri A, Goswami S, Mukherjee P, , 2013. Comparative study of various methods of fetal weight estimation in term pregnancy. South Asian Feder Obst Gynae 5: 2225.
  39. Fescina RH, De Mucio B, Martínez G, Alemán A, Sosa C, Mainero L, Rubino M, , 2011. Monitoring Fetal Growth: Self-Instruction Manual, 2nd Ed. Montevideo, Uruguay: PAHO, 1619.
  40. IOM and NRC, 2009. Weight Gain during Pregnancy: Reexamining the Guidelines. Washington, DC: The National Academies Press, 868.
  41. ACOG, 2002. ACOG practice bulletin. Diagnosis and management of preeclampsia and eclampsia. Number 33, January 2002. Obstet Gynecol 99: 159167.
  42. Hunter JM, Arbona SI, , 1995. The tooth as a marker of developing world quality of life: a field study in Guatemala. Soc Sci Med 41: 12171240.[Crossref]
  43. Simel DL, Rennie D, , 2009. The Rational Clinical Examination: Evidence-Based Clinical Diagnosis. New York, NY: McGraw Hill / JAMA Evidence, 774.
  44. Hicks MI, Elston DM, , 2009. Scabies. Dermatol Ther 22: 279292.[Crossref]
  45. Lazar AJF, Kumar V, Abbas AK, Fausto N, Mitchell R, , 2007. The skin. , eds. Robbins Basic Pathology, 8th Ed. Philadelphia, PA: Elsevier Health Sciences, 843844.
  46. Ollendorff AT, , 2012. Cervicitis Clinical Presentation. Medscape. Available at: http://emedicine.medscape.com/article/253402-clinical-a0256. Accessed June 12, 2014.
  47. Ryan CA, Courtois BN, Hawes SE, Stevens CE, Eschenbach DA, Holmes KK, , 1998. Risk assessment, symptoms, and signs as predictors of vulvovaginal and cervical infections in an urban US STD clinic: implications for use of STD algorithms. Sex Transm Infect 74 (Suppl 1): S59S76.
  48. Hainer BL, Gibson MV, , 2011. Vaginitis. Am Fam Physician 83: 807815.
  49. Patil MJ, Nagamoti JM, Metgud SC, , 2012. Diagnosis of Trichomonas vaginalis from vaginal specimens by wet mount microscopy, in pouch TV culture system, and PCR. J Glob Infect Dis 4: 2225.[Crossref]
  50. Nugent RP, Krohn MA, Hillier SL, , 1991. Reliability of diagnosing bacterial vaginosis is improved by a standardized method of gram stain interpretation. J Clin Microbiol 29: 297301.
  51. Coppolillo EF, Perazzi BE, Famiglietti AM, Cora Eliseht MG, Vay CA, Barata AD, , 2003. Diagnosis of bacterial vaginosis during pregnancy. J Low Genit Tract Dis 7: 117121.[Crossref]
  52. Deville WL, Yzermans JC, van Duijn NP, Bezemer PD, van der Windt DA, Bouter LM, , 2004. The urine dipstick test useful to rule out infections. A meta-analysis of the accuracy. BMC Urol 4: 4.[Crossref]
  53. Simerville JA, Maxted WC, Pahira JJ, , 2005. Urinalysis: a comprehensive review. Am Fam Physician 71: 11531162.
  54. Caron F, , 2010. Diagnosis and treatment of community-acquired urinary tract infections in adults: what has changed. Comments on the 2008 guidelines of the French health products safety agency (AFSSAPS). Presse Med 39: 4248.[Crossref]
  55. WHO, 1991. Basic Laboratory Methods in Medical Parasitology, 1st Ed. England, United Kingdom: World Health Organization, 2528.
  56. Cringoli G, Rinaldi L, Maurelli MP, Utzinger J, , 2010. FLOTAC: new multivalent techniques for qualitative and quantitative copromicroscopic diagnosis of parasites in animals and humans. Nat Protoc 5: 503515.[Crossref]
  57. Knopp S, Speich B, Hattendorf J, Rinaldi L, Mohammed KA, Khamis IS, Mohammed AS, Albonico M, Rollinson D, Marti H, Cringoli G, Utzinger J, , 2011. Diagnostic accuracy of Kato-Katz and FLOTAC for assessing anthelmintic drug efficacy. PLoS Negl Trop Dis 5: e1036.[Crossref]
  58. Hellard E, Pontier D, Sauvage F, Poulet H, Fouchet D, , 2012. True versus false parasite interactions: a robust method to take risk factors into account and its application to feline viruses. PLoS ONE 7: e29618.[Crossref]
  59. Soong D, Einarson A, , 2009. Vaginal yeast infections during pregnancy. Can Fam Physician 55: 255256.
  60. Edwards JL, , 2010. Neisseria gonorrhoeae survival during primary human cervical epithelial cell infection requires nitric oxide and is augmented by progesterone. Infect Immun 78: 12021213.[Crossref]
  61. Chandiramani M, Lee Y, Kindinger L, Arulkumaran S, Marchesi J, Holmes E, Nicholson J, Teoh T, MacIntyre D, Bennett P, , 2014. The evolution of the vaginal microbiome throughout uncomplicated pregnancy in a UK population. Arch Dis Child Fetal Neonatal Ed 99 (Suppl 1): A12A13.
  62. Yang XL, Yang HX, Duan T, He J, Sun LZ, Yu YH, Liu XH, Li XM, , 2009. Vaginal microflora and relevant factors in puerperium. Zhonghua Fu Chan Ke Za Zhi 44: 496499.
  63. Demirezen S, Korkmaz E, Beksac MS, , 2005. Association between trichomoniasis and bacterial vaginosis: examination of 600 cervicovaginal smears. Cent Eur J Public Health 13: 9698.
  64. Heller DS, Maslyak S, Skurnick J, , 2006. Is the presence of Trichomonas on a Pap smear associated with an increased incidence of bacterial vaginosis? J Low Genit Tract Dis 10: 137139.[Crossref]
  65. Uma S, Balakrishnan P, Murugavel KG, Srikrishnan AK, Kumarasamy N, Anand S, Cecelia JA, Celentano D, Mayer KH, Thyagarajan SP, Solomon S, , 2006. Bacterial vaginosis in women of low socioeconomic status living in slum areas in Chennai, India. Sex Health 3: 297298.[Crossref]
  66. Brotman RM, Klebanoff MA, Nansel TR, Yu KF, Andrews WW, Zhang J, Schwebke JR, , 2010. Bacterial vaginosis assessed by gram stain and diminished colonization resistance to incident gonococcal, chlamydial, and trichomonal genital infection. J Infect Dis 202: 19071915.[Crossref]
  67. Amdekar S, Singh V, Singh DD, , 2011. Probiotic therapy: immunomodulating approach toward urinary tract infection. Curr Microbiol 63: 484490.[Crossref]
  68. Cadieux PA, Burton J, Devillard E, Reid G, , 2009. Lactobacillus by-products inhibit the growth and virulence of uropathogenic Escherichia coli . J Physiol Pharmacol 60 (Suppl 6): 1318.
  69. Liu MB, Xu SR, He Y, Deng GH, Sheng HF, Huang XM, Ouyang CY, Zhou HW, , 2013. Diverse vaginal microbiomes in reproductive-age women with vulvovaginal candidiasis. PLoS ONE 8: e79812.[Crossref]
  70. Dea-Ayuela MA, Rama-Iniguez S, Bolas-Fernandez F, , 2008. Enhanced susceptibility to Trichuris muris infection of B10Br mice treated with the probiotic Lactobacillus casei . Int Immunopharmacol 8: 2835.[Crossref]
  71. McClemens J, Kim JJ, Wang H, Mao YK, Collins M, Kunze W, Bienenstock J, Forsythe P, Khan WI, , 2013. Lactobacillus rhamnosus ingestion promotes innate host defense in an enteric parasitic infection. Clin Vaccine Immunol 20: 818826.[Crossref]
  72. Yatich NJ, Funkhouser E, Ehiri JE, Agbenyega T, Stiles JK, Rayner JC, Turpin A, Ellis WO, Jiang Y, Williams JH, Afriyie-Gwayu E, Phillips T, Jolly PE, , 2010. Malaria, intestinal helminths and other risk factors for stillbirth in Ghana. Infect Dis Obstet Gynecol 2010: 350763.[Crossref]
  73. Nguyen PH, Nguyen KC, Nguyen TD, Le MB, Bern C, Flores R, Martorell R, , 2006. Intestinal helminth infections among reproductive age women in Vietnam: prevalence, co-infection and risk factors. Southeast Asian J Trop Med Public Health 37: 865874.
  74. Fleming FM, Brooker S, Geiger SM, Caldas IR, Correa-Oliveira R, Hotez PJ, Bethony JM, , 2006. Synergistic associations between hookworm and other helminth species in a rural community in Brazil. Trop Med Int Health 11: 5664.[Crossref]
  75. Bethony J, Brooker S, Albonico M, Geiger SM, Loukas A, Diemert D, Hotez PJ, , 2006. Soil-transmitted helminth infections: ascariasis, trichuriasis, and hookworm. Lancet 367: 15211532.[Crossref]
  76. Scott ME, , 2008. Ascaris lumbricoides: a review of its epidemiology and relationship to other infections. Ann Nestlé 66: 1127.
  77. Halpenny CM, Paller C, Koski KG, Valdes VE, Scott ME, , 2013. Regional, household and individual factors that influence soil transmitted helminth reinfection dynamics in preschool children from rural indigenous Panama. PLoS Negl Trop Dis 7: e2070.[Crossref]
  78. Tarafder MR, Carabin H, McGarvey ST, Joseph L, Balolong E, Jr Olveda R, , 2011. Assessing the impact of misclassification error on an epidemiological association between two helminthic infections. PLoS Negl Trop Dis 5: e995.[Crossref]
  79. Fenton A, Viney ME, Lello J, , 2010. Detecting interspecific macroparasite interactions from ecological data: patterns and process. Ecol Lett 13: 606615.[Crossref]
  80. Myziuk L, Romanowski B, Brown M, , 2001. Endocervical gram stain smears and their usefulness in the diagnosis of Chlamydia trachomatis . Sex Transm Infect 77: 103106.[Crossref]
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  • Received : 30 Aug 2014
  • Accepted : 21 Feb 2015

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