Is diabetes mellitus a risk factor in genital yeast infections?

Česká verzia

Authors: V. Buchta ^1,2; V. Matula ³; J. Kestřánek ³; M. Vejsová ^1,2; L. Křivčíková ²; J. Špaček ³
Authors place of work: Ústav klinické mikrobiologie LF UK a FN, Hradec Králové, přednosta doc. RNDr. V. Buchta, CSc. ¹; Katedra biologických a lékařských věd, Farmaceutická fakulta LF UK, Hradec Králové, vedoucí doc. PharmDr. P. Nachtigal, Ph. D. ²; Porodnicko-gynekologická klinika LF UK a FN, Hradec Králové, přednosta doc. MUDr. J. Špaček, Ph. D., IFEPAG ³
Published in the journal: Ceska Gynekol 2013; 78(6): 537-544
Category: Original Article

Summary

Objective:
To analyze experimental and clinical data on diabetes mellitus (DM) related to infections with focus on vaginal mycosis. To evaluate a role of DM in the epidemiology of vulvovaginal candidiasis.

Design:
Review.

Setting:
Department of Clinical Microbiology, Department of Biological and Medical Sciences, Faculty of Pharmacy, Department of Obstetrics and Gynecology, Charles University in Prague, Faculty of Medicine and University Hospital Hradec Kralove.

Methods:
Review of literature data.

Results:
DM is a risk factor for fungal infections caused by yeasts (Candida albicans), members of Mucorales fungi, some dimorphic fungi (Coccidioides) and agents of onychomycosis. DM is usually associated only with increased colonization of the anatomical sites (oral cavity, vagina), and/ or with an intensified symptomatology of infection (onychomycosis, mucormycosis). Diabetic patients with oropharyngeal and vulvovaginal candidiasis have frequently changed etiology spectrum. The patients with VVC and DM, especially of older age or with prone to relapses, have tendency to shift of the spectrum to non-albicans species, mainly C. glabrata. Treatment of VVC in diabetic patients can be complicated owing to unfavourable antifungal susceptibility profile (C. glabrata) and/ or adverse interactions between some azole antifungals and sulfonylurea-based antidiabetics.

Conclusion:
Diabetes mellitus is often cited as a risk factor, although in many cases there is a lack of reliable and clinically relevant information. This does not mean that this disease can be underestimated. On the contrary, it is necessary to get the DM as soon as possible under control and thus prevent complications when infection develops. Invidual approach should be apllied to the diabetic patients at risk of an infection. Yeast colonization and development of vaginal infection is complex process primarily dependent on sexual hormones, indigenous microbiota and finely tuned mechanisms of local immunity. Role of DM consists in the fact that it is one of the important co-factors that can change the setup of the vaginal environment in favour of yeasts and thus promote or facilitate the development of VVC.

Keywords:
diabetes mellitus – hyperglycemia – risk factors – infections – fungi – yeasts – Candida albicans – Candida glabrata

Zdroje

1. Ahmed, MS., Reid, E., Khardori, N. Respiratory infections in diabetes: Reviewing the risks and challenges. J Respir Dis, 2008, 29, 7, p. 285–293.

2. Alteras, I., Saryt, E. Prevalence of pathogenic fungi in the toe-webs and toe-nails of diabetic patients. Mycopathologia, 1979, 67, p. 157–159.

3. Arzeni, D., Del Poeta, M., Simonetti, O., et al. Prevalence and antifungal susceptibility of vaginal yeasts in outpatients attending a gynecological center in Ancona, Italy. Eur J Epidemiol, 1997, 13, 4, p. 447–450.

4. Babula, O., Lazdane, G., Kroica, J., et al. Relation between recurrent vulvovaginal candidiasis, vaginal concentrations of mannose-binding lectin, and a mannose-binding lectin gene polymorphism in Latvian women. Clin Infect Dis, 2003, 37, 5, p. 733–737.

5. Babula, O., Lazdāne, G., Kroica, J., et al. Frequency of interleukin-4 (IL-4) – 589 gene polymorphism and vaginal concentrations of IL-4, nitric oxide, and mannose-binding lectin in women with recurrent vulvovaginal candidiasis. Clin Infect Dis, 2005, 40, 9, p. 1258–1262.

6. Bader, MS. Diabetic foot infection. Am Fam Physician, 2008, 78, 1, p. 71–79.

7. Bagdade, JD., Root, RK., Bulger, RJ. Impaired leukocyte function in patients with poorly controlled diabetes. Diabetes, 1974, 23, 1, p. 9–15.

8. Bagdade, JD., Stewart, M., Walters, E. Impaired granulocyte adherence. A reversible defect in host defense in patients with poorly controlled diabetes. Diabetes, 1978, 27, 6, p. 677–681.

9. Belazi, M., Velegraki, A., Fleva, A., et al. Candidal over-growth in diabetic patients: potential predisposing factors. Mycoses, 2005, 48, 3, p. 192–196.

10. Bhattacharya, SK., Shastri, S., Mahajan, P., et al. Poly-morphonuclear leukocyte function in type-2 diabetes mellitus patients and its correlation with glycemic control. Nepal Med Coll J, 2007, 9, p. 111–116.

11. Bohannon, NJ. Treatment of vulvovaginal candidiasis in patients with diabetes. Diabetes Care, 1998, 21, 3, p. 451–456.

12. Buchta, V., Slezák, R., Špaček, J., et al. Současné možnosti léčby kožních a slizničních mykóz. Med pro Praxi, 2009, 6, 3, s. 155–164.

13. Buchta, V., Špaček, J. Úskalí současné laboratorní diagnostiky a terapie vulvovaginální kandidózy. Klin Mikrobiol Infekc Lek, 2011,17, 5, s. 158–163.

14. Corsello, S., Spinillo, A., Osnengo, G., et al. An epidemiological survey of vulvovaginal candidiasis in Italy. Eur J Obstet Gynecol Reprod Biol, 2003, 110, 1, p. 66–72.

15. Calderone, RA., Fonzi, WA. Virulence factors of Candida albicans. Trends Microbiol, 2001, 9, 7, p. 327–335.

16. de Leon, EM., Jacober, SJ., Sobel, JD., Foxman, B. Prevalence and risk factors for vaginal Candida colonization in women with type 1 and type 2 diabetes. BMC Infect Dis, 2002, 2:1. Epub 2002 Jan 30.

17. Delamaire, M., Maugendre, D., Moreno, M., et al. Impaired leukocyte function in diabetic patients. Diabet Med. 1997, 14, 1, p. 29–34.

18. Donders, GG. Lower genital tract infections in diabetic women. Curr Infect Dis Rep, 2002, 4, p. 536–539.

19. Donders, GG., Prenen, H., Verbeke, G., Reybrouck, R. Impaired tolerance for glucose in women with recurrent vaginal candidiasis. Am J Obstet Gynecol, 2002, 187, 4, p. 989–993.

20. Edwards, JE. Jr, Gaither, TA., O‘Shea, JJ., et al. Expression of specific binding sites on Candida with functional and antigenic characteristics of human complement receptors. J Immunol, 1986, 137, 11, p. 3577–3583.

21. Ehrström, S., Yu, A., Rylander, E. Glucose in vaginal secretions before and after oral glucose tolerance testing in women with and without recurrent vulvovaginal candidiasis. Obstet Gynecol, 2006, 108, 6, p. 1432–1437.

22. Fan, SR., Liu, XP., Li, JW. Clinical characteristics of vulvovaginal candidiasis and antifungal susceptibilities of Candida species isolates among patients in southern China from 2003 to 2006.J Obstet Gynaecol Res, 2008, 34, 4, p. 561–566.

23. Fidel, PL. Jr. Distinct protective host defenses against oral and vaginal candidiasis. Med Mycol, 2002, 40, 4, p. 359–375.

24. Fisher, JF., Newman, CL., Sobel, JD. Yeast in the urine: solutions for a budding problem. Clin Infect Dis, 1995, 20, p. 183–189.

25. Gallacher, SJ., Thomson, G., Fraser, WD., et al. Neutrophil bactericidal function in diabetes mellitus: evidence for association with blood glucose control. Diabet Med, 1995, 12, p. 916–920.

26. Geerlings, SE., Hoepelman, AI. Immune dysfunction in pa-tients with diabetes mellitus (DM). FEMS Immunol Med Microbiol, 1999, 26, p. 259–265.

27. Gilmore, BJ., Retsinas, EM., Lorenz, JS., Hostetter, MK. An iC3b receptor on Candida albicans: structure, function, and correlates for pathogenicity. J Infect Dis, 1988, 157, p. 38–43.

28. Goswamim, R., Dadhwal, V., Tejaswi, S., et al. Species-specific prevalence of vaginal candidiasis among patients with diabetes mellitus and its relation to their glycaemic status. J Infect, 2000, 41, 2, p. 162–166.

29. Goswami, D., Goswami, R., Banerjee, U., et al. Pattern of Candida species isolated from patients with diabetes mellitus and vulvovaginal candidiasis and their response to single dose oral fluconazole therapy. J Infect, 2006, 52, p. 111–117.

30. Greene, MT., Chang, R., Kuhn, L., Rogers, MA., et al. Predictors of hospital-acquired urinary tract-related bloodstream infection. Infect Control Hosp Epidemiol, 2012, 33, 10, p. 1001–1007.

31. Gupta, AK., Humke, S. The prevalence and management of onychomycosis in diabetes patients. Eur J Dermatol, 2000, 10, p. 379–384.

32. Holland, J., Young, ML., Lee, O., C-A Chen S. Vulvovaginal carriage of yeasts other than Candida albicans. Sex Transm Infect, 2003, 79, p. 249–250.

33. Horowitz, BJ., Edelstein, SW., Lippman, L. Sugar chromatography studies in recurrent Candida vulvovaginitis. J Reprod Med, 1984, 29, 7, p. 441–443.

34. Hostetter, PW. Perspectives in diabetes: handicaps to host defence. Effects of hyperglycemia on C3 and Candida albicans. Diabetes, 1990, 39, p. 271–275.

35. Hu, KK., Boyko, EJ., Scholes, D., et al. Risk factors for urinary tract infections in postmenopausal women. Arch Intern Med, 2004, 164, p. 989–993.

36. Jeon, CY., Murray, MB. Diabetes mellitus increases the risk of active tuberculosis: a systematic review of 13 observational studies. PLoS Med, 2008, 5, e152.

37. Joshi, N., Caputo, GM., Weitekamp, MR., Karchmer, AW. Infections in patients with diabetes mellitus. N Engl J Med, 1999, 341, 25, p. 1906–1912.

38. Jurevic, RJ., Bai, M., Chadwick, RB., et al. Single-nucleotide polymorphisms (SNPs) in human beta-defensin 1: high-throughput SNP assays and association with Candida carriage in type I diabetics and nondiabetic controls. J Clin Microbiol, 2003, 41, p. 90–96.

39. Kao, AS., Brandt, ME., Pruitt, WR., et al. The epidemiology of candidemia in two United States cities: results of a population-based active surveillance. Clin Infect Dis, 1999, 29, 5, p. 1164–1170.

40. Kornum, JB., Thomsen, RW., Riis, A., et al. Type 2 diabetes and pneumonia outcomes: a population-based cohort study. Diabetes Care, 2007, 30, 9, p. 2251–2257.

41. Koziel, H., Koziel, MJ. Pulmonary complications of diabetes mellitus. Infect Dis Clin North Am, 1995, 9, p. 65–96.

42. Krcmery, V., Jurga, L., Mateicka, F., Sulcová, M. Fungaemia in elderly patients. Int J Antimicrob Agents, 2001, 17, 5, p. 419–421.

43. Leth, RA., Uldbjerg, N., Nørgaard, M., et al. Obesity, diabetes, and the risk of infections diagnosed in hospital and post-discharge infections after cesarean section: a prospective cohort study. Acta Obstet Gynecol Scand, 2011, 90, 5, p. 501–509.

44. Lind, M., Garcia-Rodriguez, LA., Booth, GL., et al. Mortality trends in patients with and without diabetes in Ontario, Canada and the UK from 1996 to 2009: a population-based study. Diabetologia, 2013 Jun 22. [Epub ahead of print]

45. McFarlane, SI., Muniyappa, R., Francisco, R., Sowers, JR. Clinical review 145: pleiotropic effects of statins: lipid reduction and beyond. J Clin Endocrinol Metab, 2002, 87, 4, p. 1451–1458.

46. Muchova, J., Liptakova, A., Orszaghova, Z., et al. Antioxidant systems in polymorphonuclear leucocytes of type 2 diabetes mellitus. Diabet Med, 1999, 16, p. 74–78.

47. Muller, LM., Gorter, KJ., Hak, E., et al. Increased risk of common infections in patients with type 1 and type 2 diabetes mellitus. Clin Infect Dis, 2005, 41, 3, p. 281–288.

48. Muñoz-Hernández, B., Martínez-Rivera, MA., Palma Cortés, G., et al. Mycelial forms of Coccidioides spp. in the parasitic phase associated to pulmonary coccidioidomycosis with type 2 diabetes mellitus. Eur J Clin Microbiol Infect Dis, 2008, 27, 9, p. 813–820.

49. Nowakowska, D., Kurnatowska, A., Stray-Pedersen, B., Wilczyński, J. Activity of hydrolytic enzymes in fungi isolated from diabetic pregnant women: is there any relationship between fungal alkaline and acid phosphatase activity and glycemic control? APMIS, 2004, 112, 6, p. 374–383.

50. Nwobu, RA., Agbonlahor, DE., Odugbemi, TO. Adherence of Candida albicans to human vaginal epithelial cells. East Afr Med J, 1997, 74, 6, p. 389–391.

51. Ozcan, SK., Budak, F., Yucesoy, G., et al. Prevalence, susceptibility profile and proteinase production of yeasts causing vulvovaginitis in Turkish women. APMIS, 2006, 114, 2, p. 139–145.

52. Paulitsch, A., Weger, W., Ginter-Hanselmayer, G., et al. A 5-year (2000–2004) epidemiological survey of Candida and non-Candida yeast species causing vulvovaginal candidiasis in Graz, Austria. Mycoses, 2006, 49, 6, p. 471–475.

53. Peer, AK., Hoosen, AA., Seedat, MA., et al. Vaginal yeast infections in diabetic women. S Afr Med J, 1993, 83, 10, p. 727–729.

54. Peleg, AY., Weerarathna, T., McCarthy, JS., Davis, TM. Common infections in diabetes: pathogenesis, management and relationship to glycaemic control. Diabetes Metab Res Rev, 2007, 23, p. 3–13.

55. Petrikkos, G., Skiada, A., Lortholary, O., et al. Epidemiology and clinical manifestations of mucormycosis. Clin Infect Dis, 2012, 54 Suppl 1, p. S23–S34.

56. Ray, D., Goswami, R., Banerjee, U., et al. Prevalence of Candida glabrata and its response to boric acid vaginal suppositories in comparison with oral fluconazole in patients with diabetes and vulvovaginal candidiasis. Diabetes Care, 2007, 30, 2, p. 312–317.

57. Ray, D., Goswami, R., Dadhwal, V., et al. Prolonged (3-month) mycological cure rate after boric acid suppositories in diabetic women with vulvovaginal candidiasis. J Infect, 2007, 55, 4, p. 374–377.

58. Rayfield, EJ., Ault, MJ., Keusch, GT., et al. Infection and diabetes: the case for glucose control. Am J Med, 1982, 72, 3, p. 439–450.

59. Rich, P., Hare, A. Onychomycosis in special patient population: focus on the diabetic. Int J Dermatol, 1999, 38, suppl. 2, p. 17–19.

60. Rowe, BR., Logan, MN., Farrell, I., Barnett, AH. Is candidiasis the true cause of vulvovaginal irritation in women with diabetes mellitus? J Clin Pathol, 1990, 43, 8, p. 644–645.

61. Saiepour, D., Sehlin, J., Oldenborg, PA. Insulin inhibits phagocytosis in normal human neutrophils via PKC alpha/beta-dependent priming of F-actin assembly. Inflamm Res, 2006, 55, p. 85–91.

62. Saint, S., Kaufman, SR., Rogers, MA., et al. Risk factors for nosocomial urinary tract-related bacteremia: a case-control study. Am J Infect Control, 2006, 34, 7, p. 401–407.

63. Santelli, AC., Blair, JE., Roust, LR. Coccidioidomycosis in patients with diabetes mellitus. Am J Med, 2006, 119, 11, p. 964–969.

64. Segal, E., Soroka, A., Schechter, A. Correlative relationship between adherence of Candida albicans to human vaginalepithelial cells in vitro and candidal vaginitis. Sabouraudia, 1984, 22, 3, p. 191–200.

65. Shah, BR., Hux, JE. Quantifying the risk of infectious diseases for people with diabetes. Diabetes Care, 2003, 26, p. 510–513.

66. Schelleman, H., Bilker, WB., Brensinger, CM., et al. Anti-infectives and the risk of severe hypoglycemia in users of glipizide or glyburide. Clin Pharmacol Ther, 2010, 88, 2, p. 214–222.

67. Skořepová, M. Mykózy a diabetes. Vnitr Lek, 2006, 52, 5, s. 470–473.

68. Sobel, JD. Vulvovaginal candidiasis. Lancet, 2007, 369, 9577, p. 1961–1971.

69. Sobel, JD., Faro, S., Force, RW., et al. Vulvovaginal candidiasis: epidemiologic, diagnostic, and therapeutic considerations. Am J Obstet Gynecol, 1998, 178, 2, p. 203–211.

70. Sobel, JD., Kapernick, PS., Zervos, M., et al. Treatment of complicated Candida vaginitis: comparison of single and sequential doses of fluconazole. Am J Obstet Gynecol, 2001, 185, 2, p. 363–369.

71. Sobel, JD., Mueller, G., Buckley, H. Critical role of germ tube formation in the pathogenesis of candidal vaginitis. Infect Immun, 1984, 44, p. 576–579.

72. Soll, DR. Candida commensalism and virulence: the evolution of phenotypic plasticity. Acta Trop, 2002, 81, 2, p. 101–110.

73. Soysa, NS., Samaranayake, LP., Ellepola, AN. Diabetes mellitus as a contributory factor in oral candidosis. Diabet Med, 2006, 23, 5, p. 455–459.

74. Spanakis, EK., Kourkoumpetis, TK., Livanis, G., et al. Statin therapy and decreased incidence of positive Candida cultures among patients with type 2 diabetes mellitus undergoing gastrointestinal surgery. Mayo Clin Proc, 2010, 85, 12, p. 1073–1079.

75. Spinillo, A., Capuzzo, E., Gulminetti, R., et al. Prevalence of and risk factors for fungal vaginitis caused by non-albicans species. Am J Obstet Gynecol, 1997, 176, 1, Pt 1, p. 138–141.

76. Sun, HY., Singh, N. Antimicrobial and immunomodulatory attributes of statins: relevance in solid-organ transplant recipients. Clin Infect Dis, 2009, 48, 6, p. 745–755.

77. Tuazon, CU. Skin and skin structure infections in the patient at risk: carrier state of Staphylococcus aureus. Am J Med, 1984, 76, 5A, p. 166–171.

78. Turina, M., Fry, DE., Polk, HC. Jr. Acute hyperglycemia and innate immune system: clinical, cellular, and molecular aspects. Crit Care Med,. 2005, 33, p. 1624–1633.

79. Valerius, NH., Eff, C., Hansen, NE., et al. Neutrophil and lymphocyte function in patients with diabetes mellitus. Acta Med Scand, 1982, 211, p. 463–472.

80. Vracko, R., Thorning, D., Huang, TW. Basal lamina of alveolar epithelium and capillaries: quantitive changes with aging and diabetes mellitus. Am Rev Respir Dis, 1979, 120, p. 973–983.

81. Wojitani, MD., de Aguiar, LM., Baracat, EC., Linhares, IM. Association between mannose-binding lectin and interleukin-1 receptor antagonist gene polymorphisms and recurrent vulvovaginal candidiasis. Arch Gynecol Obstet, 2012, 285, 1, p. 149–153.

82. Xu, J., Sobel, JD. Candida vulvovaginitis in pregnancy. Curr Infect Dis Rep, 2004, 6, 6, p. 445–449.

83. Yang, H., Wei, Y., Gao, X., et al. Risk factors for gestational diabetes mellitus in Chinese women: a prospective study of 16,286 pregnant women in China. Diabet Med, 2009, 26, 11, p. 1099–1104.

84. Zanobetti, A., Schwartz, J. Are diabetics more susceptible to the health effects of airborne particles? Am J Respir Crit Care Med, 2001, 164, 5, p. 831–833.

85. Zheng, NN., Guo, XC., Liv, W., et al. Characterization of the vaginal fungal flora in pregnant diabetic women by 18S rRNA sequencing. Eur J Clin Microbiol Infect Dis, 2013, 32, 8, p. 1031–1040.