Incidence and risk factors of asymptomatic bacteriuria in patients with type 2 diabetes mellitus: a meta-analysis.

Mengqiao Dai, Shan Hua, Jiechao Yang, Dandan Geng, Weina Li, Shuqin Hu, Hu Chen, Xiaoqin Liao
Author Information
  1. Mengqiao Dai: Shanghai University of Traditional Chinese Medicine, School of Nursing, Shanghai, 201203, China.
  2. Shan Hua: Department of Urology, Shanghai General Hospital, Shanghai Jiao Tong University School of Medicine, Shanghai, China.
  3. Jiechao Yang: Shanghai University of Traditional Chinese Medicine, School of Nursing, Shanghai, 201203, China.
  4. Dandan Geng: Shanghai University of Traditional Chinese Medicine, School of Nursing, Shanghai, 201203, China.
  5. Weina Li: Shanghai University of Traditional Chinese Medicine, School of Nursing, Shanghai, 201203, China.
  6. Shuqin Hu: Shanghai University of Traditional Chinese Medicine, School of Nursing, Shanghai, 201203, China.
  7. Hu Chen: Shanghai University of Traditional Chinese Medicine, School of Nursing, Shanghai, 201203, China.
  8. Xiaoqin Liao: Shanghai University of Traditional Chinese Medicine, School of Nursing, Shanghai, 201203, China. pomeliao@aliyun.com.

Abstract

BACKGROUND: The prevalence of type 2 diabetes mellitus (T2DM) is increasing each year and has become one of the most prominent health concerns worldwide. Patients with T2DM are prone to infectious diseases, and urinary tract infections are also widespread. Despite a comprehensive understanding of urinary tract infection (UTI), there is a lack of research regarding primary prevention strategies for asymptomatic bacteriuria (ASB).
OBJECTIVE: To clarify the incidence and risk factors of asymptomatic urinary tract infection in patients with T2DM by meta-analysis to provide evidence for preventing UTI. Help patients, their families, and caregivers to identify the risk factors of patients in time and intervene to reduce the incidence of ASB in patients with T2DM. Fill in the gaps in existing research.
STUDY DESIGN: Meta-analyses were conducted in line with PRISMA guidelines.
METHODS: Eleven databases were systematically searched for articles about ASB in T2DM, and the retrieval time was selected from the establishment of the database to February 5, 2023. Literature screening, quality evaluation, and meta-analysis were independently performed by two researchers according to the inclusion and exclusion criteria, and a meta-analysis was performed using Stata 17.0.
RESULTS: Fourteen articles were included, including cohort and case-control studies. A meta-analysis of 4044 patients with T2DM was included. The incidence of ASB in patients with T2DM was 23.7%(95% CI (0.183, 0.291); P < 0.001). After controlling for confounding variables, the following risk factors were associated with ASB in patients with T2DM: age (WMD = 3.18, 95% CI (1.91, 4.45), I = 75.5%, P < 0.001), female sex (OR = 1.07, 95% CI(1.02, 1.12), I = 79.3%, P = 0.002), duration of type 2 diabetes (WMD = 2.54, 95% CI (1.53, 5.43), I = 80.7%, P < 0.001), HbA1c (WMD = 0.63, 95% CI (0.43, 0.84), I = 62.6,%. P < 0.001), hypertension (OR = 1.59, 95% CI (1.24, 2.04), I = 0%, <0.001), hyperlipidemia (OR = 1.66, 95% CI (1.27, 2.18), I = 0%, P < 0.001), Neuropathy (OR = 1.81, 95% CI (1.38, 2.37), I = 0%, P < 0.001), proteinuria (OR = 3.00, 95% CI (1.82, 4.95), I = 62.7%, P < 0.001).
CONCLUSION: The overall prevalence of ASB in T2DM is 23.7%. Age, female sex, course of T2DM, HbA1C, hypertension, hyperlipidemia, neuropathy, and proteinuria were identified as related risk factors for ASB in T2DM. These findings can provide a robust theoretical basis for preventing and managing ASB in T2DM.

Keywords

References

  1. A.D. Association, Classification and diagnosis of diabetes: standards of medical care in diabetes—2021. Diabetes Care 44(Supplement_1), S15–S33 (2020). https://doi.org/10.2337/dc21-S002 [DOI: 10.2337/dc21-S002]
  2. A.D. Association, Diagnosis and classification of diabetes mellitus. Diabetes Care 37(Supplement_1), S81–S90 (2013). https://doi.org/10.2337/dc14-S081 [DOI: 10.2337/dc14-S081]
  3. J.B. Cole, J.C. Florez, Genetics of diabetes mellitus and diabetes complications. Nat. Rev. Nephrol. 16(Jul), 377–390 (2020). https://doi.org/10.1038/s41581-020-0278-5 [DOI: 10.1038/s41581-020-0278-5]
  4. IDF Diabetes Atlas 2021. Available at: https://diabetesatlas.org/atlas/tenth-edition/
  5. J. Casqueiro, J. Casqueiro, C. Alves, Infections in patients with diabetes mellitus: a review of pathogenesis. Indian J. Endocrinol. Metab. 16(Suppl1):S27–S36 (2012) https://doi.org/10.4103/2230-8210.94253
  6. I.M. Carey, J.A. Critchley, S. DeWilde, T. Harris, F.J. Hosking, D.G. Cook, Risk of infection in type 1 and type 2 diabetes compared with the general population: a matched cohort study. Diabetes Care 41(Mar), 513–521 (2018). https://doi.org/10.2337/dc17-2131 [DOI: 10.2337/dc17-2131]
  7. S.E. Geerlings, Urinary tract infections in patients with diabetes mellitus: epidemiology, pathogenesis and treatment. Int. J. Antimicrob. Agents 31(Suppl 1), S54–S57 (2008). https://doi.org/10.1016/j.ijantimicag.2007.07.042 [DOI: 10.1016/j.ijantimicag.2007.07.042]
  8. K.G. Naber, J. Tirán-Saucedo, F.M.E. Wagenlehner, Psychosocial burden of recurrent uncomplicated urinary tract infections. GMS Infect. Dis. 10, Doc01 (2022). https://doi.org/10.3205/id000078 [DOI: 10.3205/id000078]
  9. R. Raz, Asymptomatic bacteriuria. Clinical significance and management. Int. J. Antimicrob. Agents 22, 45–47 (2003). https://doi.org/10.1016/s0924-8579(03)00248-6 [DOI: 10.1016/s0924-8579(03)00248-6]
  10. LindsayE. Nicolle et al. Clinical practice guideline for the management of asymptomatic bacteriuria: 2019 update by the Infectious Diseases Society of America. Clin. Infect. Dis. 68(10), e83–e110 (2019). https://doi.org/10.1093/cid/ciy1121 [DOI: 10.1093/cid/ciy1121]
  11. L.E. Nicolle, K. Gupta, S.F. Bradley et al. Clinical Practice Guideline for the Management of Asymptomatic Bacteriuria: 2019 Update by the Infectious Diseases Society of America. Clin. Infect. Dis. 68(May), e83–e110 (2019). https://doi.org/10.1093/cid/ciy1121 [DOI: 10.1093/cid/ciy1121]
  12. T. Zhenzhen, T. Faqiang, J. Xuejin, Q. Bin, Analysis of urinary tract pathogens in asymptomatic bacteriuria patients. Lab. Med. Clin. 16(3), 421–423 (2019)
  13. L.E. Nicolle, Asymptomatic bacteriuria and bacterial interference. Microbiol Spectr. 3(Oct), (2015) https://doi.org/10.1128/microbiolspec.UTI-0001-2012
  14. M. Bonadio, E. Boldrini, G. Forotti et al. Asymptomatic bacteriuria in women with diabetes: influence of metabolic control. Clin. Infect. Dis. 38(Mar), e41–e45 (2004). https://doi.org/10.1086/381755 [DOI: 10.1086/381755]
  15. H. Al-Musa, Asymptomatic bacteriuria among type 2 diabetic females. Bahrain Med. Bull. 38, 82–85 (2016). https://doi.org/10.12816/0047594 [DOI: 10.12816/0047594]
  16. A. Ishay, I. Lavi, R. Luboshitzky, Prevalence and risk factors for asymptomatic bacteriuria in women with Type 2 diabetes mellitus. Diabet. Med. 23(Feb), 185–188 (2006). https://doi.org/10.1111/j.1464-5491.2005.01758.x [DOI: 10.1111/j.1464-5491.2005.01758.x]
  17. B.A. Laway, T. Nabi, M.H. Bhat, B.A. Fomda, Prevalence, clinical profile and follow up of asymptomatic bacteriuria in patients with type 2 diabetes-prospective case control study in Srinagar, India. Diabetes Metab. Syndr. 15(Jan–Feb), 455–459 (2021). https://doi.org/10.1016/j.dsx.2020.12.043 [DOI: 10.1016/j.dsx.2020.12.043]
  18. G. Matthiopoulou, P. Ioannou, A. Mathioudaki et al. Asymptomatic bacteriuria in patients with type 2 diabetes mellitus. Infect. Dis. Rep. 15(Jan), 43–54 (2023). https://doi.org/10.3390/idr15010005 [DOI: 10.3390/idr15010005]
  19. H. Turan, K. Serefhanoglu, A.N. Torun et al. Frequency, risk factors, and responsible pathogenic microorganisms of asymptomatic bacteriuria in patients with type 2 diabetes mellitus. Jpn J. Infect. Dis. 61(May), 236–238 (2008). https://doi.org/10.7883/yoken.jjid.2008.236 [DOI: 10.7883/yoken.jjid.2008.236]
  20. S.M.J. Zaidi, M. Kaneez, T. Almas et al. Gauging the risk factors for asymptomatic bacteriuria in type-2 diabetic women: a case-control study. Cureus 12(Jul), e9069 (2020). https://doi.org/10.7759/cureus.9069 [DOI: 10.7759/cureus.9069]
  21. Z. Yunxian, Z. Yuhua, Z. Lu, W. Qin, Clinical study on asymptomatic bacteriuria in adult female patients with type 2 diabetes mellitus. J. Hainan Med. Univ. (6):384–386 (2004) https://doi.org/10.3969/j.issn.1007-1237.2004.06.006
  22. C. Mingwei, C. Youmin, Changjiang W., et al. Clinical analysis of asymptomatic bacteriuria in female patients with type 2 diabetes mellitus. Clin. Focus. (24):1397–1399 (2003) https://doi.org/10.3969/j.issn.1004-583X.2003.24.006
  23. H. Dongjuan, Clinical analysis of type 2 diabetes mellitus complicated with asymptomatic bacteriuria in adult women. Zhejiang Clin. Med. (6):820–821 (2007) https://doi.org/10.3969/j.issn.1008-7664.2007.06.084
  24. K. Cenxiao, S. Xiaofei, M. Jianhua, L. Huiqin, Clinical observation and risk factors analysis of asymptomatic bacteriuria in elderly patients with type 2 diabetes mellitus. Chin. J. Diabetes 24(08), 726–728 (2016). https://doi.org/10.3969/j.issn.1006-6187.2016.08.014 [DOI: 10.3969/j.issn.1006-6187.2016.08.014]
  25. M. Congqing, M. Xinlong, F. Aijuan, C. Yingzi, D. Peng, Influencing factors of asymptomatic urinary tract infection in type 2 diabetes mellitus. Chin. J. Clin. (Electron. Ed.). 7(15), 7197–7198 (2013). https://doi.org/10.3969/cma.j.issn.1674-0785.2013.15.099 [DOI: 10.3969/cma.j.issn.1674-0785.2013.15.099]
  26. Y. Mianrong Fenying. Clinical characteristics and prevention of asymptomatic bacteriuria in female patients with type 2 diabetes mellitus. Chin. J. Rehabili. Theory Pract. (2), 67–68 (2005) https://doi.org/10.3969/j.issn.1006-9771.2005.02.027
  27. Z. Yiwen, S. Zhenwei, Prevalence and risk factors of asymptomatic bacteriuria in adults with type 2 diabetes mellitus. J. Mod. Lab. Med. 27(5), 25–28 (2012) https://doi.org/10.3969/j.issn.1671-7414.2012.05.009 [DOI: 10.3969/j.issn.1671-7414.2012.05.009]
  28. G.G. Zhanel, G.K. Harding, L.E. Nicolle, Asymptomatic bacteriuria in patients with diabetes mellitus. Rev. Infect. Dis. 13(Jan–Feb), 150–154 (1991). https://doi.org/10.1093/clinids/12.5.150 [DOI: 10.1093/clinids/12.5.150]
  29. L. Zhang, B. Wang, G. Yin et al. Rapid fluorescence sensor guided detection of urinary tract bacterial infections. Int. J. Nanomed. 17, 3723–3733 (2022). https://doi.org/10.2147/IJN.S377575 [DOI: 10.2147/IJN.S377575]
  30. S.E. Geerlings, Clinical presentations and epidemiology of urinary tract infections. Microbiol. Spectr. 4(Oct), (2016) https://doi.org/10.1128/microbiolspec.UTI-0002-2012
  31. A. Kautzky-Willer, J. Harreiter, G. Pacini, Sex and gender differences in risk, pathophysiology and complications of type 2 diabetes mellitus. Endocr. Rev. 37(Jun), 278–316 (2016). https://doi.org/10.1210/er.2015-1137 [DOI: 10.1210/er.2015-1137]
  32. X. Liu, P. Zhang, Y. Zhang et al. Glycolipid iGb3 feedback amplifies innate immune responses via CD1d reverse signaling. Cell Res. 29(Jan), 42–53 (2019). https://doi.org/10.1038/s41422-018-0122-7 [DOI: 10.1038/s41422-018-0122-7]
  33. G.J. Christ, W. Bushman, M.O. Fraser, Impact of diabetes and obesity on the prostate and urethra: implications to improved bladder dysfunction understanding and treatment. J. Urol. 182(Suppl), S38–S44 (2009). https://doi.org/10.1016/j.juro.2009.07.085 [DOI: 10.1016/j.juro.2009.07.085]
  34. S. Dalal, L. Nicolle, C.F. Marrs, L. Zhang, G. Harding, B. Foxman, Long-term Escherichia coli asymptomatic bacteriuria among women with diabetes mellitus. Clin. Infect. Dis. 49(Aug), 491–497 (2009). https://doi.org/10.1086/600883 [DOI: 10.1086/600883]
  35. J.A. Ashton-Miller, J.O. DeLancey, Functional anatomy of the female pelvic floor. Ann. N.Y. Acad. Sci. 1101(Apr), 266–296 (2007). https://doi.org/10.1196/annals.1389.034 [DOI: 10.1196/annals.1389.034]
  36. P.D. Olson, K.A. Hruska, D.A. Hunstad, Androgens enhance male urinary tract infection severity in a new model. J. Am. Soc. Nephrol. 27(Jun), 1625–1634 (2016). https://doi.org/10.1681/ASN.2015030327 [DOI: 10.1681/ASN.2015030327]
  37. K.O. Tamadonfar, N.S. Omattage, C.N. Spaulding, S.J. Hultgren, Reaching the end of the line: urinary tract infections. Microbiol. Spectr. 7(May), (2019) https://doi.org/10.1128/microbiolspec.BAI-0014-2019
  38. H. Alhabeeb, S. Baradwan, H. Kord-Varkaneh et al. Association between body mass index and urinary tract infection: a systematic review and meta-analysis of observational cohort studies. Eat. Weight Disord. 26(Oct), 2117–2125 (2021). https://doi.org/10.1007/s40519-020-01101-4 [DOI: 10.1007/s40519-020-01101-4]
  39. D.W. Haslam, W.P. James, Obesity. Lancet 366(9492), 1197–1209 (2005). https://doi.org/10.1016/S0140-6736(05)67483-1 [DOI: 10.1016/S0140-6736(05)67483-1]
  40. A.L. Bahl, R.N. Chugh, K.B. Sharma, Asymptomatic bacteriuria in diabetics attending a diabetic clinic. Indian J. Med. Sci. 24(Jan), 1–6 (1970) [PMID: 4912511]
  41. L.M. Muller, K.J. Gorter, E. Hak et al. Increased risk of common infections in patients with type 1 and type 2 diabetes mellitus. Clin. Infect. Dis. 41(Aug), 281–288 (2005). https://doi.org/10.1086/431587 [DOI: 10.1086/431587]
  42. C. Weykamp, HbA1c: a review of analytical and clinical aspects. Ann. Lab. Med. 33(Nov), 393–400 (2013). https://doi.org/10.3343/alm.2013.33.6.393 [DOI: 10.3343/alm.2013.33.6.393]
  43. Z.A. Yaseen Al-Khayat, N.E. Waheda, N.F. Shaker, The prevalence of positive serum anticardiolipin antibodies and asymptomatic bacteriuria in women with recurrent abortions. Eurasia. J. Med. 45(Feb), 39–42 (2013). https://doi.org/10.5152/eajm.2013.06 [DOI: 10.5152/eajm.2013.06]
  44. H. Sharbatdaralaei, M.R. Asadi Karam, K. Ahmadi, M. Habibi, Bioinformatics analyses for the designation of a hybrid protein against urinary tract infections caused by Pseudomonas aeruginosa and investigation of the presence of pre-existing antibodies in infected humans. J. Biomol. Struct. Dyn. 40(19), 9081–9095 (2022). https://doi.org/10.1080/07391102.2021.1924264 [DOI: 10.1080/07391102.2021.1924264]
  45. C. Qi, X. Mao, Z. Zhang, H. Wu, Classification and differential diagnosis of diabetic nephropathy. J. Diabetes Res. 2017, 8637138 (2017) [DOI: 10.1155/2017/8637138]
  46. A. Orieux, A. Bouchet, A. Doreille et al. Predictive factors of glomerular filtration rate loss associated with living kidney donation: a single-center retrospective study. World J. Urol. 40(Sep), 2161–2168 (2022). https://doi.org/10.1007/s00345-022-04019-x [DOI: 10.1007/s00345-022-04019-x]
  47. L. Yang, Diagnostic value of urine glucose, urinary microalbumin, retinol binding protein and serum cystatin C in patients with early diabetic renal injury. Med. J. Chin. People’s Health 30(04), 111–126 (2018). https://doi.org/10.3969/j.issn.1672-0369.2018.04.054. [DOI: 10.3969/j.issn.1672-0369.2018.04.054.]
  48. Z. Jiale, S. Weiwei, Zhezhe et al. Distribution and influencing factors of estimated glomerular filtration rate in 1480 patients with type 2 diabetes mellitus %J World. J. Integr. Tradit. West. Med. 18(01), 142–147+152 (2023). https://doi.org/10.13935/j.cnki.sjzx.230124 [DOI: 10.13935/j.cnki.sjzx.230124]
  49. M.T. Bayram, D. Alaygut, Y. Oztürk et al. Asymptomatic proteinuria in a child with recurrent urinary tract infections-questions. Pediatr. Nephrol. 27(May), 761–762 (2012). https://doi.org/10.1007/s00467-011-1986-7 . 763-764 [DOI: 10.1007/s00467-011-1986-7]
  50. J. Karalliedde, G. Viberti, Proteinuria in diabetes: bystander or pathway to cardiorenal disease? J. Am. Soc. Nephrol. 21(Dec), 2020–2027 (2010). https://doi.org/10.1681/ASN.2010030250 [DOI: 10.1681/ASN.2010030250]
  51. S.N. Heyman, I. Raz, J.P. Dwyer, R. Weinberg Sibony, J.B. Lewis, Z. Abassi, Diabetic proteinuria revisited: updated physiologic perspectives. Cells 11(Sep), (2022) https://doi.org/10.3390/cells11182917
  52. M.S. Madhur, F. Elijovich, M.R. Alexander et al. Hypertension: do inflammation and immunity hold the key to solving this epidemic? Circ. Res. 128(Apr), 908–933 (2021). https://doi.org/10.1161/CIRCRESAHA.121.318052 [DOI: 10.1161/CIRCRESAHA.121.318052]
  53. M.T. Villarreal-Molina, B. Antuna-Puente, Adiponectin: anti-inflammatory and cardioprotective effects. Biochimie 94(Oct), 2143–2149 (2012). https://doi.org/10.1016/j.biochi.2012.06.030 [DOI: 10.1016/j.biochi.2012.06.030]
  54. Y. Arita, S. Kihara, N. Ouchi et al. Paradoxical decrease of an adipose-specific protein, adiponectin, in obesity. Biochem. Biophys. Res. Commun. 257(Apr), 79–83 (1999). https://doi.org/10.1006/bbrc.1999.0255 [DOI: 10.1006/bbrc.1999.0255]
  55. T. Kadowaki, T. Yamauchi, N. Kubota, K. Hara, K. Ueki, K. Tobe, Adiponectin and adiponectin receptors in insulin resistance, diabetes, and the metabolic syndrome. J. Clin. Invest. 116(Jul), 1784–1792 (2006). https://doi.org/10.1172/JCI29126 [DOI: 10.1172/JCI29126]
  56. L. Tian, N. Luo, X. Zhu, B.H. Chung, W.T. Garvey, Y. Fu, Adiponectin-AdipoR1/2-APPL1 signaling axis suppresses human foam cell formation: differential ability of AdipoR1 and AdipoR2 to regulate inflammatory cytokine responses. Atherosclerosis 221(Mar), 66–75 (2012). https://doi.org/10.1016/j.atherosclerosis.2011.12.014 [DOI: 10.1016/j.atherosclerosis.2011.12.014]
  57. K. Hara, M. Horikoshi, T. Yamauchi et al. Measurement of the high-molecular weight form of adiponectin in plasma is useful for the prediction of insulin resistance and metabolic syndrome. Diabetes Care 29(Jun), 1357–1362 (2006). https://doi.org/10.2337/dc05-1801 [DOI: 10.2337/dc05-1801]
  58. L.E. Nicolle, S. Bradley, R. Colgan, J.C. Rice, A. Schaeffer, T.M. Hooton, Infectious Diseases Society of America guidelines for the diagnosis and treatment of asymptomatic bacteriuria in adults. Clin. Infect. Dis. 40(Mar), 643–654 (2005). https://doi.org/10.1086/427507 [DOI: 10.1086/427507]

MeSH Term

Humans
Female
Bacteriuria
Diabetes Mellitus, Type 2
Incidence
Glycated Hemoglobin
Risk Factors
Urinary Tract Infections
Proteinuria
Hyperlipidemias
Hypertension

Chemicals

Glycated Hemoglobin

Word Cloud

Created with Highcharts 10.0.0T2DM95%CIASBpatients00112P < 0riskfactorsmeta-analysis0diabetes7%OR = 1typeurinarytractasymptomaticbacteriuriaincidenceI = 0%prevalenceinfectionUTIresearchprovidepreventingtimearticles5performedincluded23184femalesex43I = 62hypertensionhyperlipidemiaproteinuriaIncidenceBACKGROUND:mellitusincreasingyearbecomeoneprominenthealthconcernsworldwidePatientsproneinfectiousdiseasesinfectionsalsowidespreadDespitecomprehensiveunderstandinglackregardingprimarypreventionstrategiesOBJECTIVE:clarifyevidenceHelpfamiliescaregiversidentifyintervenereduceFillgapsexistingSTUDYDESIGN:Meta-analysesconductedlinePRISMAguidelinesMETHODS:ElevendatabasessystematicallysearchedretrievalselectedestablishmentdatabaseFebruary2023LiteraturescreeningqualityevaluationindependentlytworesearchersaccordinginclusionexclusioncriteriausingStata17RESULTS:Fourteenincludingcohortcase-controlstudies4044183291controllingconfoundingvariablesfollowingassociatedT2DM:ageWMD = 39145I = 755%070212I = 793%P = 0002durationWMD = 25453I = 80HbA1cWMD = 063846%592404<06627Neuropathy813837OR = 3008295CONCLUSION:overallAgecourseHbA1Cneuropathyidentifiedrelatedfindingscanrobusttheoreticalbasismanagingmellitus:AsymptomaticMeta-analysisRiskfactorType

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