Skip to main content

Advertisement

Log in

The impact of diabetes on tuberculosis treatment outcomes: evidence based on a cumulative meta-analysis

  • Review Article
  • Published:
International Journal of Diabetes in Developing Countries Aims and scope Submit manuscript

Abstract

Diabetes mellitus (DM) is a known risk factor for tuberculosis (TB). It is also associated with worse tuberculosis treatment outcomes. This study aimed to perform a systematic review and meta-analysis to quantitatively summarize evidence for the impact of diabetes on tuberculosis outcomes. We searched PubMed, Cochrane, and Web of Science from January 1980 to July 2015. The combinations of key words used were (((((“Tuberculosis”[Mesh]) OR (Tuberculosis OR pulmonary tuberculosis OR TB))) AND ((“Diabetes Mellitus”[Mesh]) OR (Diabetes Mellitus OR Diabetes OR DM))) AND (Outcome OR sequelae OR treatment OR therapy OR culture conversion OR failure OR death OR relapse OR recurrence)). We reviewed the full text of 70 papers and included 54 studies of which 16 reported culture conversion at 2 to 3 months, 24 reported the combined outcome of failure and death, 34 reported death, 8 reported relapse, and 7 reported drug-resistant recurrent tuberculosis. Patients with diabetes have an odds ratio (OR) through this cumulative meta-analysis for the combined outcome of failure and death of 1.96 (95 % CI, 1.64 to 2.33). The OR of death during tuberculosis treatment among the 34 unadjusted studies is 1.83 (95 % CI, 1.61 to 2.07). Diabetes is also associated with an increased risk of relapse (OR, 1.97; 95 % CI, 1.42 to 2.74). The OR for studies assessing sputum culture conversion after 2 to 3 months of tuberculosis therapy is 1.71 (95 % CI, 1.50 to 1.94). Diabetes increases the risk of failure and death combined, death, and relapse among patients with tuberculosis. This study highlights a need for increased attention to treatment of tuberculosis in people with diabetes, which may include testing for suspected diabetes, improving glucose control, and increasing clinical and therapeutic monitoring.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7
Fig. 8
Fig. 9
Fig. 10
Fig. 11
Fig. 12
Fig. 13
Fig. 14
Fig. 15
Fig. 16
Fig. 17
Fig. 18
Fig. 19
Fig. 20
Fig. 21

Similar content being viewed by others

References

  1. Suleiman, S.A.S., et al., Role of diabetes in the prognosis and therapeutic outcome of tuberculosis. Int J Endocrinol, 2012.

    Google Scholar 

  2. World Health Organization (2007) Tuberculosis fact sheet. Fact Sheet No. 104. Available: http://www.who.int/mediacentre/factsheets/fs104/en/print.html. Accessed 25 Sept 2007

  3. Sullivan T, Ben Amor Y. The co-management of tuberculosis and diabetes: challenges and opportunities in the developing world. PLoS Med. 2012;9(7):e1001269.

    Article  PubMed  PubMed Central  Google Scholar 

  4. van Crevel R, Dockrell HM. TANDEM: understanding diabetes and tuberculosis. Lancet Diabetes Endocrinol. 2014;2(4):270–2.

    Article  PubMed  Google Scholar 

  5. Ruslami R, Aarnoutse RE, Alisjahbana B, et al. Implications of the global increase of diabetes for tuberculosis control and patient care. Tropical Med Int Health. 2010;15:1289–99.

    Article  Google Scholar 

  6. Stevenson CR, Critchley JA, Forouhi NG, Roglic G, Williams BG, et al. Diabetes and the risk of tuberculosis: a neglected threat to public health. Chronic Illn. 2007;3:228–45.

    Article  PubMed  Google Scholar 

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

    Article  PubMed  PubMed Central  Google Scholar 

  8. World Health Organization. Treatment of tuberculosis. Guidelines for National Programmmes. Geneva, Switzerland. 2010 [http://whqlibdoc.who.int/hq/2003/WHO_CDS_TB_2003.313_eng.pdf], WHO/CDS/TB 2003.313.

  9. World Health Organization. Treatment of tuberculosis guidelines fourth edition. Geneva, Switzerland. 2010 [http://whqlibdoc.who.int/publications/2010/9789241547833_eng.pdf], WHO/HTM/TB/2009.402.

  10. World Health Organization: Definition and diagnosis of diabetes mellitus and intermediate hyperglycemia. Geneva: WHO; 2010 [http://www.who.int/diabetes/publications/Definition%20and%20diagnosis%20of%20diabetes_new.pdf].

    Google Scholar 

  11. The Expert Committee on the Diagnosis and Classification of Diabetes Mellitus. Report of the expert committee on the diagnosis and classification of diabetes mellitus. Diabetes Care. 1997;20:1183–97.

    Article  Google Scholar 

  12. Bashar M, Alcabes P, Rom WN, Condos R. Increased incidence of multidrug-resistant tuberculosis in diabetic patients on the Bellevue chest service, 1987 to 1997. Chest. 2001;120:1514–9.

    Article  CAS  PubMed  Google Scholar 

  13. Centis R, Migliori GB. Evaluation of tuberculosis treatment results in Italy, report 1999. Monaldi Arch Chest Dis. 2002;57:297–305.

    CAS  PubMed  Google Scholar 

  14. Subhash HS, Ashwin I, Mukundan U, Danda D, John G, Cherian AM, Thomas K. Drug resistant tuberculosis in diabetes mellitus: a retrospective study from South India. Trop Dr. 2003;33:154–6.

    CAS  Google Scholar 

  15. Singla R, Khan N, Al-Sharif N, Ai-Sayegh MO, Shaikh MA, Osman MM. Influence of diabetes on manifestations and treatment outcome of pulmonary TB patients. Int J Tuberc Lung Dis. 2006;10:74–9.

    CAS  PubMed  Google Scholar 

  16. Banu Rekha VV, Balasubramanian R, Swaminathan S, Ramachandran R, Rahman F, Sundaram V, Thyagarajan K, Selvakumar N, Adhilakshmi AR, Iliayas S, Narayanan PR. Sputum conversion at the end of intensive phase of category-1 regimen in the treatment of pulmonary tuberculosis patients with diabetes mellitus or HIV infection: an analysis of risk factors. Indian J Med Res. 2007;126:452–8.

    CAS  PubMed  Google Scholar 

  17. Alisjahbana B, Sahiratmadja E, Nelwan EJ, Purwa AM, Ahmad Y, Ottenhoff TH, Nelwan RH, Parwati I, van der Meer JW, van Crevel R. The effect of type 2 diabetes mellitus on the presentation and treatment response of pulmonary tuberculosis. Clin Infect Dis. 2007;45:428–35.

    Article  PubMed  Google Scholar 

  18. Fisher-Hoch SP, Whitney E, McCormick JB, Crespo G, Smith B, Rahbar MH, Restrepo BI. Nuevo Santander tuberculosis trackers: type 2 diabetes and multidrug-resistant tuberculosis. Scand J Infect Dis. 2008;40:888–93.

    Article  PubMed  PubMed Central  Google Scholar 

  19. Dooley KE, Tang T, Golub JE, Dorman SE, Cronin W. Impact of diabetes mellitus on treatment outcomes of patients with active tuberculosis. AmJTrop Med Hyg. 2009;80:634–9.

    Google Scholar 

  20. Wang CS, Yang CJ, Chen HC, Chuang SH, Chong IW, Hwang JJ, Huang MS. Impact of type 2 diabetes on manifestations and treatment outcome of pulmonary tuberculosis. Epidemiol Infect. 2009;137:203–10.

    Article  CAS  PubMed  Google Scholar 

  21. Zhang Q, Xiao H, Sugawara I. Tuberculosis complicated by diabetes mellitus at Shanghai Pulmonary Hospital, China. Jpn J Infect Dis. 62:390–1.

  22. Tatar D, Senol G, Alptekin S, Karakurum C, Aydin M, Coskunol I. Tuberculosis in diabetics: features in an endemic area. Jpn J Infect Dis. 62:423–7.

  23. Chiang CY, Lee JJ, Yu MC, Enarson DA, Lin TP, Luh KT. Tuberculosis outcomes in Taipei: factors associated with treatment interruption for 2 months and death. Int J Tuberc Lung Dis. 2009;13:105–11.

    PubMed  Google Scholar 

  24. Chang J-T et al. Effect of type 2 diabetes mellitus on the clinical severity and treatment outcome in patients with pulmonary tuberculosis: a potential role in the emergence of multidrug-resistance. J Formos Med Assoc. 2011;110(6):372–81.

    Article  PubMed  Google Scholar 

  25. Franke MF et al. Aggressive regimens for multidrug-resistant tuberculosis reduce recurrence. Clin Infect Dis. 2013;56(6):770–6.

    Article  CAS  PubMed  Google Scholar 

  26. Eugenia Jimenez-Corona M et al. Association of diabetes and tuberculosis: impact on treatment and post-treatment outcomes. Thorax. 2013;68(3):214–20.

    Article  Google Scholar 

  27. Faurholt-Jepsen D et al. Diabetes is a strong predictor of mortality during tuberculosis treatment: a prospective cohort study among tuberculosis patients from Mwanza, Tanzania. Tropical Med Int Health. 2013;18(7):822–9.

    Article  Google Scholar 

  28. Mi F et al. Diabetes mellitus and tuberculosis: pattern of tuberculosis, two-month smear conversion and treatment outcomes in Guangzhou, China. Tropical Med Int Health. 2013;18(11):1379–85.

    Article  Google Scholar 

  29. Duangrithi D et al. Impact of diabetes mellitus on clinical parameters and treatment outcomes of newly diagnosed pulmonary tuberculosis patients in Thailand. Int J Clin Pract. 2013;67(11):1199–209.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  30. Sulaiman SAS et al. Impact of diabetes mellitus on treatment outcomes of tuberculosis patients in tertiary care setup. Am J Med Sci. 2013;345(4):321–5.

    Article  PubMed  Google Scholar 

  31. Kang YA et al. Impact of diabetes on treatment outcomes and long-term survival in multidrug-resistant tuberculosis. Respiration. 2013;86(6):472–8.

    Article  CAS  PubMed  Google Scholar 

  32. K VN et al. Outcome of tuberculosis treatment in patients with diabetes mellitus treated in the revised national tuberculosis control programme in Malappuram District, Kerala, India. PLoS One. 2013;8(10):e76275.

    Article  Google Scholar 

  33. Reis-Santos B et al. Socio-demographic and clinical differences in subjects with tuberculosis with and without diabetes mellitus in Brazil—a multivariate analysis. PLoS One. 2013;8(4):e62604.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  34. Magee MJ et al. Diabetes mellitus and risk of all-cause mortality among patients with tuberculosis in the state of Georgia, 2009–2012. Ann Epidemiol. 2014;24(5):369–75.

    Article  PubMed  PubMed Central  Google Scholar 

  35. Magee MJ et al. Diabetes mellitus, smoking status, and rate of sputum culture conversion in patients with multidrug-resistant tuberculosis: a cohort study from the country of Georgia. PLoS One. 2014;9(4):e94890.

    Article  PubMed  PubMed Central  Google Scholar 

  36. Viswanathan V et al. Effect of diabetes on treatment outcome of smear-positive pulmonary tuberculosis—a report from South India. J Diabetes Complicat. 2014;28(2):162–5.

    Article  PubMed  Google Scholar 

  37. Viswanathan AA, Gawde NC. Effect of type II diabetes mellitus on treatment outcomes of tuberculosis. Lung India. 2014;31(3):244–8.

    Article  PubMed  PubMed Central  Google Scholar 

  38. Cavanaugh J et al. Effect of diabetes on tuberculosis presentation and outcomes in Kiribati. Tropical Med Int Health. 2015;20(5):643–9.

    Article  CAS  Google Scholar 

  39. Chiang CY et al. The influence of diabetes, glycemic control, and diabetes-related comorbidities on pulmonary tuberculosis. PLoS One. 2015;10(3):e0121698.

    Article  PubMed  PubMed Central  Google Scholar 

  40. Delgado-Sanchez, G., et al. Association of pulmonary tuberculosis and diabetes in Mexico: analysis of the national tuberculosis registry 2000–2012. PLoS One. 2015;10(6).

  41. Behnaz F, Mohammadzadeh M, Mohammadzade G. Five-year assessment of time of sputum smears conversion and outcome and risk factors of tuberculosis patients in Central Iran. Tuberc Res Treat. 2015;2015:609083.

    PubMed  PubMed Central  Google Scholar 

  42. Restrepo BI et al. Type 2 diabetes and tuberculosis in a dynamic bi-national border population. Epidemiol Infect. 2007;135(3):483–91.

    Article  CAS  PubMed  Google Scholar 

  43. Hongguang C et al. Impact of diabetes on clinical presentation and treatment outcome of pulmonary tuberculosis in Beijing. Epidemiol Infect. 2015;143(1):150–6.

    Article  CAS  PubMed  Google Scholar 

  44. Viswanathan V et al. Prevalence of diabetes and pre-diabetes and associated risk factors among tuberculosis patients in India. PLoS One. 2012;7(7):e41367.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  45. Ambrosetti M, Besozzi G, Codecasa LR, Farris B, Nutini S, Saini L, Casali L, Nardini S, Migliori GB. The Italian AIPO study on tuberculosis treatment results, report 1995 national AIPO “tuberculosis” study group. Monaldi Arch Chest Dis. 1999(54):49–54.

  46. Ambrosetti M, Besozzi G, Farris B, Nutini S, Saini L, Casali L, Pretto P, Orani G, Calabro S, Migliori GB. The Italian AIPO study on tuberculosis treatment results, report 1996. National AIPO “tuberculosis” study group. Associazione Italiana Pneumologi Ospedalieri. Monaldi Arch Chest Dis. 1999(54):237–41.

  47. Ambrosetti M, Besozzi G, Codecasa LR, Farris B, Nutini S, Saini L, Casali L, Nardini S, Migliori GB. The Italian AIPO study on tuberculosis treatment results, report 1997. National AIPO “tuberculosis” study group. Monaldi Arch Chest Dis. 1999(54):407–12.

  48. Anunnatsiri S, Chetchotisakd P, Wanke C. Factors associated with treatment outcomes in pulmonary tuberculosis in northeastern Thailand. Southeast Asian J Trop Med Public Health. 2005;36:324–30.

    PubMed  Google Scholar 

  49. Blanco JAG, Toste IS, Fernandez ML, Morales RG, Alvarez RF, Cuadrado GR, Gonzalvez AM, Martin IJG. Tobacco smoking and sputum smear conversion in pulmonary tuberculosis. Med Clin. 2007;128:565–8.

    Article  Google Scholar 

  50. Centis R, Ianni A, Migliori GB. Evaluation of tuberculosis treatment results in Italy, report 1998. Tuberculosis section of the National AIPO Study Group on Infectious Disease and the SMIRA Group. Monaldi Arch Chest Dis. 2000(55):293–8.

  51. Fielder JF, Chaulk CP, Dalvi M, Gachuhi R, Comstock GW, Sterling TR. A high tuberculosis case-fatality rate in a setting of effective tuberculosis control: implications for acceptable treatment success rates. Int J Tuberc Lung Dis. 2002;6:1114–7.

    CAS  PubMed  Google Scholar 

  52. Guler M, Unsal E, Dursun B, Aydln O, Capan N. Factors influencing sputum smear and culture conversion time among patients with new case pulmonary tuberculosis. Int J Clin Pract. 2007;61:231–5.

    Article  CAS  PubMed  Google Scholar 

  53. Hara H. From the aspects of complicated diseases. Kekkaku. 1996;71:47–56.

    CAS  PubMed  Google Scholar 

  54. Hasibi M, Rasoulinejad M, Hosseini SM, Davari P, Sahebian A, Khashayar P. Epidemiological, clinical, laboratory findings, and outcomes of disseminated tuberculosis in Tehran, Iran. South Med J. 2008;101:910–3.

    Article  PubMed  Google Scholar 

  55. Ito K, Wada M, Yoshiyama T, Ohmori M, Ogata H. Drug resistance in recurrent cases of tuberculosis. Kekkaku. 2004;79:461–7.

    PubMed  Google Scholar 

  56. Kitahara Y, Ikeda A, Kajiki A, Maruyama M, Harada S, Harada Y, Takamoto M, Ishibashi T. An investigation on risk factors relating to the treatment difficulty in originally treated pulmonary tuberculosis cases. Kekkaku. 1994;69:503–11.

    CAS  PubMed  Google Scholar 

  57. Kourbatova EV, Borodulin BE, Borodulina EA, del Rio C, Blumberg HM, Leonard Jr MK. Risk factors for mortality among adult patients with newly diagnosed tuberculosis in Samara, Russia. Int J Tuberc Lung Dis. 2006;10:1224–30.

    CAS  PubMed  Google Scholar 

  58. Maalej S, Belhaoui N, Bourguiba M, Mahouachi R, Chtourou A, Taktak S, Fennira H, Slim L, Kheder AB, Drira I. Pulmonary tuberculosis and diabetes. A retrospective study of 60 patients in Tunisia. Presse Med. 2009;38:20–4.

    Article  PubMed  Google Scholar 

  59. Mboussa J, Monabeka H, Kombo M, Yokolo D, Yoka-Mbio A, Yala F. Course of pulmonary tuberculosis in diabetics. Rev Pneumol Clin. 2003;59:39–44.

    CAS  PubMed  Google Scholar 

  60. Oursler KK, Moore RD, Bishai WR, Harrington SM, Pope DS, Chaisson RE. Survival of patients with pulmonary tuberculosis: clinical and molecular epidemiologic factors. Clin Infect Dis. 2002;34:752–9.

    Article  PubMed  Google Scholar 

  61. Pina JM, Dominguez A, Alcaide J, Alvarez J, Camps N, Diez M, Godoy P, Jansá JM, Minquell S, Arias C. Excess mortality due to tuberculosis and factors associated to death in and annual cohort of patients diagnosed of tuberculosis. Rev Clin Esp. 2006;206:560–5.

    Article  CAS  PubMed  Google Scholar 

  62. Ponce-De-Leon A, Garcia-Garcia Md Mde, L, Garcia-Sancho, MC, Gomez-Perez, FJ, Valdespino-Gomez, JL, Olaiz-Fernandez, G, Rojas, R, Ferreyra-Reyes, L, Cano-Arellano, B, Bobadilla, M, Small, PM, Sifuentes-Osornio, J: Tuberculosis and diabetes in southern Mexico. Diabetes Care 2004, 27:1584–1590.

  63. Vasankari T, Holmstrom P, Ollgren J, Liippo K, Kokki M, Ruutu P. Risk factors for poor tuberculosis treatment outcome in Finland: a cohort study. BMC Public Health. 2007;7:291.

    Article  PubMed  PubMed Central  Google Scholar 

  64. Wada M. The effectiveness of pyrazinamide-containing six-month short course chemotherapy. Kekkaku. 2000;75:665–73.

    CAS  PubMed  Google Scholar 

  65. Wang PD, Lin RS. Drug-resistant tuberculosis in Taipei, 1996–1999. Am J Infect Control. 2001;29:41–7.

    Article  CAS  PubMed  Google Scholar 

  66. Dixon B. Diabetes and tuberculosis: an unhealthy partnership. Lancet Infect Dis. 2007;7(7):444.

    Article  PubMed  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Qiuzhen Wang.

Ethics declarations

Source of support

The study was funded by the National Natural Science Foundation of China (81472983).

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Han, X., Wang, Q., Wang, Y. et al. The impact of diabetes on tuberculosis treatment outcomes: evidence based on a cumulative meta-analysis. Int J Diabetes Dev Ctries 36, 490–507 (2016). https://doi.org/10.1007/s13410-016-0514-5

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s13410-016-0514-5

Keywords

Navigation