Tuberculosis and diabetes mellitus: convergence of two epidemics

The Lancet Infectious Diseases

Volumn 9, Issue 12, 2009, Pages 737-746

  Dooley, Kelly E ^a   Chaisson, Richard E ^a  

^a JOHNS HOPKINS UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

2,4 THIAZOLIDINEDIONE DERIVATIVE; GLIBENCLAMIDE; GLIPIZIDE; INSULIN; ISONIAZID; NATEGLINIDE; PIOGLITAZONE; PYRIDOXINE; REPAGLINIDE; RIFAMPICIN; ROSIGLITAZONE; SULFONYLUREA;

AREA UNDER THE CURVE; CLINICAL FEATURE; CULTURAL ANTHROPOLOGY; DEVELOPED COUNTRY; DEVELOPING COUNTRY; DIABETES CONTROL; DIABETES MELLITUS; DISEASE ASSOCIATION; DISEASE SEVERITY; DRUG METABOLISM; EPIDEMIC; EVIDENCE BASED MEDICINE; GLUCOSE INTOLERANCE; GLUCOSE TOLERANCE; GLYCEMIC CONTROL; HEALTH CARE COST; HUMAN; HYPERGLYCEMIA; HYPERINSULINEMIA; INCIDENCE; INSULIN DEPENDENT DIABETES MELLITUS; MYCOBACTERIUM TUBERCULOSIS; NON INSULIN DEPENDENT DIABETES MELLITUS; NONHUMAN; OUTCOME ASSESSMENT; PRIORITY JOURNAL; RADIODIAGNOSIS; REVIEW; RISK FACTOR; THORAX RADIOGRAPHY; TREATMENT FAILURE; TREATMENT RESPONSE; TUBERCULOSIS;

ANTI-BACTERIAL AGENTS; DIABETES COMPLICATIONS; DISEASE OUTBREAKS; FEMALE; HUMANS; HYPOGLYCEMIC AGENTS; MALE; PREVALENCE; TUBERCULOSIS; WORLD HEALTH;

EID: 71549126811     PISSN: 14733099     EISSN: None     Source Type: Journal    
DOI: 10.1016/S1473-3099(09)70282-8     Document Type: Review

References (105)

1. Rajalakshmi S., and Veluchamy G. Yugi's pramegam and diebetes mellitus: an analogue. Bull Indian Inst Hist Med Hyderabad 29 (1999) 83-87
2. Hu F.B., Manson J.E., Stampfer M.J., et al. Diet, lifestyle, and the risk of type 2 diabetes mellitus in women. N Engl J Med 345 (2001) 790-797
3. van Dam R.M., Rimm E.B., Willett W.C., Stampfer M.J., and Hu F.B. Dietary patterns and risk for type 2 diabetes mellitus in U.S. men. Ann Intern Med 136 (2002) 201-209
4. Popkin B.M. Will China's nutrition transition overwhelm its health care system and slow economic growth?. Health Aff (Millwood) 27 (2008) 1064-1076
5. Mozaffarian D., Kamineni A., Carnethon M., Djousse L., Mukamal K.J., and Siscovick D. Lifestyle risk factors and new-onset diabetes mellitus in older adults: the cardiovascular health study. Arch Intern Med 169 (2009) 798-807
6. Stevenson C.R., Critchley J.A., Forouhi N.G., et al. Diabetes and the risk of tuberculosis: a neglected threat to public health?. Chronic Illn 3 (2007) 228-245
7. Harries A.D., Billo N., and Kapur A. Links between diabetes mellitus and tuberculosis: should we integrate screening and care?. Trans R Soc Trop Med Hyg 103 (2009) 1-2
8. Leung C.C., Lam T.H., Chan W.M., et al. Lower risk of tuberculosis in obesity. Arch Intern Med 167 (2007) 1297-1304
9. Boutayeb A. The double burden of communicable and non-communicable diseases in developing countries. Trans R Soc Trop Med Hyg 100 (2006) 191-199
10. International Diabetes Foundation. Diabetes atlas. 4th edn. (2009), International Diabetes Foundation, Brussels
11. WHO. WHO report 2009: Global tuberculosis control-annex 3: the Stop TB Strategy, case reports, treatment outcomes and estimates of TB burden. http://www.who.int/tb/publications/global_report/2009/annex_3/en/ (accessed Oct 25, 2009).
12. Wild S., Roglic G., Green A., Sicree R., and King H. Global prevalence of diabetes: estimates for the year 2000 and projections for 2030. Diabetes Care 27 (2004) 1047-1053
13. King H., Aubert R.E., and Herman W.H. Global burden of diabetes, 1995-2025: prevalence, numerical estimates, and projections. Diabetes Care 21 (1998) 1414-1431
14. Kirigia J.M., Sambo H.B., Sambo L.G., and Barry S.P. Economic burden of diabetes mellitus in the WHO African region. BMC Int Health Hum Rights 9 (2009) 6
15. Mendis S., Fukino K., Cameron A., et al. The availability and affordability of selected essential medicines for chronic diseases in six low- and middle-income countries. Bull World Health Organ 85 (2007) 279-288
16. Sidibe E.H. Main complications of diabetes mellitus in Africa. Ann Med Interne (Paris) 151 (2000) 624-628
17. Lopez A.D., Mathers C.D., Ezzati M., Jamison D.T., and Murray C.J. Global and regional burden of disease and risk factors, 2001: systematic analysis of population health data. Lancet 367 (2006) 1747-1757
18. Keshavjee S., Gelmanova I.Y., Pasechnikov A.D., et al. Treating multidrug-resistant tuberculosis in Tomsk, Russia: developing programs that address the linkage between poverty and disease. Ann NY Acad Sci 1136 (2008) 1-11
19. Stevenson C.R., Forouhi N.G., Roglic G., et al. Diabetes and tuberculosis: the impact of the diabetes epidemic on tuberculosis incidence. BMC Public Health 7 (2007) 234
20. Dooley K.E., Tang T., Golub J.E., Dorman S.E., and Cronin W. Impact of diabetes mellitus on treatment outcomes of patients with active tuberculosis. Am J Trop Med Hyg 80 (2009) 634-639
21. Lindoso A.A., Waldman E.A., Komatsu N.K., Figueiredo S.M., Taniguchi M., and Rodrigues L.C. Profile of tuberculosis patients progressing to death, city of Sao Paulo, Brazil, 2002. Rev Saude Publica 42 (2008) 805-812
22. Restrepo B.I., Fisher-Hoch S.P., Crespo J.G., et al. Type 2 diabetes and tuberculosis in a dynamic bi-national border population. Epidemiol Infect 135 (2007) 483-491
23. Barach J. Historical facts in diabetes mellitus. Ann Med Hist 10 (1928) 387
24. Root H. The association of diabetes and tuberculosis. N Engl J Med 210 (1934) 1 78,127.
25. Boucot K.R., Dillon E.S., Cooper D.A., Meier P., and Richardson R. Tuberculosis among diabetics: the Philadelphia survey. Am Rev Tuberc 65 (1952) 1-50
26. Bermejo M., Gil S., Velasco M., Prado A., Garcia C., and Guijarro M. Tuberculin test in diabetic patients in a health center. Aten Primaria 16 (1995) 154-157
27. Mboussa J., Monabeka H., Kombo M., Yokolo D., Yoka-Mbio A., and Yala F. Course of pulmonary tuberculosis in diabetics. Rev Pneumol Clin 59 (2003) 39-44
28. Shetty N., Shemko M., Vaz M., and D'Souza G. An epidemiological evaluation of risk factors for tuberculosis in South India: a matched case control study. Int J Tuberc Lung Dis 10 (2006) 80-86
29. Coker R., McKee M., Atun R., et al. Risk factors for pulmonary tuberculosis in Russia: case-control study. BMJ 332 (2006) 85-87
30. Jabbar A., Hussain S.F., and Khan A.A. Clinical characteristics of pulmonary tuberculosis in adult Pakistani patients with co-existing diabetes mellitus. East Mediterr Health J 12 (2006) 522-527
31. Olmos P., Donoso J., Rojas N., et al. Tuberculosis and diabetes mellitus: a longitudinal-retrospective study in a teaching hospital. Rev Med Chil 117 (1989) 979-983
32. Swai A.B., McLarty D.G., and Mugusi F. Tuberculosis in diabetic patients in Tanzania. Trop Doct 20 (1990) 147-150
33. Kim S.J., Hong Y.P., Lew W.J., Yang S.C., and Lee E.G. Incidence of pulmonary tuberculosis among diabetics. Tuber Lung Dis 76 (1995) 529-533
34. Pablos-Mendez A., Blustein J., and Knirsch C.A. The role of diabetes mellitus in the higher prevalence of tuberculosis among Hispanics. Am J Public Health 87 (1997) 574-579
35. Shah B.R., and Hux J.E. Quantifying the risk of infectious diseases for people with diabetes. Diabetes Care 26 (2003) 510-513
36. Ponce-De-León A., García-García M.L., García-Sancho M.C., et al. Tuberculosis and diabetes in southern Mexico. Diabetes Care 27 (2004) 1584-1590
37. Jick S.S., Lieberman E.S., Rahman M.U., and Choi H.K. Glucocorticoid use, other associated factors, and the risk of tuberculosis. Arthritis Rheum 55 (2006) 19-26
38. Perez A., Brown III H.S., and Restrepo B.I. Association between tuberculosis and diabetes in the Mexican border and non-border regions of Texas. Am J Trop Med Hyg 74 (2006) 604-611
39. Dyck R.F., Klomp H., Marciniuk D.D., et al. The relationship between diabetes and tuberculosis in Saskatchewan: comparison of registered Indians and other Saskatchewan people. Can J Public Health 98 (2007) 55-59
40. Leung C.C., Lam T.H., Chan W.M., et al. Diabetic control and risk of tuberculosis: a cohort study. Am J Epidemiol 167 (2008) 1486-1494
41. Jeon C.Y., and Murray M.B. Diabetes mellitus increases the risk of active tuberculosis: a systematic review of 13 observational studies. PLoS Med 5 (2008) e152
42. Bashar M., Alcabes P., Rom W.N., and Condos R. Increased incidence of multidrug-resistant tuberculosis in diabetic patients on the Bellevue Chest Service, 1987 to 1997. Chest 120 (2001) 1514-1519
43. Fisher-Hoch S.P., Whitney E., McCormick J.B., et al. Type 2 diabetes and multidrug-resistant tuberculosis. Scand J Infect Dis 40 (2008) 888-893
44. Singla R., and Khan N. Does diabetes predispose to the development of multidrug-resistant tuberculosis?. Chest 123 (2003) 308-309
45. Subhash H.S., Ashwin I., Mukundan U., et al. Drug resistant tuberculosis in diabetes mellitus: a retrospective study from south India. Trop Doct 33 (2003) 154-156
46. Suárez-García I., Rodríguez-Blanco A., Vidal-Pérez J.L., et al. Risk factors for multidrug-resistant tuberculosis in a tuberculosis unit in Madrid, Spain. Eur J Clin Microbiol Infect Dis 28 (2009) 325-330
47. Tanrikulu A.C., Hosoglu S., Ozekinci T., Abakay A., and Gurkan F. Risk factors for drug resistant tuberculosis in southeast Turkey. Trop Doct 38 (2008) 91-93
48. Sosman M., and Steidl J. Diabetic tuberculosis. Am J Roentgenol 17 (1927) 625
49. Weaver R.A. Unusual radiographic presentation of pulmonary tuberculosis in diabetic patients. Am Rev Respir Dis 109 (1974) 162-163
50. Marais R.M. Diabetes mellitus in black and coloured tuberculosis patients. S Afr Med J 57 (1980) 483-484
51. Al-Tawfiq J.A., and Saadeh B.M. Radiographic manifestations of culture-positive pulmonary tuberculosis: cavitary or non-cavitary?. Int J Tuberc Lung Dis 13 (2009) 367-370
52. Segarra F., Sherman D.S., and Rodriguez-Aguero J. Lower lung field tuberculosis. Am Rev Respir Dis 87 (1963) 37-40
53. Hadlock F.P., Park S.K., Awe R.J., and Rivera M. Unusual radiographic findings in adult pulmonary tuberculosis. AJR Am J Roentgenol 134 (1980) 1015-1018
54. Ikezoe J., Takeuchi N., Johkoh T., et al. CT appearance of pulmonary tuberculosis in diabetic and immunocompromised patients: comparison with patients who had no underlying disease. AJR Am J Roentgenol 159 (1992) 1175-1179
55. Morris J.T., Seaworth B.J., and McAllister C.K. Pulmonary tuberculosis in diabetics. Chest 102 (1992) 539-541
56. Umut S., Tosun G.A., and Yildirim N. Radiographic location of pulmonary tuberculosis in diabetic patients. Chest 106 (1994) 326
57. Kuaban C., Fotsin J.G., Koulla-Shiro S., Ekono M.R., and Hagbe P. Lower lung field tuberculosis in Yaounde, Cameroon. Cent Afr J Med 42 (1996) 62-65
58. al-Wabel A.H., Teklu B., Mahfouz A.A., al-Ghamdi A.S., el-Amin O.B., and Khan A.S. Symptomatology and chest roentgenographic changes of pulmonary tuberculosis among diabetics. East Afr Med J 74 (1997) 62-64
59. Bacakoglu F., Basoglu O.K., Cok G., Sayiner A., and Ates M. Pulmonary tuberculosis in patients with diabetes mellitus. Respiration 68 (2001) 595-600
60. Perez-Guzman C., Torres-Cruz A., Villarreal-Velarde H., Salazar-Lezama M.A., and Vargas M.H. Atypical radiological images of pulmonary tuberculosis in 192 diabetic patients: a comparative study. Int J Tuberc Lung Dis 5 (2001) 455-461
61. Perez-Guzman C., Torres-Cruz A., Villarreal-Velarde H., and Vargas M.H. Progressive age-related changes in pulmonary tuberculosis images and the effect of diabetes. Am J Respir Crit Care Med 162 (2000) 1738-1740
62. Shaikh M.A., Singla R., Khan N.B., Sharif N.S., and Saigh M.O. Does diabetes alter the radiological presentation of pulmonary tuberculosis. Saudi Med J 24 (2003) 278-281
63. Wang J.Y., Lee L.N., and Hsueh P.R. Factors changing the manifestation of pulmonary tuberculosis. Int J Tuberc Lung Dis 9 (2005) 777-783
64. Wang C.S., Yang C.J., Chen H.C., et al. Impact of type 2 diabetes on manifestations and treatment outcome of pulmonary tuberculosis. Epidemiol Infect 137 (2009) 203-210
65. Hendy M., and Stableforth D. The effect of established diabetes mellitus on the presentation of infiltrative pulmonary tuberculosis in the immigrant Asian community of an inner city area of the United Kingdom. Br J Dis Chest 77 (1983) 87-90
66. Singla R., Khan N., Al-Sharif N., Ai-Sayegh M.O., Shaikh M.A., and Osman M.M. Influence of diabetes on manifestations and treatment outcome of pulmonary TB patients. Int J Tuberc Lung Dis 10 (2006) 74-79
67. Alisjahbana B., Sahiratmadja E., Nelwan E.J., et al. The effect of type 2 diabetes mellitus on the presentation and treatment response of pulmonary tuberculosis. Clin Infect Dis 45 (2007) 428-435
68. Rekha V.B., Balasubramanian R., Swaminathan S., et al. 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 126 (2007) 452-458
69. Guler M., Unsal E., Dursun B., Aydln O., and Capan N. Factors influencing sputum smear and culture conversion time among patients with new case pulmonary tuberculosis. Int J Clin Pract 61 (2007) 231-235
70. Restrepo B.I., Fisher-Hoch S.P., Smith B., et al. Mycobacterial clearance from sputum is delayed during the first phase of treatment in patients with diabetes. Am J Trop Med Hyg 79 (2008) 541-544
71. Maalej S., Belhaoui N., Bourguiba M., et al. Pulmonary tuberculosis and diabetes. A retrospective study of 60 patients in Tunisia. Presse Med 38 (2009) 20-24
72. Morsy A.M., Zaher H.H., Hassan M.H., and Shouman A. Predictors of treatment failure among tuberculosis patients under DOTS strategy in Egypt. East Mediterr Health J 9 (2003) 689-701
73. Oursler K.K., Moore R.D., Bishai W.R., Harrington S.M., Pope D.S., and Chaisson R.E. Survival of patients with pulmonary tuberculosis: clinical and molecular epidemiologic factors. Clin Infect Dis 34 (2002) 752-759
74. Bloomgarden Z.T. Inflammation and insulin resistance. Diabetes Care 26 (2003) 1922-1926
75. Moutschen M.P., Scheen A.J., and Lefebvre P.J. Impaired immune responses in diabetes mellitus: analysis of the factors and mechanisms involved. Relevance to the increased susceptibility of diabetic patients to specific infections. Diabetes Metab 18 (1992) 187-201
76. Saiki O., Negoro S., Tsuyuguchi I., and Yamamura Y. Depressed immunological defence mechanisms in mice with experimentally induced diabetes. Infect Immun 28 (1980) 127-131
77. Wang C.H., Yu C.T., Lin H.C., Liu C.Y., and Kuo H.P. Hypodense alveolar macrophages in patients with diabetes mellitus and active pulmonary tuberculosis. Tuber Lung Dis 79 (1999) 235-242
78. Abbras C.K. Fc receptor-mediated phagocytosis: abnormalities associated with diabetesmellitus. Clin Immunol Immunopathol 58 (1991) 1-17
79. Chang F.Y., and Shaio M.F. Decreased cell-mediated immunity in patients with non-insulin-dependent diabetes mellitus. Diabetes Res Clin Pract 28 (1995) 137-146
80. Yamashiro S., Kawakami K., Uezu K., et al. Lower expression of Th1-related cytokines and inducible nitric oxide synthase in mice with streptozotocin-induced diabetes mellitus infected with Mycobacterium tuberculosis. Clin Exp Immunol 139 (2005) 57-64
81. Martens G.W., Arikan M.C., Lee J., Ren F., Greiner D., and Kornfeld H. Tuberculosis susceptibility of diabetic mice. Am J Respir Cell Mol Biol 37 (2007) 518-524
82. Sugawara I., Yamada H., and Mizuno S. Pulmonary tuberculosis in spontaneously diabetic goto kakizaki rats. Tohoku J Exp Med 204 (2004) 135-145
83. MacCuish A.C., Urbaniak S.J., Campbell C.J., Duncan L.J., and Irvine W.J. Phytohemagglutinin transformation and circulating lymphocyte subpopulations in insulin-dependent diabetic patients. Diabetes 23 (1974) 708-712
84. Restrepo B.I., Fisher-Hoch S.P., Pino P.A., et al. Tuberculosis in poorly controlled type 2 diabetes: altered cytokine expression in peripheral white blood cells. Clin Infect Dis 47 (2008) 634-641
85. In: Larsen P.R., Kronenberg H.M., Melmed S., and Polonsky K.S. (Eds). Williams' textbook of endocrinology. 10th edn. (2003), WB Saunders Company, Philadelphia
86. Nichols G.P. Diabetes among young tuberculous patients; a review of the association of the two diseases. Am Rev Tuberc 76 (1957) 1016-1030
87. Zack M.B., Fulkerson L.L., and Stein E. Glucose intolerance in pulmonary tuberculosis. Am Rev Respir Dis 108 (1973) 1164-1169
88. Oluboyo P.O., and Erasmus R.T. The significance of glucose intolerance in pulmonary tuberculosis. Tubercle 71 (1990) 135-138
89. Basoglu O.K., Bacakoglu F., Cok G., Sayiner A., and Ates M. The oral glucose tolerance test in patients with respiratory infections. Monaldi Arch Chest Dis 54 (1999) 307-310
90. Alisjahbana B., van Crevel R., Sahiratmadja E., et al. Diabetes mellitus is strongly associated with tuberculosis in Indonesia. Int J Tuberc Lung Dis 10 (2006) 696-700
91. American Thoracic Society, CDC, Infectious Diseases Society of America. Treatment of tuberculosis. MMWR Recomm Rep 52 (2003) 1-77
92. Niemi M., Backman J.T., Neuvonen M., Neuvonen P.J., and Kivisto K.T. Effects of rifampin on the pharmacokinetics and pharmacodynamics of glyburide and glipizide. Clin Pharmacol Ther 69 (2001) 400-406
93. Atkin S., Masson E., Bodmer C., Walker B., and White M. Increased insulin requirement in a patient with type 1 diabetes on rifampicin. Diab Med 10 (1992) 202
94. Niemi M., Backman J.T., Fromm M.F., Neuvonen P.J., and Kivisto K.T. Pharmacokinetic interactions with rifampicin: clinical relevance. Clin Pharmacokinet 42 (2003) 819-850
95. Niemi M., Backman J.T., and Neuvonen P.J. Effects of trimethoprim and rifampin on the pharmacokinetics of the cytochrome P450 2C8 substrate rosiglitazone. Clin Pharmacol Ther 76 (2004) 239-249
96. Park J.Y., Kim K.A., Kang M.H., Kim S.L., and Shin J.G. Effect of rifampin on the pharmacokinetics of rosiglitazone in healthy subjects. Clin Pharmacol Ther 75 (2004) 157-162
97. Jaakkola T., Backman J.T., Neuvonen M., Laitila J., and Neuvonen P.J. Effect of rifampicin on the pharmacokinetics of pioglitazone. Br J Clin Pharmacol 61 (2006) 70-78
98. Niemi M., Backman J.T., Neuvonen M., and Neuvonen P.J. Effect of rifampicin on the pharmacokinetics and pharmacodynamics of nateglinide in healthy subjects. Br J Clin Pharmacol 56 (2003) 427-432
99. Hatorp V., Hansen K.T., and Thomsen M.S. Influence of drugs interacting with CYP3A4 on the pharmacokinetics, pharmacodynamics, and safety of the prandial glucose regulator repaglinide. J Clin Pharmacol 43 (2003) 649-660
100. Niemi M., Backman J.T., Neuvonen M., Neuvonen P.J., and Kivisto K.T. Rifampin decreases the plasma concentrations and effects of repaglinide. Clin Pharmacol Ther 68 (2000) 495-500
101. Takasu N., Yamada T., Miura H., et al. Rifampicin-induced early phase hyperglycemia in humans. Am Rev Respir Dis 125 (1982) 23-27
102. Waterhouse M., Wilson C., White V.L., and Chowdhury T.A. Resolution of insulin-requiring diabetes after cessation of chemotherapy for tuberculosis. J R Soc Med 98 (2005) 270-271
103. Nijland H.M., Ruslami R., Stalenhoef J.E., et al. Exposure to rifampicin is strongly reduced in patients with tuberculosis and type 2 diabetes. Clin Infect Dis 43 (2006) 848-854
104. Gwilt P.R., Nahhas R.R., and Tracewell W.G. The effects of diabetes mellitus on pharmacokinetics and pharmacodynamics in humans. Clin Pharmacokinet 20 (1991) 477-490
105. Peloquin C.A. Therapeutic drug monitoring in the treatment of tuberculosis. Drugs 62 (2002) 2169-2183