Prior tuberculosis, radiographic lung abnormalities and prevalent diabetes in rural South Africa.
Humans
South Africa
/ epidemiology
Female
Male
Adult
Cross-Sectional Studies
Middle Aged
Diabetes Mellitus
/ epidemiology
Rural Population
/ statistics & numerical data
Prevalence
Young Adult
Radiography, Thoracic
Adolescent
Tuberculosis, Pulmonary
/ epidemiology
Lung
/ diagnostic imaging
Radiography
Aged
Tuberculosis
/ epidemiology
Chest imaging
Diabetes
Prior tuberculosis
Journal
BMC infectious diseases
ISSN: 1471-2334
Titre abrégé: BMC Infect Dis
Pays: England
ID NLM: 100968551
Informations de publication
Date de publication:
11 Jul 2024
11 Jul 2024
Historique:
received:
03
01
2024
accepted:
02
07
2024
medline:
12
7
2024
pubmed:
12
7
2024
entrez:
11
7
2024
Statut:
epublish
Résumé
Growing evidence suggests that chronic inflammation caused by tuberculosis (TB) may increase the incidence of diabetes. However, the relationship between post-TB pulmonary abnormalities and diabetes has not been well characterized. We analyzed data from a cross-sectional study in KwaZulu-Natal, South Africa, of people 15 years and older who underwent chest X-ray and diabetes screening with hemoglobin A1c testing. The analytic sample was restricted to persons with prior TB, defined by either (1) a self-reported history of TB treatment, (2) radiologist-confirmed prior TB on chest radiography, and (3) a negative sputum culture and GeneXpert. Chest X-rays of all participants were evaluated by the study radiologist to determine the presence of TB lung abnormalities. To assess the relationships between our outcome of interest, prevalent diabetes (HBA1c ≥6.5%), and our exposure of interest, chest X-ray abnormalities, we fitted logistic regression models adjusted for potential clinical and demographic confounders. In secondary analyses, we used the computer-aided detection system CAD4TB, which scores X-rays from 10 to 100 for detection of TB disease, as our exposure interest, and repeated analyses with a comparator group that had no history of TB disease. In the analytic cohort of people with prior TB (n = 3,276), approximately two-thirds (64.9%) were women, and the average age was 50.8 years (SD 17.4). The prevalence of diabetes was 10.9%, and 53.0% of people were living with HIV. In univariate analyses, there was no association between diabetes prevalence and radiologist chest X-ray abnormalities (OR 1.23, 95%CI 0.95-1.58). In multivariate analyses, the presence of pulmonary abnormalities was associated with an 29% reduction in the odds of prevalent diabetes (aOR 0.71, 95%CI 0.53-0.97, p = 0.030). A similar inverse relationship was observed for diabetes with each 10-unit increase in the CAD4TB chest X-ray scores among people with prior TB (aOR 0.92, 95%CI 0.87-0.97; p = 0.002), but this relationship was less pronounced in the no TB comparator group (aOR 0.96, 95%CI 0.94-0.99). Among people with prior TB, pulmonary abnormalities on digital chest X-ray are inversely associated with prevalent diabetes. The severity of radiographic post-TB lung disease does not appear to be a determinant of diabetes in this South African population.
Sections du résumé
BACKGROUND
BACKGROUND
Growing evidence suggests that chronic inflammation caused by tuberculosis (TB) may increase the incidence of diabetes. However, the relationship between post-TB pulmonary abnormalities and diabetes has not been well characterized.
METHODS
METHODS
We analyzed data from a cross-sectional study in KwaZulu-Natal, South Africa, of people 15 years and older who underwent chest X-ray and diabetes screening with hemoglobin A1c testing. The analytic sample was restricted to persons with prior TB, defined by either (1) a self-reported history of TB treatment, (2) radiologist-confirmed prior TB on chest radiography, and (3) a negative sputum culture and GeneXpert. Chest X-rays of all participants were evaluated by the study radiologist to determine the presence of TB lung abnormalities. To assess the relationships between our outcome of interest, prevalent diabetes (HBA1c ≥6.5%), and our exposure of interest, chest X-ray abnormalities, we fitted logistic regression models adjusted for potential clinical and demographic confounders. In secondary analyses, we used the computer-aided detection system CAD4TB, which scores X-rays from 10 to 100 for detection of TB disease, as our exposure interest, and repeated analyses with a comparator group that had no history of TB disease.
RESULTS
RESULTS
In the analytic cohort of people with prior TB (n = 3,276), approximately two-thirds (64.9%) were women, and the average age was 50.8 years (SD 17.4). The prevalence of diabetes was 10.9%, and 53.0% of people were living with HIV. In univariate analyses, there was no association between diabetes prevalence and radiologist chest X-ray abnormalities (OR 1.23, 95%CI 0.95-1.58). In multivariate analyses, the presence of pulmonary abnormalities was associated with an 29% reduction in the odds of prevalent diabetes (aOR 0.71, 95%CI 0.53-0.97, p = 0.030). A similar inverse relationship was observed for diabetes with each 10-unit increase in the CAD4TB chest X-ray scores among people with prior TB (aOR 0.92, 95%CI 0.87-0.97; p = 0.002), but this relationship was less pronounced in the no TB comparator group (aOR 0.96, 95%CI 0.94-0.99).
CONCLUSIONS
CONCLUSIONS
Among people with prior TB, pulmonary abnormalities on digital chest X-ray are inversely associated with prevalent diabetes. The severity of radiographic post-TB lung disease does not appear to be a determinant of diabetes in this South African population.
Identifiants
pubmed: 38992607
doi: 10.1186/s12879-024-09583-8
pii: 10.1186/s12879-024-09583-8
doi:
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Pagination
690Subventions
Organisme : FIC NIH HHS
ID : D43 TW010543
Pays : United States
Organisme : NIAID NIH HHS
ID : T32 AI007433
Pays : United States
Organisme : NIAID NIH HHS
ID : K24 AI141036
Pays : United States
Organisme : Wellcome Trust
ID : 201433/Z/16/A
Pays : United Kingdom
Organisme : NHLBI NIH HHS
ID : K24 HL166024
Pays : United States
Informations de copyright
© 2024. The Author(s).
Références
WHO. Global tuberculosis report 2021. World Health Organization; 2020.
Federation ID. IDF Diabetes Atlas, 9th edition. 2019.
Jeon CY, Murray MB. Diabetes mellitus increases the risk of active tuberculosis: a systematic review of 13 observational studies. PLoS Med. 2008;5(7):e152.
pubmed: 18630984
pmcid: 2459204
doi: 10.1371/journal.pmed.0050152
Baker MA, Harries AD, Jeon CY, Hart JE, Kapur A, Lonnroth K, et al. The impact of diabetes on tuberculosis treatment outcomes: a systematic review. BMC Med. 2011;9:81.
pubmed: 21722362
pmcid: 3155828
doi: 10.1186/1741-7015-9-81
Awad SF, Dargham SR, Omori R, Pearson F, Critchley JA, Abu-Raddad LJ. Analytical Exploration of potential pathways by which diabetes Mellitus impacts Tuberculosis Epidemiology. Sci Rep. 2019;9(1):8494.
pubmed: 31186499
pmcid: 6560095
doi: 10.1038/s41598-019-44916-7
Odone A, Houben RM, White RG, Lonnroth K. The effect of diabetes and undernutrition trends on reaching 2035 global tuberculosis targets. Lancet Diabetes Endocrinol. 2014;2(9):754–64.
pubmed: 25194888
doi: 10.1016/S2213-8587(14)70164-0
Magee MJ, Khakharia A, Gandhi NR, Day CL, Kornfeld H, Rhee MK et al. Increased risk of Incident Diabetes among individuals with latent tuberculosis infection. Diabetes Care. 2022.
Pearson F, Huangfu P, McNally R, Pearce M, Unwin N, Critchley JA. Tuberculosis and diabetes: bidirectional association in a UK primary care data set. J Epidemiol Community Health. 2019;73(2):142–7.
pubmed: 30377249
doi: 10.1136/jech-2018-211231
Magee MJ, Salindri AD, Kyaw NTT, Auld SC, Haw JS, Umpierrez GE. Stress hyperglycemia in patients with tuberculosis disease: epidemiology and clinical implications. Curr Diab Rep. 2018;18(9):71.
pubmed: 30090969
pmcid: 6309553
doi: 10.1007/s11892-018-1036-y
Magee MJ, Salindri AD, Gujral UP, Auld SC, Bao J, Haw JS, et al. Convergence of non-communicable diseases and tuberculosis: a two-way street? Int J Tuberc Lung Dis. 2018;22(11):1258–68.
pubmed: 30355404
doi: 10.5588/ijtld.18.0045
Brown TT, Tassiopoulos K, Bosch RJ, Shikuma C, McComsey GA. Association between systemic inflammation and incident diabetes in HIV-infected patients after initiation of antiretroviral therapy. Diabetes Care. 2010;33(10):2244–9.
pubmed: 20664016
pmcid: 2945167
doi: 10.2337/dc10-0633
Martinez N, Cheng CY, Ketheesan N, Cullen A, Tang Y, Lum J, et al. mTORC2/Akt activation in adipocytes is required for adipose tissue inflammation in tuberculosis. EBioMedicine. 2019;45:314–27.
pubmed: 31279779
pmcid: 6642333
doi: 10.1016/j.ebiom.2019.06.052
Beigier-Bompadre M, Montagna GN, Kuhl AA, Lozza L, Weiner J 3rd, Kupz A, et al. Mycobacterium tuberculosis infection modulates adipose tissue biology. PLoS Pathog. 2017;13(10):e1006676.
pubmed: 29040326
pmcid: 5695609
doi: 10.1371/journal.ppat.1006676
Podell BK, Ackart DF, Kirk NM, Eck SP, Bell C, Basaraba RJ. Non-diabetic hyperglycemia exacerbates disease severity in Mycobacterium tuberculosis infected guinea pigs. PLoS ONE. 2012;7(10):e46824.
pubmed: 23056469
pmcid: 3464230
doi: 10.1371/journal.pone.0046824
Kornfeld H, West K, Kane K, Kumpatla S, Zacharias RR, Martinez-Balzano C, et al. High prevalence and heterogeneity of diabetes in patients with TB in South India: a report from the effects of Diabetes on Tuberculosis Severity (EDOTS) Study. Chest. 2016;149(6):1501–8.
pubmed: 26973015
pmcid: 4944775
doi: 10.1016/j.chest.2016.02.675
Tepekule B, Kusejko K, Zeeb M, Tarr PE, Calmy A, Battegay M, et al. Impact of latent tuberculosis on diabetes. J Infect Dis. 2022;225(12):2229–34.
pubmed: 35172332
doi: 10.1093/infdis/jiac054
Boillat-Blanco N, Ramaiya KL, Mganga M, Minja LT, Bovet P, Schindler C, et al. Transient hyperglycemia in patients with tuberculosis in Tanzania: implications for diabetes screening algorithms. J Infect Dis. 2016;213(7):1163–72.
pubmed: 26609005
doi: 10.1093/infdis/jiv568
Kornfeld H, Procter-Gray E, Kumpatla S, Kane K, Li W, Magee MJ, et al. Longitudinal trends in glycated hemoglobin during and after tuberculosis treatment. Diabetes Res Clin Pract. 2023;196:110242.
pubmed: 36627027
doi: 10.1016/j.diabres.2023.110242
Bellamy L, Casas JP, Hingorani AD, Williams D. Type 2 diabetes mellitus after gestational diabetes: a systematic review and meta-analysis. Lancet. 2009;373(9677):1773–9.
pubmed: 19465232
doi: 10.1016/S0140-6736(09)60731-5
Castle AC, Hoeppner SS, Magodoro IM, Singh U, Moosa Y, Bassett IV, et al. Association between prior tuberculosis disease and dysglycemia within an HIV-endemic, rural South African population. PLoS ONE. 2023;18(3):e0282371.
pubmed: 36928895
pmcid: 10019670
doi: 10.1371/journal.pone.0282371
Bisht MK, Dahiya P, Ghosh S, Mukhopadhyay S. The cause-effect relation of tuberculosis on incidence of diabetes mellitus. Front Cell Infect Microbiol. 2023;13:1134036.
pubmed: 37434784
pmcid: 10330781
doi: 10.3389/fcimb.2023.1134036
Ding Y, Haks MC, van den Eeden SJF, Ottenhoff THM, Harms AC, Hankemeier T, et al. Leptin mutation and mycobacterial infection lead non-synergistically to a similar metabolic syndrome. Metabolomics. 2022;18(8):67.
pubmed: 35933481
pmcid: 9356939
doi: 10.1007/s11306-022-01921-8
Vrieling F, Ronacher K, Kleynhans L, van den Akker E, Walzl G, Ottenhoff THM, et al. Patients with concurrent tuberculosis and diabetes have a pro-atherogenic plasma lipid Profile. EBioMedicine. 2018;32:192–200.
pubmed: 29779698
pmcid: 6020709
doi: 10.1016/j.ebiom.2018.05.011
Krug S, Parveen S, Bishai WR. Host-Directed therapies: modulating inflammation to treat tuberculosis. Front Immunol. 2021;12:660916.
pubmed: 33953722
pmcid: 8089478
doi: 10.3389/fimmu.2021.660916
Stek C, Allwood B, Walker NF, Wilkinson RJ, Lynen L, Meintjes G. The Immune mechanisms of Lung Parenchymal damage in tuberculosis and the role of host-Directed Therapy. Front Microbiol. 2018;9:2603.
pubmed: 30425706
pmcid: 6218626
doi: 10.3389/fmicb.2018.02603
Moreira-Teixeira L, Stimpson PJ, Stavropoulos E, Hadebe S, Chakravarty P, Ioannou M, et al. Type I IFN exacerbates disease in tuberculosis-susceptible mice by inducing neutrophil-mediated lung inflammation and NETosis. Nat Commun. 2020;11(1):5566.
pubmed: 33149141
pmcid: 7643080
doi: 10.1038/s41467-020-19412-6
Gunda R, Koole O, Gareta D, Olivier S, Surujdeen A, Smit T et al. Cohort Profile: The Vukuzazi (‘Wake Up and Know Yourself’ in isiZulu) population science programme. Int J Epidemiol. 2021.
Wong EB, Olivier S, Gunda R, Koole O, Surujdeen A, Gareta D, et al. Convergence of infectious and non-communicable disease epidemics in rural South Africa: a cross-sectional, population-based multimorbidity study. Lancet Glob Health. 2021;9(7):e967–76.
pubmed: 34143995
pmcid: 8220132
doi: 10.1016/S2214-109X(21)00176-5
WHO. The WHO STEPwise approach to noncommunicable disease risk factor surveillance (STEPS) - Instrument.
Fehr J, Konigorski S, Olivier S, Gunda R, Surujdeen A, Gareta D, et al. Computer-aided interpretation of chest radiography reveals the spectrum of tuberculosis in rural South Africa. NPJ Digit Med. 2021;4(1):106.
pubmed: 34215836
pmcid: 8253848
doi: 10.1038/s41746-021-00471-y
Murphy K, Habib SS, Zaidi SMA, Khowaja S, Khan A, Melendez J, et al. Computer aided detection of tuberculosis on chest radiographs: an evaluation of the CAD4TB v6 system. Sci Rep. 2020;10(1):5492.
pubmed: 32218458
pmcid: 7099074
doi: 10.1038/s41598-020-62148-y
Menon S, Rossi R, Dusabimana A, Zdraveska N, Bhattacharyya S, Francis J. The epidemiology of tuberculosis-associated hyperglycemia in individuals newly screened for type 2 diabetes mellitus: systematic review and meta-analysis. BMC Infect Dis. 2020;20(1):937.
pubmed: 33297969
pmcid: 7724718
doi: 10.1186/s12879-020-05512-7
WHO. Classification of Diabetes Mellitus. World Health Organization. 2019:36.
Darbandi M, Pasdar Y, Moradi S, Mohamed HJJ, Hamzeh B, Salimi Y. Discriminatory capacity of Anthropometric Indices for Cardiovascular Disease in adults: a systematic review and Meta-analysis. Prev Chronic Dis. 2020;17:E131.
pubmed: 33092686
pmcid: 7587303
doi: 10.5888/pcd17.200112
Gareta D, Baisley K, Mngomezulu T, Smit T, Khoza T, Nxumalo S, et al. Cohort Profile Update: Africa Centre Demographic Information System (ACDIS) and population-based HIV survey. Int J Epidemiol. 2021;50(1):33–4.
pubmed: 33437994
pmcid: 7938501
doi: 10.1093/ije/dyaa264
Filmer D, Pritchett LH. Estimating wealth effects without expenditure data–or tears: an application to educational enrollments in states of India. Demography. 2001;38(1):115–32.
pubmed: 11227840
Kagujje M, Kerkhoff AD, Nteeni M, Dunn I, Mateyo K, Muyoyeta M. The performance of computer-aided detection digital chest X-ray Reading technologies for triage of active tuberculosis among persons with a history of previous tuberculosis. Clin Infect Dis. 2023;76(3):e894–901.
pubmed: 36004409
doi: 10.1093/cid/ciac679
Qin ZZ, Barrett R, Ahmed S, Sarker MS, Paul K, Adel ASS, et al. Comparing different versions of computer-aided detection products when reading chest X-rays for tuberculosis. PLOS Digit Health. 2022;1(6):e0000067.
pubmed: 36812562
pmcid: 9931298
doi: 10.1371/journal.pdig.0000067
Soares TR, Oliveira RD, Liu YE, Santos ADS, Santos P, Monte LRS, et al. Evaluation of chest X-ray with automated interpretation algorithms for mass tuberculosis screening in prisons: a cross-sectional study. Lancet Reg Health Am. 2023;17:100388.
pubmed: 36776567
Prada-Medina CA, Fukutani KF, Pavan Kumar N, Gil-Santana L, Babu S, Lichtenstein F, et al. Systems Immunology of Diabetes-Tuberculosis Comorbidity reveals signatures of Disease complications. Sci Rep. 2017;7(1):1999.
pubmed: 28515464
pmcid: 5435727
doi: 10.1038/s41598-017-01767-4
Mayer Bridwell AE. mSphere of influence: the key role of neutrophils in tuberculosis and type 2 diabetes comorbidity. mSphere. 2021;6(3):e0025121.
pubmed: 34047649
doi: 10.1128/mSphere.00251-21
Huang LK, Wang HH, Lai YC, Chang SC. The impact of glycemic status on radiological manifestations of pulmonary tuberculosis in diabetic patients. PLoS ONE. 2017;12(6):e0179750.
pubmed: 28628646
pmcid: 5476287
doi: 10.1371/journal.pone.0179750
Perez-Guzman C, Torres-Cruz A, Villarreal-Velarde H, Vargas MH. Progressive age-related changes in pulmonary tuberculosis images and the effect of diabetes. Am J Respir Crit Care Med. 2000;162(5):1738–40.
pubmed: 11069805
doi: 10.1164/ajrccm.162.5.2001040
Shaikh MA, Singla R, Khan NB, Sharif NS, Saigh MO. Does diabetes alter the radiological presentation of pulmonary tuberculosis. Saudi Med J. 2003;24(3):278–81.
pubmed: 12704504
Habib SS, Rafiq S, Zaidi SMA, Ferrand RA, Creswell J, Van Ginneken B, et al. Evaluation of computer aided detection of tuberculosis on chest radiography among people with diabetes in Karachi Pakistan. Sci Rep. 2020;10(1):6276.
pubmed: 32286389
pmcid: 7156514
doi: 10.1038/s41598-020-63084-7
Jimenez-Corona ME, Cruz-Hervert LP, Garcia-Garcia L, Ferreyra-Reyes L, Delgado-Sanchez G, Bobadilla-Del-Valle M, et al. Association of diabetes and tuberculosis: impact on treatment and post-treatment outcomes. Thorax. 2013;68(3):214–20.
pubmed: 23250998
doi: 10.1136/thoraxjnl-2012-201756
Kuruva P, Kandi SR, Kandi S. Clinico-radiological profile and treatment outcome of pulmonary tuberculosis with and without type 2 diabetes mellitus. Indian J Tuberc. 2021;68(2):249–54.
pubmed: 33845960
doi: 10.1016/j.ijtb.2020.09.020
Alkabab YM, Enani MA, Indarkiri NY, Heysell SK. Performance of computed tomography versus chest radiography in patients with pulmonary tuberculosis with and without diabetes at a tertiary hospital in Riyadh, Saudi Arabia. Infect Drug Resist. 2018;11:37–43.
pubmed: 29379307
pmcid: 5757200
doi: 10.2147/IDR.S151844
Geric C, Majidulla A, Tavaziva G, Nazish A, Saeed S, Benedetti A, et al. Artificial intelligence-reported chest X-ray findings of culture-confirmed pulmonary tuberculosis in people with and without diabetes. J Clin Tuberc Other Mycobact Dis. 2023;31:100365.
pubmed: 37095759
pmcid: 10121442
doi: 10.1016/j.jctube.2023.100365
Schols AM. Pulmonary cachexia. Int J Cardiol. 2002;85(1):101–10.
pubmed: 12163214
doi: 10.1016/S0167-5273(02)00238-3
Ferrer M, Anthony TG, Ayres JS, Biffi G, Brown JC, Caan BJ, et al. Cachexia: a systemic consequence of progressive, unresolved disease. Cell. 2023;186(9):1824–45.
pubmed: 37116469
pmcid: 11059056
doi: 10.1016/j.cell.2023.03.028
Agusti A, Calverley PM, Celli B, Coxson HO, Edwards LD, Lomas DA, et al. Characterisation of COPD heterogeneity in the ECLIPSE cohort. Respir Res. 2010;11(1):122.
pubmed: 20831787
pmcid: 2944278
doi: 10.1186/1465-9921-11-122
Hersh CP, Make BJ, Lynch DA, Barr RG, Bowler RP, Calverley PM, et al. Non-emphysematous chronic obstructive pulmonary disease is associated with diabetes mellitus. BMC Pulm Med. 2014;14:164.
pubmed: 25341556
pmcid: 4216374
doi: 10.1186/1471-2466-14-164
Jin J, Li S, Yu W, Liu X, Sun Y. Emphysema and bronchiectasis in COPD patients with previous pulmonary tuberculosis: computed tomography features and clinical implications. Int J Chron Obstruct Pulmon Dis. 2018;13:375–84.
pubmed: 29416328
pmcid: 5788930
doi: 10.2147/COPD.S152447
Romanowski K, Baumann B, Basham CA, Ahmad Khan F, Fox GJ, Johnston JC. Long-term all-cause mortality in people treated for tuberculosis: a systematic review and meta-analysis. Lancet Infect Dis. 2019;19(10):1129–37.
pubmed: 31324519
doi: 10.1016/S1473-3099(19)30309-3
Mpagama SG, Msaji KS, Kaswaga O, Zurba LJ, Mbelele PM, Allwood BW, et al. The burden and determinants of post-TB lung disease. Int J Tuberc Lung Dis. 2021;25(10):846–53.
pubmed: 34615582
pmcid: 8504494
doi: 10.5588/ijtld.21.0278
van Kampen SC, Wanner A, Edwards M, Harries AD, Kirenga BJ, Chakaya J, et al. International research and guidelines on post-tuberculosis chronic lung disorders: a systematic scoping review. BMJ Glob Health. 2018;3(4):e000745.
pubmed: 30057796
pmcid: 6058174
doi: 10.1136/bmjgh-2018-000745
Mungai BN, Joekes E, Masini E, Obasi A, Manduku V, Mugi B, et al. If not TB, what could it be?’ Chest X-ray findings from the 2016 Kenya Tuberculosis Prevalence Survey. Thorax. 2021;76(6):607–14.
pubmed: 33504563
doi: 10.1136/thoraxjnl-2020-216123