Article:Meta-analysis of the prevalence of tuberculosis in diabetic patients and its association with cigarette smoking in African and Asian countries. (5952828)
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Title: BMC Research Notes
Meta-analysis of the prevalence of tuberculosis in diabetic patients and its association with cigarette smoking in African and Asian countries
- Fasil Wagnew
- Setegn Eshetie
- Animut Alebel
- Getenet Dessie
- Cheru Tesema
- Amanuel Alemu Abajobir
Publication date (epub): 5/2018
Publication date (pmc-release): 5/2018
Publication date (collection): /2018
This systematic review and meta-analysis was undertaken to estimate the prevalence of tuberculosis in diabetic patients and to determine the effect of cigarette smoking.
A total of 15 studies was included in the meta-analysis. The pooled overall prevalence of tuberculosis in diabetes was 4.72% (95% CI 3.62–5.83%). In sub-group analyses, the prevalence was 5.13% (95% CI 4.34–5.92%) in Africa, followed by 4.16% (95% CI 2.9–5.4%) in Asia. The odd ratio of tuberculosis among diabetes patients was 7.6 (95% CI 1.46–39) in cigarette smokers as compared to nonsmokers. Publication bias was detected based on graphic asymmetry of fun-nel plots, Begg’s and Egger’s tests (p < 0.05). Tuberculosis is a common co-morbidity in diabetic patients. Tuberculosis-diabetes co-morbidity is significantly higher in cigarette smokers.
Electronic supplementary material
The online version of this article (10.1186/s13104-018-3390-x) contains supplementary material, which is available to authorized users.
Tuberculosis (TB) is an infectious disease caused by various strains of mycobacterium, particularly Mycobacterium tuberculosis, and usually affects the respiratory system . Diabetes mellitus (DM) is a complex metabolic disorder featured by a high level of blood sugar either because of inadequate insulin production or less sensitivity of cells responsible to the insulin metabolism , and associated with impairment of cell-mediated immunity involving the lungs, kidney dysfunctions, and micronutrient deficiencies . The World Health Organization (WHO, 2017) reported that there were 10.4 million TB new cases and 1.7 million deaths due to TB . Similarly, 415 million cases and 5.0 million deaths due to DM were registered . Tragically, 95% TB and 75% DM cases exist in low and middle income countries (e.g., Africa and Southeast Asia) .
TB and DM co-morbidity is considerably an emerging public health problem , and TB is the third leading cause of death among patients with non-communicable disease (NCD), particularly DM . For example, the number of patients with TB-DM co-morbidity is higher than the number of patients with TB-HIV(Human Immuno Deficiency) co-infection globally . That is, the rising prevalence of DM is becoming a challenge to TB control [, ] and vice versa. This may partially be due to the risk of uncontrolled hyperglycemia for TB  and diabetic  patients with substantial immuno compromisation . That said, people with diabetes are three times more likely to develop TB when exposed and approximately 15% of TB globally is thought to be related to diabetes . Moreover, those people with TB and coexisting diabetes have 4 times higher risk of worsening TB treatment outcomes and death during the course of TB regimen . In addition, this may be more complicated by common risk factors for TB including HIV, malnutrition, alcoholism and cigarette smoking .
A previous study of TB-DM co-morbidity has reported high prevalence of TB in DM patients, ranging from 1.7 to 36% . As a result, WHO has strongly recommended a collaborative framework for clinical management and control of TB-DM co-morbidity. That is, people with diabetes to be screened for cough of 2 weeks or more at the time of diagnosis for diabetes and, possibly, during regular follow-ups. Thus, three important intervention strategies, namely, establishing mechanisms of collaboration between TB and DM control programs, early detection and management of TB in patients with DM, and early detection and management of DM in TB patients have been recommended . These strategies may also have pivotal roles, notably for high TB burden countries to mitigate the dual burden of TB-DM co-morbidity. Thus, it is crucial to understand the prevalence of TB-DM co-morbidity particularly in low and middle-income countries.
Furthermore, cigarette smoking has adverse effects on respiratory function and is associated with an increased risk of respiratory tract infection and TB-DM co-morbidity [–]. Cognizant to this, WHO and International Union Against Tuberculosis and Lung Disease (The Union) have encouraged a National TB Programme to address the combined challenges of smoking, diabetes and TB [, ].
Generally, previous TB-DM co-morbidity studies, mainly from African countries, on bi-directional screenings of TB and DM and have not considered the risk of cigarette smoking. In another words, even though some previous studies [, ] determined the association between smoking status and the risk of TB in DM patients, the evidence base still remains inconsistence and inconclusive. This systematic review and meta-analysis is therefore aimed to summarize the prevalence of TB in DM adult patients and its association with history of cigarette smoking.
Study design and search strategy
This systematic review and meta-analysis was carried out using both published and unpublished literature to estimate the prevalence of TB among diabetes patients and to determine the risk of TB-DM co-morbidity in cigarette smoking patients. Studies were found through electronic and manual searches using databases, Psych INFO, EMBASE, MEDLINE/PubMed, Google scholar and Google for gray literature from 1980-2017. The search terms were used, entering the following key terms: “prevalence” OR “Epidemiology” AND “tuberculosis,” OR “TB” AND “Diabetes Mellitus,” OR “DM*” OR “Diabet* “Co-morbid*” AND Asian countries” OR “African countries”. Electronic searches were supplemented by screening the reference lists of included studies, expert recommendations and hand searches for sources of gray literature. The preferred reporting of systematic reviews and meta-analysis (PRISMA) guidelines were used  for the review.
Included studies were those that obtained ethical approval and were undertaken in high TB burden countries (African and Asian countries) and/or reported the prevalence of TB among diabetes patients and/or determine the effect of cigarette smoking in these patients. Peer-reviewed studies with cross-sectional survey or case-series designs, and those studies that involved primary outcome(s) of interest were included.
Those studies that reported incidence, only multi-drug resistance TB and latent TB were excluded from the analysis.
Two reviewers (FW and SE) screened the titles and abstracts of identified studies and assessed the full text of potentially eligible studies. Any controversy was resolved by consensus. We made some efforts to communicate the authors whenever further information was needed. Data from the included studies were extracted independently by these reviewers. Interestingly, we checked a random sample of 30% of the extracted data and found no difference. Data on author(s), study year, region of study, study design and sample size were extracted using Microsoft excel. The overall prevalence of TB in diabetic patients was also extracted from each included study. Moreover, data on the risk of cigarette smoking among these patients were extracted. AAA critically reviewed the manuscript.
Articles were assessed for quality score using Newcastle–Ottawa Scale adapted for cross-sectional studies quality assessment tool, with a score of ≥ 5 out of 10 considered as high quality score. Two authors (FW, SE) assessed the quality of each paper. The reviewers compared quality appraisal scores and resolved any disagreements before calculating the final appraisal score. All included studies were of high quality score.
Meta-analysis of pooled prevalence of TB in DM patients was carried out using a random-effects model, generating a pooled prevalence with 95% CIs, using STATA/se version 14. Subgroup analyses by continents (Africa and Asia) were carried out because of significant heterogeneity between studies and/or countries.
OR of TB among diabetic patients with cigarette smokers (compared to nonsmokers) was also determined. Heterogeneity among studies was estimated using the I2 statistics . Publication bias was determined based on the symmetry of fun-nel plots , Begg’s and Egger’s tests . As well, the trim-and-fill analysis was considered to estimate the final effect-size while publication bias detected .
After screening for titles, 1313 studies were excluded because of unrelated topics and duplication. The full-texts of 31 studies were screened and 16 studies of which were subsequently omitted from the meta-analysis for there were insufficient data on outcome(s) of interest. A total of 15 studies representing 23,068 participants, which fulfilled the eligibility criteria, were included in the final meta-analysis (Additional file 1: Figure S1). Sixteen studies were excluded because of 2 studies were reported TB incidence done in Korea and Indonesia [, ], 11 studies were not reported outcome of interest [–], 1 MDR-TB , 2 studies were explore pharmacological aspect of TB-DM [, ]).
Prevalence of TB among DM patients
Among the 15 cross-sectional studies included, 9 (52.6%) were from the Asian countries and the prevalence ranged from 0.38% in Taiwan  to 14% in Pakistan . Six (36.8%) prevalence studies were conducted in African countries, and the prevalence revealed as low as 3.4% in South Africa  and as high as 6.2% in Ethiopia  (Tables 1).Table 1
The descriptive summary of 15 studies on the prevalence of TB among DM patients and its associated with history of smoking in Africa and Asia with high TB burden
Prevalence of TB among DM patients
The overall pooled prevalence of TB among DM patients was 4.72% (95% CI 3.62–5.83). Based on subgroup analyses by continents, the pooled prevalence of TB among DM patients was 4.16% (95% CI 2.9–5.42) in Asia and 5.13% (95% CI 4.34–5.92) in Africa (Fig. 1).Fig. 1
Pooled prevalence of TB among DM patients in African and Asian countries with high TB-burden
Effect of cigarette smoking on TB-DM co-morbidity
To determine the association of cigarette smoking with TB-DM co-morbidity, we included 3 studies which reported data on the prevalence of TB among DM patients who had a history of cigarette smoking. It was shown that the risk of TB-DM co-morbidity was more than 7 (95% CI 1.46–39.53) times higher in patients who had a history of cigarette smoking as compared to their nonsmoker counterparts (Fig. 2).Fig. 2
Pooled odds ratio indicating the association of cigarette smoking with TB-DM co-morbidity
Publication bias was detected based on graphic asymmetry of funnel plots, and Egger’s test (p < 0.05). However, Begg’s test indicated no publication bias (Additional file 2: Fig S2). Considering the conflicting evidence on the possible publication bias, trim-and-fill method was used to estimate the publication bias . Though this method indicated 2 potential studies missing, the final results were almost similar to the original findings after 2 virtual studies were appended, indicating that the results of this meta-analysis were steady.
The present meta-analysis was conducted to determine the point prevalence of TB among diabetic patients and its association with cigarette smoking in Asian and African countries with a high TB burden. Existing evidence based on data from 15 included studies with 23,068 study participants revealed a 4.7% point prevalence of TB among diabetic patients in these countries. Poor DM control (as indicated by high HbA1c level) may be associated with differences in the physiological/pathological functions that perhaps boost progression to active TB disease  in these patients. This finding is higher as compared to a previous systematic review by Jeon. et al. . The observed variations might be due to aging, changes in lifestyle, and socioeconomic factors. This may be that some countries are experiencing the fastest increase in DM prevalence along with the highest burden of TB and HIV [, ]. Despite substantial overlaps of CIs, subgroup analyses by continents suggested the point prevalence of TB among diabetic patients was fairly higher in Africa as compared to Asia. This finding is supported by previous systematic review that reported higher median prevalence of TB in African diabetic patients than the Asian counterparts . This discrepancy might partly be attributable to the functional “Collaborative Framework for the care and control of Diabetes and Tuberculosis” to detect and treat TB in diabetic patients  that might have contributed to the lower prevalence of TB-DM co-morbidity. In other words, African countries (e.g., sub-Saharan Africa) have recently been experiencing DM and other chronic conditions  possibly because of lack of such an intervention.
A further aim of this study was to determine the effect of cigarette smoking on the occurance of TB among DM patients. Cigarette smoking was found to be significantly associated with TB-DM co-morbidity. This was in accordance with another systematic review that reported exposure to environmental tobacco smoke increases the risks of developing TB disease and infection . Another systematic review by Lonnroth, et al.  also revealed that under-nutrition, cigarette smoking and inappropriate alcohol consumption can double or triple the risk of TB-DM co-morbidity. This could be because of the complex etiopathological mechanisms in cigarette smokers resulting in inflammation and oxidative stress that may increase the risk of developing TB-DM . Furthermore, cigarette smoking can increase the availability of iron in lower respiratory tract part  that may react with nitric oxide to produce toxic chemicals that can decrease immunity .
TB is a common co-morbidity in diabetic patients. TB-DM co-morbidity is significantly higher in cigarette smokers. Screening for TB in diabetic patients as well as lifestyle intervention may improve early case detection, prevent transmission and decrease the risk of TB-DM co-morbidity.
The inclusion of studies published only in English may compromise representativeness (language bias). Incapability to reliable differentiate between type-I and type-II diabetes mellitus. As well, because of lack of uniformity across each study, we did not explore other factors affecting TB-DM co-morbidity but cigarette smoking.
Additional file 1: Figure S1. Flow chart describing selection of studies for a systematic review and meta-analysis of the prevalence of tuberculosis among diabetes patients and its association with cigarette smoking.
Additional file 2: Figure S2. Funnel plots, exploring publication bias for the analysis of pooled estimate.
FW involved in the conception of the research idea; (FW, SE) undertook data extraction, analysis, interpretation, and manuscript write-up. (FW, SE and AAA) interpreted the results, and drafted the manuscript. (AA, GD, CT) revised the manuscript. All authors read and approved the final manuscript.
The authors would like to acknowledge the Debre Markos University library for providing us with a wide range of available online databases.
The authors declare that they have no competing interests.
Availability of data and materials
The datasets used and/or analysed during the current study are available from the corresponding author on reasonable request.
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- I SmithMycobacterium tuberculosis pathogenesis and molecular determinants of virulenceClin Microbiol Rev200316346349610.1128/CMR.16.3.463-496.200312857778
- International Diabetes FederationDiabetes blue circle symbol2006BrusselsInternational Diabetes Federation
- Y LinL LiF MiJ DuY DongZ LiW QiX ZhaoY CuiF HouScreening patients with diabetes mellitus for tuberculosis in ChinaTropical Med Int Health201217101302130810.1111/j.1365-3156.2012.03069.x
- World Health OrganizationGlobal tuberculosis report2017GenevaWorld Health Organization
- International Diabetes FederationDiabetes atlas20157BrusselsInternational Diabetes Federation
- K SyalA SrinivasanD BanerjeeVDR, RXR, coronin-1 and interferonγ levels in PBMCs of type-2 diabetes patients: molecular link between diabetes and tuberculosisIndian J Clin Biochem201530332332810.1007/s12291-014-0431-726089620
- D BanerjeeR BhattacharyyaD KaulP SharmaDiabetes and tuberculosis: analysis of a paradoxAdv Clin Chem20115313910.1016/B978-0-12-385855-9.00006-021404917
- R RuslamiRE AarnoutseB AlisjahbanaAJ Van Der VenR Van CrevelImplications of the global increase of diabetes for tuberculosis control and patient careTrop Med Int Health201015111289129910.1111/j.1365-3156.2010.02625.x20955495
- CY JeonAD HarriesMA BakerJE HartA KapurK LönnrothSE OttmaniS GoonesekeraMB MurrayBi-directional screening for tuberculosis and diabetes: a systematic reviewTrop Med Int Health201015111300131410.1111/j.1365-3156.2010.02632.x20958887
- AL RizaF PearsonC Ugarte-GilB AlisjahbanaS van de VijverNM PanduruPC HillR RuslamiD MooreR AarnoutseClinical management of concurrent diabetes and tuberculosis and the implications for patient servicesLancet Diabetes Endocrinol20142974075310.1016/S2213-8587(14)70110-X25194887
- USAID Health-Related Research and Development Progress Report, Report to Congress; 2013. p. 25–27. Available at: https://www.usaid.gov/sites/default/files/documents/1864/Health%20Research%20Report.pdf
- MA BakerAD HarriesCY JeonJE HartA KapurK LönnrothS-E OttmaniSD GoonesekeraMB MurrayThe impact of diabetes on tuberculosis treatment outcomes: a systematic reviewBMC Med2011918110.1186/1741-7015-9-8121722362
- International Diabetes Federation (IDF). Global Diabetes Plan 2011–2021. Brussels: International Diabetes Federation. Available at: https://www.worlddiabetesfoundation.org/sites/default/files/TB-diabetes%20co-epidemic%20fact%20sheet_March2014%20update.pdf
- The International Union against Tuberculosis and Lung Disease and the World Diabetes Foundation. The growing threat of the double burden of diabetes and tuberculosis. 2014. Available at: https://www.worlddiabetesfoundation.org/sites/default/files/TB-diabetes%20co-epidemic%20fact%20sheet_March2014%20update.pdf
- World Health OrganizationCollaborative framework for care and control of tuberculosis and diabetes2013GenevaWorld Health Organization
- J-Y FengS-F HuangW-Y TingM-C LeeY-C ChenY-Y LinY-C LeeW-J SuImpact of cigarette smoking on latent tuberculosis infection: does age matter?Eur Respir J201443263063210.1183/09031936.0011831324072215
- J GarmendiaP MoreyJ BengoecheaImpact of cigarette smoke exposure on host–bacterial pathogen interactionsEur Respir J201239246747710.1183/09031936.0006191121737564
- CC LeungWW YewWS LawCM TamM LeungYW ChungKW CheungKW ChanF FuSmoking and tuberculosis among silicotic patientsEur Respir J200729474575010.1183/09031936.0013470617182648
- S ShangD OrdwayM Henao-TamayoX BaiR Oberley-DeeganC ShanleyIM OrmeS CaseM MinorD AckartCigarette smoke increases susceptibility to tuberculosis—evidence from in vivo and in vitro modelsJ Infect Dis201120391240124810.1093/infdis/jir00921357942
- K BissellT FraserCY ChiangDA EnarsonSmoking cessation and smoke free environments for tuberculosis patients20102ParisInternational Union Against Tuberculosis and Lung Disease250
- World Health OrganizationInternational Union Against Tuberculosis and Lung DiseaseCollaborative framework for care and control of tuberculosis and diabetesWorld Health Organ Doc201115140
- H AmareA GelawB AnagawB GelawSmear positive pulmonary tuberculosis among diabetic patients at the Dessie referral hospital, Northeast EthiopiaInfect Dis Poverty201321610.1186/2049-9957-2-624499664
- Sisay T. The magnitude and associated factors of tuberculosis among diabetic patients at Tikur Anbessa specialized teaching hospital in Addis Ababa, Ethiopia. MPH thesis, Addis Ababa University. 2015. Available at: https://oatd.org/oatd/search?q=sisay+tiroro%26form=basic.
- A LiberatiDG AltmanJ TetzlaffC MulrowPC GotzscheJP IoannidisM ClarkePJ DevereauxJ KleijnenD MoherThe PRISMA statement for reporting systematic reviews and meta-analyses of studies that evaluate health care interventions: explanation and elaborationJ Clin Epidemiol20096210e1e3410.1016/j.jclinepi.2009.06.00619631507
- JP HigginsSG ThompsonJJ DeeksDG AltmanMeasuring inconsistency in meta-analysesBMJ2003327741455756010.1136/bmj.327.7414.55712958120
- M BorensteinLV HedgesJ HigginsHR RothsteinA basic introduction to fixed-effect and random-effects models for meta-analysisRes Synth Methods2010129711110.1002/jrsm.1226061376
- CB BeggM MazumdarOperating characteristics of a rank correlation test for publication biasBiometrics199411088110110.2307/2533446
- S DuvalR TweedieTrim and fill: a simple funnel-plot–based method of testing and adjusting for publication bias in meta-analysisBiometrics200056245546310.1111/j.0006-341X.2000.00455.x10877304
- S KimY HongW LewS YangE LeeIncidence of pulmonary tuberculosis among diabeticsTuber Lung Dis199576652953310.1016/0962-8479(95)90529-48593374
- B AlisjahbanaR Van CrevelE SahiratmadjaM Den HeijerA MayaE IstrianaH DanusantosoT OttenhoffR NelwanJ Van Der MeerDiabetes mellitus is strongly associated with tuberculosis in IndonesiaInt J Tuberc Lung Dis200610669670016776459
- KE DooleyT TangJE GolubSE DormanW CroninImpact of diabetes mellitus on treatment outcomes of patients with active tuberculosisAm J Trop Med Hyg200980463463919346391
- JD Goldhaber-FiebertCY JeonT CohenMB MurrayDiabetes mellitus and tuberculosis in countries with high tuberculosis burdens: individual risks and social determinantsInt J Epidemiol201140241742810.1093/ije/dyq23821252210
- A HarriesY LinS SatyanarayanaK LönnrothL LiN WilsonL ChauhanR ZachariahM BakerC JeonThe looming epidemic of diabetes-associated tuberculosis: learning lessons from HIV-associated tuberculosisInt J Tuberc Lung Dis201115111436144510.5588/ijtld.11.050321902876
- A KumarD GuptaSB NagarajaSA NairS SatyanarayanaR ZachariahA HarriesScreening of patients with diabetes mellitus for tuberculosis in IndiaTrop Med Int Health.201318563845
- D PizzolF Di GennaroKD ChhaganlalC FabrizioL MonnoG PutotoA SaracinoTuberculosis and diabetes: current state and future perspectivesTrop Med Int Health201621669470210.1111/tmi.1270427102229
- R SinglaN KhanN Al-SharifM Al-SayeghM ShaikhM OsmanInfluence of diabetes on manifestations and treatment outcome of pulmonary TB patientsInt J Tuberc Lung Dis2006101747916466041
- V ViswanathanS KumpatlaV AravindalochananR RajanC ChinnasamyR SrinivasanJM SelvamA KapurPrevalence of diabetes and pre-diabetes and associated risk factors among tuberculosis patients in IndiaPLoS ONE201277e4136710.1371/journal.pone.004136722848473
- C ZhengM HuF GaoDiabetes and pulmonary tuberculosis: a global overview with special focus on the situation in Asian countries with high TB-DM burdenGlobal Health Action2017101126470210.1080/16549716.2016.1264702
- T SenSR JoshiZF UdwadiaTuberculosis and diabetes mellitus: merging epidemicsJ Assoc Physicians India200957139940419634288
- M SkowrońskiD Zozulińska-ZiółkiewiczA Barinow-WojewódzkiTuberculosis and diabetes mellitus—an underappreciated associationArch Med Sci AMS2014105101910.5114/aoms.2014.4622025395955
- F BacakoğluÖK BaşoğluG ÇokA SayınerM AteşPulmonary tuberculosis in patients with diabetes mellitusRespiration20016859560010.1159/00005057811786714
- J-T ChangH-Y DouC-L YenY-H WuR-M HuangH-J LinI-J SuC-C ShiehEffect 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-resistanceJ Formos Med Assoc2011110637238110.1016/S0929-6646(11)60055-721741005
- Gnanasan S: Pharmaceutical care for patients with tuberculosis and diabetes mellitus in Malaysia: a complex intervention. University of Nottingham; 2012.
- ME Jiménez-CoronaLP Cruz-HervertL García-GarcíaL Ferreyra-ReyesG Delgado-SánchezM Bobadilla-del-ValleS Canizales-QuinteroE Ferreira-GuerreroR Báez-SaldañaN Téllez-VázquezAssociation of diabetes and tuberculosis: impact on treatment and post-treatment outcomesThorax201223250998
- Y-H LinC-P ChenP-Y ChenJ-C HuangC HoH-H WengY-H TsaiY-S PengScreening for pulmonary tuberculosis in type 2 diabetes elderly: a cross-sectional study in a community hospitalBMC Public Health2015151310.1186/1471-2458-15-325572102
- S AminMI KhattakG ShabbierMN WazirFrequency of pulmonary tuberculosis in patients with diabetes mellitusGomal J Med Sci.20129216369
- E WebbA HesselingH SchaafR GieC LombardA SpitaelsS DelportB MaraisK DonaldP HindmarshHigh prevalence of Mycobacterium tuberculosis infection and disease in children and adolescents with type 1 diabetes mellitusInt J Tuberc Lung Dis200913786887419555537
- L-N JiJ-M LuX-H GuoW-Y YangJ-P WengW-P JiaD-J ZouZ-G ZhouD-M YuJ LiuGlycemic control among patients in China with type 2 diabetes mellitus receiving oral drugs or injectablesBMC Public Health201313160210.1186/1471-2458-13-60223800082
- D KibirigeR SsekitolekoE MutebiW WorodriaOvert diabetes mellitus among newly diagnosed Ugandan tuberculosis patients: a cross sectional studyBMC Infect Dis201313112210.1186/1471-2334-13-12223497232
- RA UsmaniMI NasirS WazirZ PervaizT ZahraM AkhtarDiabetes mellitus among tuberculosis patients in a tertiary care hospital of LahoreJ Ayub Med Coll Abbottabad2014261616325358220
- MH WorknehGA BjuneSA YimerPrevalence and associated factors of tuberculosis and diabetes mellitus comorbidity: a systematic reviewPLoS ONE2017124e017592510.1371/journal.pone.017592528430796
- KE DooleyRE ChaissonTuberculosis and diabetes mellitus: convergence of two epidemicsLancet Infect Dis200991273774610.1016/S1473-3099(09)70282-819926034
- N JaftaP JeenaL BarregardR NaidooChildhood tuberculosis and exposure to indoor air pollution: a systematic review and meta-analysisInt J Tuberc Lung Dis201519559660210.5588/ijtld.14.068625868030
- K LönnrothKG CastroJM ChakayaLS ChauhanK FloydP GlaziouMC RaviglioneTuberculosis control and elimination 2010–50: cure, care, and social developmentLancet201037597281814182910.1016/S0140-6736(10)60483-720488524
- World Health OrganizationCollaborative framework for care and control of tuberculosis and diabetes2011GenevaWorld Health Organization
- A ThompsonT BohlingA HeiresJ LinderS RennardLower respiratory tract iron burden is increased in association with cigarette smokingJ Lab Clin Med199111764934992045717
- SE McGowanSA HenleyIron and ferritin contents and distribution in human alveolar macrophagesJ Lab Clin Med198811166116173373107
- S TripathyK KarD ChakrabortyA MajumdarDiabetes mellitus and pulmonary tuberculosis. A prospective studyInd J Tub1984313122125
- A SwaiD McLartyF MugusiTuberculosis in diabetic patients in TanzaniaTrop Doct199020414715010.1177/0049475590020004022284664
- Y FelekeJ AbdulkadirG AderayePrevalence and clinical features of tuberculosis in Ethiopian diabetic patientsEast Afr Med J199976736136410520361
- ASM QayyumA FaroghPrevalence of pulmonary tuberculosis among diabeticsBiomedical2004206873
- A JabbarS HussainA KhanClinical characteristics of pulmonary tuberculosis in adult Pakistani patients with co-existing diabetes mellitusEast Mediterr Health J200612552252717333789
- N KiruiS PastakiaJ KamanoS ChengE ManuthuP ChegeA GardnerA MwangiD EnarsonA ReidImportant co-morbidity in patients with diabetes mellitus in three clinics in Western KenyaPublic Health Action20122414815110.5588/pha.12.003126392975
- MV JaliVK MahishaleMB HiremathBidirectional screening of tuberculosis patients for diabetes mellitus and diabetes patients for tuberculosisDiabetes Metab J201337429129510.4093/dmj.2013.37.4.29123991408
- S KumpatlaA SekarS AchantaB SharathA KumarA HarriesV ViswanathanCharacteristics of patients with diabetes screened for tuberculosis in a tertiary care hospital in South IndiaPublic Health Action201331232810.5588/pha.13.003526392991
- B PrakashK RavishB PrabhakarT RanganathB NaikS SatyanarayanaP IsaakidisA KumarTuberculosis-diabetes mellitus bidirectional screening at a tertiary care centre, South IndiaPublic Health Action201331182210.5588/pha.13.0032
- MS RaoM ShridharK PavaniV VE DS: screening of tuberculosis in diabetic patients at a tertiary care hospital in HyderabadIndian J Microbiol Res20152422022610.5958/2394-5478.2015.00018.7