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Table of Contents
Vol. 68, No. 6, 2001
Issue release date: November–December 2001
Section title: Clinical Investigations
Respiration 2001;68:595–600
(DOI:10.1159/000050578)

Pulmonary Tuberculosis in Patients with Diabetes mellitus

Bacakoğlu F. · Başoğlu Ö. · Çok G. · Sayıner A. · Ateş M.
Department of Chest Diseases, Ege University Medical School, Izmir, Turkey
email Corresponding Author

Abstract

Background: Diabetes mellitus has been reported to modify the presenting features of pulmonary tuberculosis, but there are varying data, particularly regarding the association with lower lung field involvement. Objectives: To determine whether diabetes mellitus alters the clinical and radiographic manifestations of tuberculosis in nonimmunocompromised hosts and to define the determinants of lower lung field involvement. Methods: A retrospective review of the records of all patients with tuberculosis and diabetes mellitus seen during a 14-year period and of an age- and sex-matched nondiabetic control group with tuberculosis was carried out. The duration of symptoms, tuberculin reaction, bacteriologic and radiographic findings of the two groups were compared. Results: The presence of diabetes mellitus was found not to have an effect on patients’ symptomatology, bacteriology results, tuberculin reaction and localization of pulmonary infiltrates. On the other hand, fewer diabetic patients were smear-positive and fewer had reticulonodular opacities compared with the control patients. A higher number of insulin-dependent diabetic patients presented with cavitary disease as compared with nondiabetic controls. Lower lung field tuberculosis was significantly associated with female gender and, in patients older than 40 years, was more frequently observed in diabetics. Conclusion: These data show that diabetes does not affect the presenting features of pulmonary tuberculosis to a large extent and is only associated with lower lung field disease in older patients.

© 2001 S. Karger AG, Basel


  

Key Words

  • Tuberculosis
  • Diabetes mellitus, insulin-dependent
  • Radiography
  • Cavity
  • Bacteriology

 introduction

The relationship between diabetes mellitus (DM) and pulmonary tuberculosis has attracted the interest of many clinicians and investigators for a long time. Many studies have shown that the prevalence of tuberculosis among diabetics is 2–5 times higher than in the nondiabetic population [1, 2]. On the other hand, there appears to be little information on whether DM affects the diagnostic findings in tuberculosis.

The radiographic manifestations of tuberculosis may differ from the findings in nondiabetic controls as was initially reported by Sosman and Steidl [3], who found a higher rate of lower lung field (LLF) involvement in their diabetic patients. This was followed by other studies which reported rates ranging between 3.4 and 32.2% [4, 5, 6, 7, 8]. These were, on the other hand, mainly uncontrolled, descriptive studies and have not been confirmed by more recent reports which included control groups. Instead, some of the latter studies showed higher prevalences of multilobar involvement and of cavitary disease [8, 9, 10, 11, 12]. It is as yet difficult to draw definitive conclusions from the literature because of the varying findings in the reported studies done on relatively small populations. There is even less data on clinical and microbiologic findings and on tuberculin reactivity in diabetic patients.

The aims of this study were to determine whether DM alters the clinical and radiographic manifestations of tuberculosis in nonimmunocompromised hosts and to define the determinants of LLF involvement. We thus retrospectively reviewed the findings of patients with tuberculosis and diabetes hospitalized in our department during the last 14 years and compared them with those of an age- and sex-matched nondiabetic control group. We also further examined the patients with tuberculosis involving the LLF so as to identify whether there was any difference in these patients’ characteristics, clinical course and other radiographic features.

 

 material and methods


 study population

A review of the records of all patients admitted to our department, a 105-bed department for chest diseases in a 1,600-bed university hospital, between 1985 and 1998 disclosed 927 cases with culture-positive pulmonary tuberculosis, i.e. ‘definite’ cases, as defined by Rieder et al. [13]. All patients were hospitalized for 1–4 weeks, which is an institutional policy. This period includes educational sessions on the treatment and social aspects of the disease and facilitates early control of compliance with therapy.

One hundred and fourteen of the patients (12.3%) were found to have concomitant DM. The files were retrieved from the department archives and 22 patients were excluded because either the radiogram done at the first presentation was missing or there was no clear data on bacteriology and history of DM, as radiographic and bacteriologic findings were the main parameters that this study investigated in patients with and without diabetes. These were, therefore, not examined and 92 cases were finally included as the study group (group 1).

Patients were included in the DM group if they had a previous history of DM and had been receiving insulin and/or an oral hypoglycemic agent at the time of hospital admission or were found to have two or more fasting blood glucose levels greater than 140 mg/dl and were thus started on antidiabetic treatment. An age- and sex-matched group of 92 cases, who were hospitalized in the same period and who did not have DM, was chosen as the control group (group 2). None of the patients in the study or control groups was HIV-positive. Patients who had been receiving immunosuppressive treatment or corticosteroids during the 6 months preceding the diagnosis of tuberculosis were excluded from analysis.

 reviewed parameters

Upon examination of the patients’ files, the following parameters were recorded and comparisons were made between the two groups: symptoms and their duration, smear and culture positivity, resistance to antituberculosis drugs, interval at which the sputum culture became negative, tuberculin skin test reactivity as measured by the Mantoux method [14], radiographic features including localization and characteristics of the infiltrates, presence of pleural involvement, duration of hospitalization and treatment.

 radiographic interpretation

The data on radiographic findings were collected using the P-A roentgenograms obtained at the time of diagnosis. The X-rays were read by two of the investigators (G.C., A.S.) who remained blinded to the presence or absence of diabetes. Localizations of the infiltrates were interpreted using two different classifications. First, in compliance with the usual clinical approach, the upper, mid and lower zones were defined to be separated by imaginary horizontal lines passing at the level of the anterior ends of the second and fourth ribs, respectively. The LLF was separately defined as the area below an imaginary line traced across the hila and including the parahilar regions on a standard posteroanterior chest roentgenogram. This was to allow comparisons to be made with previous reports that used the same definition [4, 15].

 treatment of tuberculosis

The usual treatment regimen consisted of an initial phase of isoniazid, rifampin, pyrazinamide, and streptomycin or ethambutol given daily for 2 months followed by isoniazid and rifampin for 7 months. This standard regimen was modified or extended depending on the rate of response and the presence of drug resistance.

 analysis

Student’s t test was used to compare the ages, durations of symptoms and of treatment, and time to sputum conversion. =χ2 test was done to determine the significance of the differences in sex, symptoms, tuberculin positivity, smear positivity, drug resistance and radiographic characteristics. Unless otherwise stated, all data are expressed as mean ± SD. A p value of less than 0.05 was considered significant.

 

 results

The demographic data of the study and control groups (groups 1 and 2, respectively) are presented in table 1. There was no difference between the two groups regarding the prevalence of symptoms. Group 1 had a shorter duration of symptoms, but it was found not to be statistically significant (p = 0.16).

TAB01

Table 1. Demographic data of the study and control groups

 history and treatment of dm

By definition, none of the cases in the control group was diagnosed to have DM, nor was hyperglycemia detected in the routine biochemistry workup.

Fifty-nine patients (64.1%) in the study group had prior diagnosis of DM of 1–22 years’ duration (mean 6.8 ± 8.9 years). In 33 cases (35.9%), it was diagnosed when they were admitted to hospital for tuberculosis and they continued to receive medication for DM for at least 1 year. Twenty-one cases required insulin treatment for the control of hyperglycemia (type 1, insulin-dependent), whereas the remaining 71 cases were controlled with oral hypoglycemic agents (type 2, non-insulin-dependent). These cases had a diabetes history of 13.0 ± 13.6 years (0–15) and 5.0 ± 4.2 years (0–22), respectively (p < 0.01).

One patient in group 1 also had lung cancer. In group 2, lung cancer and breast cancer were found in 1 patient each (table 1).

 bacteriology

By definition, tuberculosis was proven in all cases by positive cultures for Mycobacterium tuberculosis. The smears were positive for acid-fast bacilli in 67 cases (72.8%) and 84 cases (91.3%) in groups 1 and 2, respectively (p < 0.01). There was no difference between the study and control groups regarding the time taken for the sputum culture to become negative and drug resistance rates (table 2).

TAB02

Table 2. Results of bacteriology and tuberculin test in the study and control groups

 tuberculin test results

Tuberculin skin test was performed on 62 cases (67.4%) in the diabetic group (group 1) and 65 cases (70.7%) in the control group (group 2). It was found to be positive in 48 cases (77.4%) and 50 cases (76.9%) in the two groups, respectively.

 radiographic findings

Fewer cases in group 1 (11/92, 12.0%) had upper-zone involvement only compared with group 2 (16/92 cases, 17.4%), but the difference was not statistically significant (p = 0.30). Similarly, there was a higher number of cases in group 1 with only LLF involvement (20/92 cases, 21.7% vs. 13/92 cases, 14.1%), but this again did not reach statistical significance (p = 0.18).

There was no difference between the two groups regarding the radiographic involvement of the lung zones. The radiographic features including the prevalences of acinar opacities, cavities and pleural thickening were again similar in the two groups, but significantly fewer patients in the diabetes group presented with reticulonodular opacities (table 3).

TAB03

Table 3. Radiographic findings in the study and control groups

In the diabetic group, 21 cases (22.8%) were insulin-dependent (type 1) and 71 cases were non-insulin-dependent (type 2). The clinical features of these two subgroups are presented in table 4 and the radiographic characteristics in table 5. No significant difference was found between these two subgroups of diabetic patients. However, when compared with nondiabetic controls, type 1 DM patients presented with cavitary disease significantly more frequently (76.2 vs. 51.1%, respectively, p = 0.037).

TAB04

Table 4. Characteristics of cases with DM

TAB05

Table 5. Radiographic features of patients with DM

 characteristics of patients with llf tuberculosis

A total of 33 cases (17.9%) had LLF tuberculosis only, i.e. without the involvement of other fields. This was more frequently observed in female patients (p < 0.001), but was not related to the presence of DM (p = 0.18). However, DM was significantly associated with LLF disease in older patients. Thus, among patients older than 40 years, LLF disease was more frequently observed in diabetics (17/81, 21.0%) as compared to nondiabetics (4/61, 6.6%; p = 0.031).

None of the cases presenting with LLF tuberculosis had reticulonodular opacities. The comparisons of the clinical and radiographic findings of these patients with the findings of cases without LLF disease are shown in tables 6 and 7.

TAB06

Table 6. Characteristics of cases with LLF tuberculosis only

TAB07

Table 7. Radiographic features of patients with LLF tuberculosis only

 

 discussion

The association of tuberculosis and DM has attracted the attention of clinicians for years. The incidence of diabetes among tuberculosis cases reviewed in this study, 12.3%, is similar to those rates previously reported, 2.1 and 13.2% [16, 17], and is markedly higher than in the general population. With this retrospective review of patients’ records, we aimed to provide information regarding the clinical and radiographic manifestations of this association.

This study, which included a matched control group of nondiabetic patients, showed that DM did not alter the symptomatology, tuberculin reactivity, the rate of drug resistance and the response to antituberculosis therapy. It also did not affect the radiographic localization of pulmonary infiltrates, except that LLF involvement was significantly associated with DM in patients older than 40 years and with female gender. The higher prevalence in women has been consistently reported in other studies [4, 16, 18]. Besides, two significant differences were detected between tuberculosis patients with and without DM, i.e. the prevalences of smear-positive cases and of reticulonodular opacities were lower in the former group.

Early studies on the radiographic findings of tuberculosis patients with DM reported atypical localization patterns, namely an increased incidence of LLF involvement that ranged between 8.1 and 29% [5, 8, 12]. More recent reports did not confirm these observations [8, 12, 17, 18]; instead, some found higher rates of multilobar involvement [12, 19, 20], which was not confirmed in this study. In the largest series on clinical findings in tuberculosis, Aktoğu et al. [16] also found a higher rate of LLF tuberculosis among diabetics as compared with nondiabetics (11.0 and 5.3%, respectively). This was a retrospective review of all tuberculosis cases, however, and was not designed for this purpose. The two groups were not matched and they possibly included immunocompromised hosts.

In our study, although there was a tendency for an increased prevalence of LLF disease in diabetics, this was not statistically significant. However, age was found to be an important determinant of the relationship between DM and LLF disease; LLF involvement was significantly associated with DM only in patients older than 40 years. This is partly in accordance with recent reports on the more frequent occurrence of unusual presentations in older age groups [18, 21]. This effect of age may explain the differences in the results of previous studies which might have included populations with varying ages.

A similar controversy exists as regards the prevalence of cavitary disease in diabetics. Studies that reported a higher rate [12, 20, 22] have not been confirmed by others [8, 19]. In the present study, although diabetics and nondiabetics had similar rates of cavitary disease, a significantly higher rate was observed in tuberculosis patients with type 1 DM. Differences in the composition of diabetic patients (type 1 vs. type 2), therefore, may have been the reason for the contradictory results in previous studies.

An interesting finding was the presence of increasing cavitation together with decreased smear positivity in the diabetic group. Cavitary disease is expected to be associated with a larger population of bacilli and we speculate that this finding might be related with the muscle weakness caused by uncontrolled glycemia, leading to less effective expectoration.

Lower rates of reticulonodular opacities were observed in patients with DM and in cases with LLF involvement. This may be evaluated in conjunction with the finding that these patients had somewhat shorter durations of symptoms, although they were not found to be statistically significant. A more acute onset has been observed and reported by others [7] in LLF disease. It may perhaps be speculated that a shorter duration of disease enables earlier diagnosis, leading to a less frequent occurrence of fibronodular opacities and a lower incidence of positive smears in microscopic examination.

Whether the type of diabetes influences the clinical and radiographic presentation of tuberculosis is another issue, on which there is little data in the literature. Poorly controlled hyperglycemia is usually considered to be the main factor causing increased susceptibility to infections [23] and thus insulin-dependent diabetics are expected to be more frequently or severely affected. One study published in Russian showed that type 1 diabetes has a more acute onset and runs a more symptomatic course compared with type 2 disease [24], but no data can be obtained from the abstract as to the glycemia level, gender, age and immune status of the two groups. The present study documented that similar findings are observed in these two groups of diabetic patients, except for the higher rate of cavitary disease in type 1 disease as compared to nondiabetics.

In conclusion, diabetes does not affect the clinical and radiographic presentation of tuberculosis to a significant extent. However, age appears to be a determinant of the effects of DM on tuberculosis presentation, in that LLF tuberculosis occurs more frequently in patients with DM who are older than 40 years when compared to nondiabetic patients. It is also significantly associated with the female gender.


References

  1. Turner WM: Pulmonary tuberculosis and diabetes mellitus. Q J Med 1951;26:31.
  2. Opsald R, Riddervald HO, Aas TW: Pulmonary tuberculosis in mitral stenosis and diabetes. Acta Tuberc Scand 1961;4:290.
  3. Sosman MC, Steidl JH: Diabetic tuberculosis. Am J Roentgenol 1927;17:625.
  4. Parmer M: Lower lung field tuberculosis. Am Rev Respir Dis 1969;96:310–313.
  5. Weaver R: Unusual radiographic presentation of pulmonary tuberculosis in diabetic patients. Am Rev Respir Dis 1974;109:162–163.

    External Resources

  6. Zack MB, Fulkerson LL, Stein E: Glucose intolerance in pulmonary tuberculosis. Am Rev Respir Dis 1973;108:1164–1169.

    External Resources

  7. Berger HW, Granada MG: Lower lung field tuberculosis. Chest 1974;5:522–526.
  8. Morris JT, Seaworth BJ, McAllister CK: Pulmonary tuberculosis in diabetics. Chest 1992;102:539–541.

    External Resources

  9. Olmos P, Donoso J, Rojas N, Meza M, Martinez C: Tuberculosis and diabetes mellitus: A longitudinal-retrospective study in a teaching hospital. Rev Med Chil 1989;117:979–983.

    External Resources

  10. Smurova TF, Egorova IL: Endocrine disorders and principles of their correction in patients with pulmonary tuberculosis and concomitant diabetes mellitus. Probl Tuberk 1991;5:31–33.

    External Resources

  11. Swai AB, McLarty DG, Mugusi F: Tuberculosis in diabetic patients in Tanzania. Trop Doct 1990;20:147–150.

    External Resources

  12. Umut S, Tosun GA, Yildirim N: Radiographic location of pulmonary tuberculosis in diabetic patients. Chest 1994;106:326.
  13. Rieder HL, Wastson JM, Raviglione MC, Forssbohm M, Migliori GB, Schwoeber V, Leitch AG, Zellweger J-P: Surveillance of tuberculosis in Europe. Eur Respir J 1996;9:1097–1104.
  14. Bloch AB: Screening for tuberculosis and tuberculosis infection; in Fishman AP (ed): Fishman’s Pulmonary Diseases and Disorders. New York, McGraw-Hill, 1998, pp 2473–2481.
  15. Segarra F, Sherman DS, Rodriguez-Aguero J: Lower lung field tuberculosis. Am Rev Respir Dis 1963;87:37–40.
  16. Aktogu S, Yorgancioglu A, Cirak K, Kose T, Dereli SM: Clinical spectrum of pulmonary and pleural tuberculosis: A report of 5480 cases. Eur Respir J 1996;9:2031–2035.
  17. Yamagishi F, Suzuki K, Sasaki Y, Saitoh M, Izumizaki M, Koizumi K: Prevalence of coexisting diabetes mellitus among patients with active pulmonary tuberculosis. Kekkaku 1996;71:569–572.
  18. Chang SC, Lee PY, Perng RP: Lower lung field tuberculosis. Chest 1987;91:230–232.
  19. al-Wabel AH, Teklu B, Mahfouz AA, al-Ghamdi AS, el-Amin OB, Khan AS: Symptomatology and chest roentgenographic changes of pulmonary tuberculosis among diabetics. East Afr Med J 1997;74:62–64.

    External Resources

  20. Ekim NN, Cilli A, Guz G, Arslan M: Pulmonary tuberculosis in diabetic patients. Tuber Lung Dis 1995;76(suppl 2):28.
  21. Van den Brande P, Dockx S, Valck B, Demedts M: Pulmonary tuberculosis in the adult in a low prevalence area: Is the radiological presentation changing? Int J Tuberc Lung Dis 1998;2:904–908.
  22. 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;162:1738–1740.

    External Resources

  23. McMahon MM, Bistrian BR: Host defenses and susceptibility to infection in patients with diabetes mellitus. Infect Dis Clin North Am 1995;9:1–9.
  24. Karachunskii MA, Kossii IUE, Iakovleva OB: Clinical symptoms and course of pulmonary tuberculosis in patients with various types of diabetes mellitus. Probl Tuberk 1993;4:20–21.

    External Resources

  

Author Contacts

Dr. Abdullah Sayıner
Ege Üniversitesi Tıp Fakültesi Göğüs Hastalıkları A.D.
TR–35100 Bornova, Izmir (Turkey)
Tel. +90 232 388 1423, Fax +90 232 388 7192, E-Mail asayiner@med.ege.edu.tr

  

Article Information

Received: Received: November 13, 2000
Accepted after revision: April 24, 2001
Number of Print Pages : 6
Number of Figures : 0, Number of Tables : 7, Number of References : 24

  

Publication Details

Respiration (International Review of Thoracic Diseases)
Founded 1944 as ‘Schweizerische Zeitschrift für Tuberkulose und Pneumonologie’ by E. Bachmann, M. Gilbert, F. Häberlin, W. Löffler, P. Steiner and E. Uehlinger, continued 1962–1967 as ‘Medicina Thoracalis’

Vol. 68, No. 6, Year 2001 (Cover Date: November-December 2001)

Journal Editor: C.T. Bolliger, Cape Town
ISSN: 0025–7931 (print), 1423–0356 (Online)

For additional information: http://www.karger.com/journals/res


Copyright / Drug Dosage / Disclaimer

Copyright: All rights reserved. No part of this publication may be translated into other languages, reproduced or utilized in any form or by any means, electronic or mechanical, including photocopying, recording, microcopying, or by any information storage and retrieval system, without permission in writing from the publisher or, in the case of photocopying, direct payment of a specified fee to the Copyright Clearance Center.
Drug Dosage: The authors and the publisher have exerted every effort to ensure that drug selection and dosage set forth in this text are in accord with current recommendations and practice at the time of publication. However, in view of ongoing research, changes in goverment regulations, and the constant flow of information relating to drug therapy and drug reactions, the reader is urged to check the package insert for each drug for any changes in indications and dosage and for added warnings and precautions. This is particularly important when the recommended agent is a new and/or infrequently employed drug.
Disclaimer: The statements, opinions and data contained in this publication are solely those of the individual authors and contributors and not of the publishers and the editor(s). The appearance of advertisements or/and product references in the publication is not a warranty, endorsement, or approval of the products or services advertised or of their effectiveness, quality or safety. The publisher and the editor(s) disclaim responsibility for any injury to persons or property resulting from any ideas, methods, instructions or products referred to in the content or advertisements.

Abstract

Background: Diabetes mellitus has been reported to modify the presenting features of pulmonary tuberculosis, but there are varying data, particularly regarding the association with lower lung field involvement. Objectives: To determine whether diabetes mellitus alters the clinical and radiographic manifestations of tuberculosis in nonimmunocompromised hosts and to define the determinants of lower lung field involvement. Methods: A retrospective review of the records of all patients with tuberculosis and diabetes mellitus seen during a 14-year period and of an age- and sex-matched nondiabetic control group with tuberculosis was carried out. The duration of symptoms, tuberculin reaction, bacteriologic and radiographic findings of the two groups were compared. Results: The presence of diabetes mellitus was found not to have an effect on patients’ symptomatology, bacteriology results, tuberculin reaction and localization of pulmonary infiltrates. On the other hand, fewer diabetic patients were smear-positive and fewer had reticulonodular opacities compared with the control patients. A higher number of insulin-dependent diabetic patients presented with cavitary disease as compared with nondiabetic controls. Lower lung field tuberculosis was significantly associated with female gender and, in patients older than 40 years, was more frequently observed in diabetics. Conclusion: These data show that diabetes does not affect the presenting features of pulmonary tuberculosis to a large extent and is only associated with lower lung field disease in older patients.

© 2001 S. Karger AG, Basel


  

Author Contacts

Dr. Abdullah Sayıner
Ege Üniversitesi Tıp Fakültesi Göğüs Hastalıkları A.D.
TR–35100 Bornova, Izmir (Turkey)
Tel. +90 232 388 1423, Fax +90 232 388 7192, E-Mail asayiner@med.ege.edu.tr

  

Article Information

Received: Received: November 13, 2000
Accepted after revision: April 24, 2001
Number of Print Pages : 6
Number of Figures : 0, Number of Tables : 7, Number of References : 24

  

Publication Details

Respiration (International Review of Thoracic Diseases)
Founded 1944 as ‘Schweizerische Zeitschrift für Tuberkulose und Pneumonologie’ by E. Bachmann, M. Gilbert, F. Häberlin, W. Löffler, P. Steiner and E. Uehlinger, continued 1962–1967 as ‘Medicina Thoracalis’

Vol. 68, No. 6, Year 2001 (Cover Date: November-December 2001)

Journal Editor: C.T. Bolliger, Cape Town
ISSN: 0025–7931 (print), 1423–0356 (Online)

For additional information: http://www.karger.com/journals/res


Article / Publication Details

First-Page Preview
Abstract of Clinical Investigations

Published online: 12/21/2001
Issue release date: November–December 2001

Number of Print Pages: 6
Number of Figures: 0
Number of Tables: 7

ISSN: 0025-7931 (Print)
eISSN: 1423-0356 (Online)

For additional information: http://www.karger.com/RES


Copyright / Drug Dosage

Copyright: All rights reserved. No part of this publication may be translated into other languages, reproduced or utilized in any form or by any means, electronic or mechanical, including photocopying, recording, microcopying, or by any information storage and retrieval system, without permission in writing from the publisher or, in the case of photocopying, direct payment of a specified fee to the Copyright Clearance Center.
Drug Dosage: The authors and the publisher have exerted every effort to ensure that drug selection and dosage set forth in this text are in accord with current recommendations and practice at the time of publication. However, in view of ongoing research, changes in goverment regulations, and the constant flow of information relating to drug therapy and drug reactions, the reader is urged to check the package insert for each drug for any changes in indications and dosage and for added warnings and precautions. This is particularly important when the recommended agent is a new and/or infrequently employed drug.
Disclaimer: The statements, opinions and data contained in this publication are solely those of the individual authors and contributors and not of the publishers and the editor(s). The appearance of advertisements or/and product references in the publication is not a warranty, endorsement, or approval of the products or services advertised or of their effectiveness, quality or safety. The publisher and the editor(s) disclaim responsibility for any injury to persons or property resulting from any ideas, methods, instructions or products referred to in the content or advertisements.

References

  1. Turner WM: Pulmonary tuberculosis and diabetes mellitus. Q J Med 1951;26:31.
  2. Opsald R, Riddervald HO, Aas TW: Pulmonary tuberculosis in mitral stenosis and diabetes. Acta Tuberc Scand 1961;4:290.
  3. Sosman MC, Steidl JH: Diabetic tuberculosis. Am J Roentgenol 1927;17:625.
  4. Parmer M: Lower lung field tuberculosis. Am Rev Respir Dis 1969;96:310–313.
  5. Weaver R: Unusual radiographic presentation of pulmonary tuberculosis in diabetic patients. Am Rev Respir Dis 1974;109:162–163.

    External Resources

  6. Zack MB, Fulkerson LL, Stein E: Glucose intolerance in pulmonary tuberculosis. Am Rev Respir Dis 1973;108:1164–1169.

    External Resources

  7. Berger HW, Granada MG: Lower lung field tuberculosis. Chest 1974;5:522–526.
  8. Morris JT, Seaworth BJ, McAllister CK: Pulmonary tuberculosis in diabetics. Chest 1992;102:539–541.

    External Resources

  9. Olmos P, Donoso J, Rojas N, Meza M, Martinez C: Tuberculosis and diabetes mellitus: A longitudinal-retrospective study in a teaching hospital. Rev Med Chil 1989;117:979–983.

    External Resources

  10. Smurova TF, Egorova IL: Endocrine disorders and principles of their correction in patients with pulmonary tuberculosis and concomitant diabetes mellitus. Probl Tuberk 1991;5:31–33.

    External Resources

  11. Swai AB, McLarty DG, Mugusi F: Tuberculosis in diabetic patients in Tanzania. Trop Doct 1990;20:147–150.

    External Resources

  12. Umut S, Tosun GA, Yildirim N: Radiographic location of pulmonary tuberculosis in diabetic patients. Chest 1994;106:326.
  13. Rieder HL, Wastson JM, Raviglione MC, Forssbohm M, Migliori GB, Schwoeber V, Leitch AG, Zellweger J-P: Surveillance of tuberculosis in Europe. Eur Respir J 1996;9:1097–1104.
  14. Bloch AB: Screening for tuberculosis and tuberculosis infection; in Fishman AP (ed): Fishman’s Pulmonary Diseases and Disorders. New York, McGraw-Hill, 1998, pp 2473–2481.
  15. Segarra F, Sherman DS, Rodriguez-Aguero J: Lower lung field tuberculosis. Am Rev Respir Dis 1963;87:37–40.
  16. Aktogu S, Yorgancioglu A, Cirak K, Kose T, Dereli SM: Clinical spectrum of pulmonary and pleural tuberculosis: A report of 5480 cases. Eur Respir J 1996;9:2031–2035.
  17. Yamagishi F, Suzuki K, Sasaki Y, Saitoh M, Izumizaki M, Koizumi K: Prevalence of coexisting diabetes mellitus among patients with active pulmonary tuberculosis. Kekkaku 1996;71:569–572.
  18. Chang SC, Lee PY, Perng RP: Lower lung field tuberculosis. Chest 1987;91:230–232.
  19. al-Wabel AH, Teklu B, Mahfouz AA, al-Ghamdi AS, el-Amin OB, Khan AS: Symptomatology and chest roentgenographic changes of pulmonary tuberculosis among diabetics. East Afr Med J 1997;74:62–64.

    External Resources

  20. Ekim NN, Cilli A, Guz G, Arslan M: Pulmonary tuberculosis in diabetic patients. Tuber Lung Dis 1995;76(suppl 2):28.
  21. Van den Brande P, Dockx S, Valck B, Demedts M: Pulmonary tuberculosis in the adult in a low prevalence area: Is the radiological presentation changing? Int J Tuberc Lung Dis 1998;2:904–908.
  22. 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;162:1738–1740.

    External Resources

  23. McMahon MM, Bistrian BR: Host defenses and susceptibility to infection in patients with diabetes mellitus. Infect Dis Clin North Am 1995;9:1–9.
  24. Karachunskii MA, Kossii IUE, Iakovleva OB: Clinical symptoms and course of pulmonary tuberculosis in patients with various types of diabetes mellitus. Probl Tuberk 1993;4:20–21.

    External Resources