Demographic and microbiological characteristics of tuberculous lymphadenitis and other extrapulmonary tuberculosis cases

Abstract

Objective: Tuberculosis (TB) is a significant public health problem that remains important worldwide. This study aimed to examine the demographic characteristics and clinical features of patients with extrapulmonary tuberculosis (EPTB) and also identify the comorbidities of EPTB. Our secondary aim was to compare tuberculous lymphadenitis (TBL) with other forms of EPTB. Patients and Methods: This single-center, retrospective, observational study was conducted on patients diagnosed with EPTB in a training hospital in Turkey between January 1, 2011 and December 31, 2020. The demographic characteristics and clinical features of the patients were examined. TBL cases were compared with other forms of EPTB cases. Results: The most common clinical form was TBL. Fever, night sweats, and accelerated erythrocyte sedimentation rate were significantly more common in the other forms of the EPTB group compared to TBL. The rate of tuberculin skin test positivity was significantly higher in patients with TBL. The complication rate was 3%, and mortality rate was 4% among all patients. Conclusions: Extrapulmonary tuberculosis should be considered in the differential diagnosis by evaluating the medical history of patients who present with organ-specific symptoms, especially in TB endemic countries. The clinic may differ according to the organ involvement. TBL may be seen with milder symptoms compared to other clinical forms.

Keywords

• Extra pulmonary tuberculosis
• Tuberculous lymphadenitis
• Mycobacterium tuberculosis

References

1. World Health Organization [WHO]. Cause specific mortality. https://www.who.int/data/gho/data/themes/mortalityand- global-health-estimates/ghe-leading-causes-of-death. Accessed: 10 March 2022.
2. World Health Organization [WHO]. Global tuberculosis report 2021. https://www.who.int/publications/digital/globaltuberculosis- report-2021. Accessed: 10 March 2022
3. T.C Ministry of Health. Istatistics of tuberculosis. https:// hsgm.saglik.gov.tr/tr/tuberkuloz-istatistikler. Accessed: 10 March 2022
4. Holden IK, Lillebaek T, Andersen PH, Bjerrum S, Wejse C, Johansen IS. Extrapulmonary tuberculosis in Denmark from 2009 to 2014; Characteristics and predictors for treatment outcome. Open Forum Infect Dis 2019;6:ofz388. doi: 10.1093/ ofid/ofz388.
5. Cukic V, Ustamujic A. Extrapulmonary tuberculosis in Federation of Bosnia and Herzegovina. Mater Sociomed 2018;30:153-6. doi: 10.5455/msm.2018.30.153-156.
6. Natali D, Cloatre G, Brosset C, et al. What pulmonologists need to know about extrapulmonary tuberculosis. Breathe (Sheff) 2020;16:200216. doi: 10.1183/20734.735.0216-2020.
7. Peto HM, Pratt RH, Harrington TA, LoBue PA, Armstrong LR. Epidemiology of extrapulmonary tuberculosis in the United States, 1993-2006. Clin Infect Dis 2009;49:1350-7. doi: 10.1086/605559.
8. Sama JN, Chida N, Polan RM, Nuzzo J, Page K, Shah M. High proportion of extrapulmonary tuberculosis in a low prevalence setting: a retrospective cohort study. Public Health 2016;138:101-7. doi: 10.1016/j.puhe.2016.03.033.

9. Sandgren A, Hollo V, van der Werf MJ. Extrapulmonary tuberculosis in the European Union and European Economic Area, 2002 to 2011. Euro Surveill 2013;18:20431.
10. Norbis L, Alagna R, Tortoli E, Codecasa LR, Migliori GB, Cirillo DM. Challenges and perspectives in the diagnosis of extrapulmonary tuberculosis. Expert Rev Anti Infect Ther 2014;12:633-47. doi: 10.1586/14787.210.2014.899900.
11. World Health Organization (2013). Using the Xpert MTB/RIF assay to detect pulmonary and extrapulmonary tuberculosis and rifampicin resistance in adults and children: expert group meeting report: 2013 (No. WHO/HTM/TB/2013.14).
12. Deveci HS, Kule M, Kule ZA, Habesoglu TE. Diagnostic challenges in cervical tuberculous lymphadenitis: A review. North Clin Istanb 2016;3:150-5. doi: 10.14744/nci.2016.20982.
13. Bauer CM, Schmähl A, Kreuter M. Bildgebung und Labordiagnostik bei Tuberkulose [Imaging and Laboratory Diagnostics for Tuberculosis]. Klin Monbl Augenheilkd. 2016;233:587-93. doi: 10.1055/s-0042-104062.
14. Nhlema S, Kemp J, Steenbergen S, Theobald S, Tang S, Squire S. Asystematic analysis of TB and poverty. Technical Paper Commissioned by the STOP TB Partnership. Geneva: World Health Organization; 2003.
15. Antunes JL, Waldman EA. The impact of AIDS, immigration and housing overcrowding on tuberculosis deaths in São Paulo, Brazil, 1994-1998. Soc Sci Med 2001;52:1071-80. doi: 10.1016/s0277-9536(00)00214-8.
16. Wandwalo ER, Mørkve O. Delay in tuberculosis case-finding and treatment in Mwanza, Tanzania. Int J Tuberc Lung Dis 2000;4:133-8.
17. Targeted tuberculin testing and treatment of latent tuberculosis infection. This official statement of the American Thoracic Society was adopted by the ATS Board of Directors, July 1999. This is a Joint Statement of the American Thoracic Society (ATS) and the Centers for Disease Control and Prevention (CDC). This statement was endorsed by the Council of the Infectious Diseases Society of America. (IDSA), September 1999, and the sections of this statement. Am J Respir Crit Care Med 2000;161(4 Pt 2):S221-47. doi: 10.1164/ajrccm.161. supplement_3.ats600.
18. Kamboj M, Sepkowitz KA. The risk of tuberculosis in patients with cancer. Clin Infect Dis 2006;42:1592-5. doi: 10.1086/503917.
19. Sreeramareddy CT, Panduru KV, Verma SC, Joshi HS, Bates MN. Comparison of pulmonary and extrapulmonary tuberculosis in Nepal – a hospital-based retrospective study. BMC Infect Dis 2008;8:8. doi: 10.1186/1471-2334-8-8.
20. Djannah F, Massi MN, Hatta M, Bukhari A, Hasanah I. Profile and histopathology features of top three cases of Extra Pulmonary Tuberculosis (EPTB) in West Nusa Tenggara: A retrospective cross-sectional study. Ann Med Surg (Lond) 2022;75:103318. doi: 10.1016/j.amsu.2022.103318.
21. Khan AH, Sulaiman SAS, Laghari M, et al. Treatment outcomes and risk factors of extra-pulmonary tuberculosis in patients with co-morbidities. BMC Infect Dis. 2019;19:691. doi: 10.1186/s12879.019.4312-9.
22. Forssbohm M, Zwahlen M, Loddenkemper R, Rieder HL. Demographic characteristics of patients with extrapulmonary tuberculosis in Germany. Eur Respir J 2008;31:99-105. doi: 10.1183/09031.936.00020607.
23. Rieder HL, Snider DE Jr, Cauthen GM. Extrapulmonary tuberculosis in the United States. Am Rev Respir Dis 1990;141:347-51. doi: 10.1164/ajrccm/141.2.347.
24. Oztop A, Unsal I, Gunay T, et al. The study of evaluation of tuberculous patients who registered in Kahramanlar tuberculous struggle dispensary. Tuberk Toraks 2000;48:243- 7. doi: 10.1159/000365511.
25. Guler SA, Bozkus F, Inci MF, et al. Evaluation of pulmonary and extrapulmonary tuberculosis in immunocompetent adults: a retrospective case series analysis. Med Princ Pract 2015;24:75-9. doi: 10.1159/000365511.
26. Cailhol J, Decludt B, Che D. Sociodemographic factors that contribute to the development of extrapulmonary tuberculosis were identified. J Clin Epidemiol 2005;58:1066-71. doi: 10.1016/j.jclinepi.2005.02.023.
27. Kang W, Yu J, Du J, et al. The epidemiology of extrapulmonary tuberculosis in China: A large-scale multi-center observational study. PLoS One 2020;15:e0237753. doi: 10.1371/journal. pone.0237753.
28. Gunal S, Yang Z, Agarwal M, Koroglu M, Arıcı ZK, Durmaz R. Demographic and microbial characteristics of extrapulmonary tuberculosis cases diagnosed in Malatya, Turkey, 2001-2007. BMC Public Health 2011;11:154. doi: 10.1186/1471-2458-11- 154.
29. Sevgi DY, Derin O, Alpay AS, et al. Extrapulmonary tuberculosis: 7 year-experience of a tertiary center in Istanbul. Eur J Intern Med 2013;24:864-7. doi: 10.1016/j. ejim.2013.08.704.
30. Bal İA, Tartar AS, Akbulut, A, Demirdağ K. Mediterr J Infect Microb Antimicrob 2021;10: 58.
31. Yang Z, Kong Y, Wilson F, et al. Identification of risk factors for extrapulmonary tuberculosis. Clin Infect Dis 2004;38:199- 205. doi: 10.1086/380644.
32. Lin JN, Lai CH, Chen YH, et al. Risk factors for extrapulmonary tuberculosis compared to pulmonary tuberculosis. Int J Tuberc Lung Dis 2009;13:620-5.
33. Shirzad-Aski H, Hamidi N, Sohrabi A, Abbasi A, Golsha R, Movahedi J. Incidence, risk factors and clinical characteristics of extra-pulmonary tuberculosis patients: a ten-year study in the North of Iran. Trop Med Int Health. 2020;25:1131-9. doi: 10.1111/tmi.13452.
34. Mohapatra PR, Janmeja AK. Tuberculous lymphadenitis. J Assoc Physicians India 2009;57:585-90.
35. Lee KC, Tami TA, Lalwani AK, Schecter G. Contemporary management of cervical tuberculosis. Laryngoscope. 1992;102:60-4. doi: 10.1288/00005.537.199201000-00012.
36. Levin-Epstein AA, Lucente FE. Scrofula—the dangerous masquerader. Laryngoscope 1982;92(8 Pt 1):938-43.
37. Diagnostic Standards and Classification of Tuberculosis in Adults and Children. This official statement of the American Thoracic Society and the Centers for Disease Control and Prevention was adopted by the ATS Board of Directors, July 1999. This statement was endorsed by the Council of the Infectious Disease Society of America, September 1999. Am J Respir Crit Care Med 2000;161(4 Pt 1):1376-95. doi: 10.1164/ ajrccm.161.4.16141.
38. Mandal SK, Laxmikant C. Erythrocyte sedimentation rate values in cases of active tuberculosis without HIV coinfection. J Med Sci Clin Res 2016;4:13156-9. doi: 10.18535/ jmscr/v4i10.58.
39. T.C. Ministry of Health, General Directorate of Public Health, Department of Tuberculosis. Distribution of Total Tuberculosis Cases by Country of Birth, 2005-2018. https://hsgm.saglik. gov.tr/depo/birimler/tuberkuloz_db/dosya/Istatistikler/Yeni/ Tuberkuloz_Olgularinin_Dogdugu_Ulkeye_Gore_Dagilimi. pdf. Accessed: 19 April 2019
40. Ilgazli A, Boyaci H, Basyigit I, Yildiz F. Extrapulmonary tuberculosis: clinical and epidemiologic spectrum of 636 cases. Arch Med Res 2004;35:435-41. doi: 10.1016/j. arcmed.2004.05.008.
41. Sirin Y, Coskunol I. Yuzyetmisuc ekstrapulmoner tuberkuloz olgusu. Tuberkuloz ve Toraks 2002;50:272-7.
42. Olson NR. Nontuberculous mycobacterial infections of the face and neck—practical considerations. Laryngoscope 1981;91:1714-26. doi: 10.1288/00005.537.198110000-00018.
43. Sinha SK, Chatterjee M, Bhattacharya S, et al. Diagnostic evaluation of extrapulmonary tuberculosis by fine needle aspiraton (FNA) supplemented with AFB smear and culture. J Indian Med Assoc 2003;101:588, 90-1.
44. Das DK. Fine-needle aspiration cytology in the diagnosis of tuberculous lesions. Lab Med 2000;31:625-32.