Advertisement

Nontuberculous mycobacteria infections of the pleura: A systematic review

Published:October 31, 2022DOI:https://doi.org/10.1016/j.rmed.2022.107036

      Highlights

      • Nontuberculous mycobacteria infections of the pleura arise in immunocompetent and immunosuppressed patients.
      • The pleural infection does not necessarily co-exist with a nontuberculous mycobacteria pulmonary infection.
      • The prognosis of nontuberculous mycobacteria pleural infection is poor including a high risk of complications.

      Abstract

      Background

      Nontuberculous mycobacterial (NTM) pleuritis is an uncommon manifestation of NTM infection. Case reports and small case series have shown a variable clinical course and high mortality rates.

      Objective

      To describe patients' characteristics, clinical presentation and outcomes of NTM pleural infections.

      Methods

      A systematic review of cases of NTM pleural infections published in PubMed-indexed journals from 1980 to 2021.

      Results

      A total of 206 cases of NTM pleural infections were found and analyzed. Fifty-eight percent of cases were males. The mean age was 57.5 yrs (range 9–87 yrs). Forty-three percent of patients were immunosuppressed, and 43% had a chronic lung disease; thirty-two percent had neither risk factor. In addition to the pleural infection, 67% of cases had a concurrent pulmonary NTM infection, and in 18 cases there was another extrapulmonary site of NTM infection. In 29% of cases the pleural infection was the sole manifestation of NTM disease. The most common isolated mycobacterium was Mycobacterium avium complex (65%). Fifty-three percent and 26% of patients required pleural effusion drainage and a surgical intervention, respectively, to treat the infection, in addition to anti-NTM chemotherapy. Forty percent of patients developed pneumothorax, 16% suffered from empyema, and 16.5% had broncho-pleural fistula. The reported mortality rate was 24%.

      Conclusion

      NTM pleural infections may arise in immunocompetent and immunosuppressed patients, with or without chronic lung disease or concurrent NTM pulmonary infection. These infections carry a poor prognosis and a high risk of complications requiring surgical interventions in addition to anti-NTM chemotherapy.

      Keywords

      Abbreviations:

      NTM (nontuberculous mycobacteria), AIDS (acquired immunodeficiency syndrome), PCR (polymerase chain reaction), HIV (human immunodeficiency virus), TB (tuberculosis), INF-ɣ (interferon-gamma), IL-12 (interleukin 12), TNF-α (tumor necrosis factor-alpha)
      To read this article in full you will need to make a payment

      Purchase one-time access:

      Academic & Personal: 24 hour online accessCorporate R&D Professionals: 24 hour online access
      One-time access price info
      • For academic or personal research use, select 'Academic and Personal'
      • For corporate R&D use, select 'Corporate R&D Professionals'

      Subscribe:

      Subscribe to Respiratory Medicine
      Already a print subscriber? Claim online access
      Already an online subscriber? Sign in
      Institutional Access: Sign in to ScienceDirect

      References

        • Griffith D.E.
        • Aksamit T.
        • Brown-Elliott B.A.
        • et al.
        An official ATS/IDSA statement: diagnosis, treatment, and prevention of nontuberculous mycobacterial diseases.
        Am. J. Respir. Crit. Care Med. 2007; 175: 367-416
        • Falkinham 3rd, J.O.
        Epidemiology of infection by nontuberculous mycobacteria.
        Clin. Microbiol. Rev. 1996; 9: 177-215
        • O'Brien R.J.
        • Geiter L.J.
        • Snider D.E.
        The epidemiology of nontuberculous mycobacterial diseases in the United States: results from a national survey.
        Am. Rev. Respir. Dis. 1987; 135: 1007-1014
        • Horsburgh Jr., C.J.
        • Selik R.M.
        The epidemiology of disseminated nontuberculous mycobacterial infection in the acquired immunodeficiency syndrome (AIDS).
        Am. Rev. Respir. Dis. 1989; 139: 4-7
        • McShane P.J.
        • Glassroth J.
        Pulmonary disease due to nontuberculous mycobacteria: current state and new insights.
        Chest. 2015; 148: 1517-1527
        • Shu C.C.
        • Lee L.N.
        • Wang J.T.
        • et al.
        Non-tuberculous mycobacterial pleurisy: an 8-year single-centre experience in Taiwan.
        Int. J. Tubercul. Lung Dis. 2010; 14: 635-664
        • Ando T.
        • Kawashima M.
        • Matsui H.
        • et al.
        Clinical features and prognosis of nontuberculous mycobacterial pleuritis.
        Respiration. 2018; 96: 507-513
        • Park S.
        • Kyung-Wook J.
        • Sang-Do L.
        • et al.
        Clinical characteristics and treatment outcomes of pleural effusions in patients with nontuberculous mycobacterial disease.
        Respir. Med. 2017; 133: 36-41
        • Wen P.
        • Wei M.
        • Xu Y.R.
        • Dong L.
        Clinical relevance and characteristics of nontuberculous mycobacterial pleuritis.
        Jpn. J. Infect. Dis. 2020; 73: 282-287
        • Naito M.
        • Maekura T.
        • Kurahara Y.
        • et al.
        Clinical features of nontuberculous mycobacterial pleurisy: a review of 12 cases.
        Intern. Med. 2018; 57: 13-16
        • Okada Y.
        • Ichinose Y.
        • Yamaguchi K.
        • et al.
        Mycobacterium avium-intracellulare pleuritis with massive pleural effusion.
        Eur. Respir. J. 1995; 8: 1428-1429
        • Kadota N.
        • Shinohara T.
        • Hino H.
        • et al.
        Mycobacterium abscessus ssp. abscessus infection progressing to empyema from vertebral osteomyelitis in an immunocompetent patient without pulmonary disease: a case report.
        BMC Pulm. Med. 2019; 19: 100
        • Page M.J.
        • Moher D.
        • Bossuyt P.M.
        • et al.
        PRISMA 2020 explanation and elaboration: updated guidance and exemplars for reporting systematic reviews.
        BMJ. 2021; (n160. Published 2021 Mar 29): 372https://doi.org/10.1136/bmj.n160
        • Yagi K.
        • Ito A.
        • Fujiwara K.
        • et al.
        Clinical features and prognosis of nontuberculous mycobacterial pleuritis: a multicenter retrospective study.
        Ann Am Thorac Soc. 2021; 18: 1490-1497
        • Tanaka Y.
        • Hori T.
        • Ito K.
        • Fujita T.
        • Ishikawa T.
        • Uchiyama T.
        Disseminated Mycobacterium avium complex infection in a patient with autoantibody to interferon-gamma.
        Intern. Med. 2007; 46: 1005-1009
        • Lai C.C.
        • Chao C.M.
        • Gau S.J.
        • Hsueh P.R.
        Thoracic empyema and bacteremia due to Mycobacterium abscessus in a patient with liver cirrhosis.
        J. Microbiol. Immunol. Infect. 2013; 46: 482-484
        • Ogata H.
        • Harada E.
        • Takao T.
        • Ijichi K.
        • Hamada N.
        • Matsumoto K.
        Mycobacterium avium pleuritis with multiple nodules in the pleura.
        Respirol Case Rep. 2020; 8e00608
        • Ikeue T.
        • Yoshida H.
        • Tanaka E.
        • et al.
        Pleuritis caused by Mycobacterium kyorinense without pulmonary involvement.
        Intern. Med. 2017; 56: 2785-2790
        • Furuuchi K.
        • Morimoto K.
        • Fujiwara K.
        • et al.
        Mycobacterium avium complex pleuritis with elevated anti-glycopeptidolipid-core IgA antibody levels in pleural effusion.
        Intern. Med. 2019; 58: 2577-2579
        • Coolen-Allou N.
        • Belmonte O.
        • Andre M.
        • Gazaille V.
        Hydropneumothorax révélant une infection pleurale à Mycobacterium intracellulare [Hydropneumothorax revealing Mycobacterium intracellulare pleural infection].
        Med. Maladies Infect. 2018; 48: 215-217
        • Hirabayashi R.
        • Nakagawa A.
        • Takegawa H.
        • Tomii K.
        A case of pleural effusion caused by Mycobacterium fortuitum and Mycobacterium mageritense coinfection.
        BMC Infect. Dis. 2019; 19 (Published 2019 Aug 15): 720
        • Noguchi S.
        • Hanami K.
        • Miyata H.
        • et al.
        Pleurisy caused by Mycobacterium abscessus in a young patient with dermatomyositis: a case report and brief review of the literature.
        Intern. Med. 2018; 57: 997-1002
        • Schubel K.
        • Bassinet L.
        • Monnet I.
        • et al.
        Pleuropneumonie à Mycobacterium chelonae [Pleuropneumonia due to Mycobacterium chelonae].
        Rev. Mal. Respir. 2011; 28: 348-351
        • Yamoto M.
        • Kawagishi Y.
        • Murata A.
        • Tsuji H.
        Successful treatment of non-tuberculous mycobacterial pleurisy with acute fever by antimycobacterial therapy.
        BMJ Case Rep. 2018; 2018 (bcr2017222439. Published 2018 Feb 8)
        • Nagaia T.
        • Akiyama M.
        • Mita Y.
        • Tomizawa T.
        • Dobashi K.
        • Mori M.
        Mycobacterium avium complex pleuritis accompanied by diabetes mellitus.
        Diabetes Res. Clin. Pract. 2000; 48: 99-104
        • Fabbian F.
        • De Giorgi A.
        • Pala M.
        • Fratti D.
        • Contini C.
        Pleural effusion in an immunocompetent woman caused by Mycobacterium fortuitum.
        J. Med. Microbiol. 2011; 60: 1375-1378
        • Lee Y.C.
        • Kim S.B.
        • Gang S.J.
        • Park S.Y.
        • Kim S.R.
        Acute necrotizing pneumonia combined with parapneumonic effusion caused by Mycobacterium lentiflavum: a case report.
        BMC Infect. Dis. 2015; 15 (. Published 2015 Aug 19): 354
        • Zeitler K.
        • Walter J.
        • Khan F.
        • Sriaroon C.
        Recurrent disseminated Mycobacterium avium in a female patient from Thailand with anti-interferon-gamma autoantibodies: dilemma on treatment approach.
        BMJ Case Rep. 2021; 14 (Published 2021 Jan 28)e237909
        • Lee H.T.
        • Su W.J.
        • Chou T.Y.
        • Chen W.S.
        • Su K.Y.
        • Huang D.F.
        Mycobacterium avium complex-induced pleurisy in a patient with amyopathic dermatomyositis and interstitial lung disease after prolonged immunosuppressive therapy.
        J. Clin. Rheumatol. 2009; 15: 193-194
        • Vonmoos S.
        • Leuenberger P.
        • Beer V.
        • de Haller R.
        Infection pleuro-pulmonaire à Mycobacterium smegmatis. Description d'un cas et revue de la littérature [Pleuropulmonary infection caused by Mycobacterium smegmatis. Case description and literature review].
        Schweiz. Med. Wochenschr. 1986; 116: 1852-1856
        • Blair P.
        • Moshgriz M.
        • Siegel M.
        Mycobacterium fortuitum empyema associated with an indwelling pleural catheter: case report and review of the literature.
        J. Infect. Chemother. 2017; 23: 177-179
        • Manglani R.P.
        • Khaja M.
        • Hennessey K.
        • Kennedy O.
        Pleural mycobacterium avium complex infection in an immunocompetent female with no risk factors.
        Case Rep Pulmonol. 2015; 2015760614
        • Kakugawa T.
        • Mukae H.
        • Kajiki S.
        • et al.
        Mycobacterium avium pleuritis in a non-immunocompromised patient.
        Intern. Med. 2008; 47: 1727-1731
        • Domfeh A.B.
        • Nodit L.
        • Gradowski J.F.
        • Bastacky S.
        Mycobacterium kansasii infection diagnosed by pleural fluid cytology: a case report.
        Acta Cytol. 2007; 51: 627-630
        • Dorion I.
        • Mayeux I.
        • François Y.
        • Remond A.
        • Gontier M.F.
        • Jounieaux V.
        Pneumopathie lipidique et mycobactériose atypique pleuro-pulmonaire [Lipid pneumonia and pleural-pulmonary atypical mycobacteriosis].
        Rev. Mal. Respir. 2000; 17: 700-703
        • O'Beirne S.L.
        • Escalon J.G.
        • Momtahen S.
        • et al.
        Severe cavitary, fistulating Mycobacterium avium-intracellulare complex disease in an immunocompetent host.
        Am. J. Respir. Crit. Care Med. 2015; 192: 1387-1388
        • Gribetz A.R.
        • Damsker B.
        • Marchevsky A.
        • Bottone E.J.
        Nontuberculous mycobacteria in pleural fluid. Assessment of clinical significance.
        Chest. 1985; 87: 495-498
        • Zhou X.
        • Ruan Q.
        • Jiang W.
        • et al.
        Isolation of Mycobacterium arupense from pleural effusion: culprit or not?.
        BMC Infect. Dis. 2018; 18 (Published 2018 May 15): 221
        • Buijtels P.C.
        • Petit P.L.
        • Verbrugh H.A.
        • van Belkum A.
        • van Soolingen D.
        Isolation of nontuberculous mycobacteria in Zambia: eight case reports.
        J. Clin. Microbiol. 2005; 43: 6020-6026
        • Park S.U.
        • Koh W.J.
        • Kwon O.J.
        • et al.
        Acute pneumonia and empyema caused by Mycobacterium intracellulare.
        Intern. Med. 2006; 45: 1007-1010
        • Yoon H.J.
        • Chung M.J.
        • Lee K.S.
        • Kim J.S.
        • Park H.Y.
        • Koh W.J.
        Broncho-pleural fistula with hydropneumothorax at CT: diagnostic implications in Mycobacterium avium complex lung disease with pleural involvement.
        Korean J. Radiol. 2016; 17: 295-301
        • Kapetanopoulos A.
        • Habboub A.
        • Gillam L.D.
        • Ross J.W.
        Cardiac tamponade as a result of Mycobacterium avium-complex pleural effusion.
        Conn. Med. 2004; 68: 147-151
        • Yanagihara K.
        • Tomono K.
        • Sawai T.
        • et al.
        Mycobacterium avium complex pleuritis.
        Respiration. 2002; 69: 547-549
        • Lim J.G.
        • Sw O.
        • Lee K.D.
        • et al.
        Mycobacterium intracellulare pleurisy identified on liquid cultures of the pleural fluid and pleural biopsy.
        Tuberc. Respir. Dis. 2013; 74: 124-128
        • Howell D.
        • Galen B.T.
        Recurrent rheumatoid pleural effusions complicated by Mycobacterium heckeshornense infection.
        Respir Med Case Rep. 2018; 25 (Published 2018 Oct 26): 333-335
        • Chau C.H.
        • Yew W.W.
        • Lam F.M.
        Pleural effusion due to Mycobacterium gordonae infection.
        Int. J. Tubercul. Lung Dis. 2003; 7: 503
        • Nei T.
        • Okabe M.
        • Mikami I.
        • et al.
        A non-HIV case with disseminated Mycobacterium kansasii disease associated with strong neutralizing autoantibody to interferon-γ.
        Respir Med Case Rep. 2012; 8 (Published 2012 Dec 31): 10-13
        • Shah I.
        • Shah F.
        Nontuberculous mycobacterial empyema in an immunocompetent child.
        Indian J. Pathol. Microbiol. 2018; 61: 141-142
        • Goto A.
        • Ando M.
        • Komiya K.
        • et al.
        Mycobacterium abscessus subsp. abscessus empyema complicated with subcutaneous abscess.
        J. Infect. Chemother. 2020; 26: 300-304
        • Matsumoto T.
        • Otsuka K.
        • Tomii K.
        Mycobacterium fortuitum thoracic empyema: a case report and review of the literature.
        J. Infect. Chemother. 2015; 21: 747-750
        • Haider A.
        • Schliep T.
        • Zeana C.
        Nontuberculous mycobacterium disease with pleural empyema in a patient with advanced AIDS.
        Am. J. Med. Sci. 2009; 338: 418-420
        • Hsieh H.C.
        • Lu P.L.
        • Chen T.C.
        • Chang K.
        • Chen Y.H.
        Mycobacterium chelonae empyema in an immunocompetent patient.
        J. Med. Microbiol. 2008; 57: 664-667
        • Paull D.E.
        • Decker G.R.
        • Brown R.L.
        Mycobacterium Kansasii empyema in a renal transplant recipient case report and review of the literature.
        Transplantation. 2003; 76: 270-271
        • Fairhurst R.M.
        • Kubak B.M.
        • Shpiner R.B.
        • Levine M.S.
        • Pegues D.A.
        • Ardehali A.
        Mycobacterium abscessus empyema in a lung transplant recipient.
        J. Heart Lung Transplant. 2002; 21: 391-394
        • Agheli A.
        • Tehranirad M.
        • Cofsky R.
        An unusual presentation of mycobacterium fortuitum: massive isolated empyema in a patient with HIV.
        MedGenMed. 2006; 8 (Published 2006 Jun 29): 90
        • Olafsson E.J.
        • Naum C.C.
        • Sarosi G.A.
        • Mastronarde J.G.
        Bilateral pleural effusions and right pneumothorax in a 25-year-old man.
        Chest. 2004; 126: 986-992
        • DeLeon T.T.
        • Chung H.H.
        • Opal S.M.
        • Dworkin J.D.
        Mycobacterium avium complex empyema in a patient with interferon gamma autoantibodies.
        Hawai‘i J. Med. Public Health. 2014; 73: 15-17
        • Zvetina J.R.
        • Difilippo N.M.
        • Ali M.M.
        • Vandrunen M.
        Mycobacterium kansasii empyema.
        Tubercle. 1981; 62: 135-138
        • Jo K.W.
        • Kim J.W.
        • Hong Y.
        • Shim T.S.
        A case of empyema necessitatis caused by Mycobacterium abscessus.
        Respir Med Case Rep. 2012; 6 (Published 2012 Aug 9): 1-4
        • Huang H.C.
        • Yu W.L.
        • Shieh C.C.
        • Cheng K.C.
        • Cheng H.H.
        Unusual mixed infection of thoracic empyema caused by Mycobacteria tuberculosis, nontuberculosis mycobacteria and Nocardia asteroides in a woman with systemic lupus erythematosus.
        J. Infect. 2007; 54: e25-e28
        • Varkey M.R.
        • Kohal T.M.
        • Barua A.
        • Lapinel N.C.
        • Ali J.
        A tale of two images: from mycobacterium avium complex-lung disease (MAC-LD) to mycobacterium avium complex-pleural disease.
        Respir Med Case Rep. 2021; 33 (Published 2021 Apr 13)101410
        • Kawai N.
        • Kawaguchi T.
        • Tojo T.
        • et al.
        Endobronchial watanabe spigots for treatment of pyopneumothorax due to nontuberculous mycobacteriosis in a patient with rheumatoid arthritis: a case report based on past experience.
        Case Rep Pulmonol. 2018; 2018 (. Published 2018 Sep. 26)6738435
        • Kotani K.
        • Hirose Y.
        • Endo S.
        • Yamamoto H.
        • Makihara S.
        Surgical treatment of atypical Mycobacterium intracellulare infection with chronic empyema: a case report.
        J. Thorac. Cardiovasc. Surg. 2005; 130: 907-908
        • Kho B.G.
        • Na Y.O.
        • Park H.K.
        • et al.
        Life-threatening Mycobacterium intracellulare pleuritis in an immunocompetent host: case reports.
        Medicine (Baltim.). 2021; 100e28342
        • Niitsu T.
        • Kuge T.
        • Fukushima K.
        • et al.
        Pleural effusion caused by mycolicibacterium mageritense in an immunocompetent host: a case report.
        Front. Med. 2021; 8 (Published 2021 Nov 24)797171
        • Shaw J.A.
        • Diacon A.H.
        • Koegelenberg C.F.N.
        Tuberculous pleural effusion.
        Respirology. 2019 Oct; 24: 962-971
        • Maskell N.A.
        • Light R.W.
        Chapter 80: pleural infections.
        in: Broaddus V.C. Mason R.J. Ernst J.D. King T.E. Lazarus S.C. Murray and Nadel's Textbook of Respiratory Medicine. sixth ed. Elsevier/Saunders, 2016: 1425-1438
        • Corcoran J.P.
        • Wrightson J.M.
        • Belcher E.
        • DeCamp M.M.
        • Feller-Kopman D.
        • Rahman N.M.
        Pleural infection: past, present, and future directions.
        Lancet Respir. Med. 2015 Jul; 3: 563-577
        • Bedawi E.O.
        • Hassan M.
        • McCracken D.
        • Rahman N.M.
        Pleural infection: a closer look at the etiopathogenesis, microbiology and role of antibiotics.
        Expet Rev. Respir. Med. 2019 Apr; 13: 337-347
        • Davies C.W.
        • Kearney S.E.
        • Gleeson F.V.
        • Davies R.J.
        Predictors of outcome and long-term survival in patients with pleural infection.
        Am. J. Respir. Crit. Care Med. 1999; 160: 1682-1687
        • Rahman N.M.
        • Kahan B.C.
        • Miller R.F.
        • Gleeson F.V.
        • Nunn A.J.
        • Maskell N.A.
        A clinical score (RAPID) to identify those at risk for poor outcome at presentation in patients with pleural infection.
        Chest. 2014; 145: 848-855
        • Bedawi E.O.
        • Hassan M.
        • Rahman N.M.
        Recent developments in the management of pleural infection: a comprehensive review.
        Clin. Res. J. 2018; 12: 2309-2320
        • Light R.W.
        Parapneumonic effusions and empyema.
        Proc. Am. Thorac. Soc. 2006; 3: 75-80