Hospitalization Risk for Medicare Beneficiaries With Nontuberculous Mycobacterial Pulmonary Disease

BackgroundNontuberculous mycobacterial pulmonary disease (NTM-PD) is an uncommon mycobacterial infection characterized by worsening lung function and increased health care resource utilization; however, the overall risk for hospitalization among patients with NTM-PD remains unclear.Research QuestionWhat is the hospitalization risk among older adults with NTM-PD?Study Design and MethodsA retrospective, nested, case-control study was conducted by using the Medicare claims database. Cases were defined as patients with ≥ 2 NTM-PD claims ≥ 30 days apart between January 1, 2007, and December 31, 2015. The study included individuals aged ≥ 65 years with ≥ 12 months of continuous enrollment in both Parts A and B before the first NTM-PD diagnosis. Cases were matched 1:2 to Medicare beneficiaries without NTM-PD (control subjects) according to age and sex. Hospitalizations following the first NTM-PD claim were compared between case and control subjects by using univariate and multivariate analyses.ResultsA total of 35,444 case subjects and 65,467 matched control subjects (mean age, 76.6 years; 70% female; ≥ 87% White) were identified. Baseline comorbidities, particularly pulmonary comorbidities, were more common in case subjects than in control subjects (81.1% vs 17.7% for COPD; 44.6% vs 0.6% for bronchiectasis). All-cause hospitalization was observed in 65.7% of case subjects and 44.9% of control subjects. Unadjusted annual hospitalization rates were significantly (P < .05) greater among case subjects than control subjects. Case subjects also had a significantly shorter time to hospitalization than control subjects. The increased burden due to hospitalization was reflected in multivariate analysis adjusting for baseline comorbidities. All-cause hospitalization in patients with NTM-PD relative to control subjects was 1.2 times more likely (relative risk, 1.23; 95% CI, 1.21-1.25; P < .0001) with a 46% greater hazard (hazard ratio, 1.46; 95% CI, 1.43-1.50; P < .0001).InterpretationPatients with NTM-PD were significantly more likely to be hospitalized, had greater annualized hospitalization rates, and had shorter time to hospitalization than age- and sex-matched control subjects without NTM-PD. These findings highlight the significantly increased burden of hospitalizations among patients with NTM-PD. Nontuberculous mycobacterial pulmonary disease (NTM-PD) is an uncommon mycobacterial infection characterized by worsening lung function and increased health care resource utilization; however, the overall risk for hospitalization among patients with NTM-PD remains unclear. What is the hospitalization risk among older adults with NTM-PD? A retrospective, nested, case-control study was conducted by using the Medicare claims database. Cases were defined as patients with ≥ 2 NTM-PD claims ≥ 30 days apart between January 1, 2007, and December 31, 2015. The study included individuals aged ≥ 65 years with ≥ 12 months of continuous enrollment in both Parts A and B before the first NTM-PD diagnosis. Cases were matched 1:2 to Medicare beneficiaries without NTM-PD (control subjects) according to age and sex. Hospitalizations following the first NTM-PD claim were compared between case and control subjects by using univariate and multivariate analyses. A total of 35,444 case subjects and 65,467 matched control subjects (mean age, 76.6 years; 70% female; ≥ 87% White) were identified. Baseline comorbidities, particularly pulmonary comorbidities, were more common in case subjects than in control subjects (81.1% vs 17.7% for COPD; 44.6% vs 0.6% for bronchiectasis). All-cause hospitalization was observed in 65.7% of case subjects and 44.9% of control subjects. Unadjusted annual hospitalization rates were significantly (P < .05) greater among case subjects than control subjects. Case subjects also had a significantly shorter time to hospitalization than control subjects. The increased burden due to hospitalization was reflected in multivariate analysis adjusting for baseline comorbidities. All-cause hospitalization in patients with NTM-PD relative to control subjects was 1.2 times more likely (relative risk, 1.23; 95% CI, 1.21-1.25; P < .0001) with a 46% greater hazard (hazard ratio, 1.46; 95% CI, 1.43-1.50; P < .0001). Patients with NTM-PD were significantly more likely to be hospitalized, had greater annualized hospitalization rates, and had shorter time to hospitalization than age- and sex-matched control subjects without NTM-PD. These findings highlight the significantly increased burden of hospitalizations among patients with NTM-PD. Take-home PointsStudy Question: What is the hospitalization risk among older adults with NTM-PD?Results: In this nested case-control study of Medicare beneficiaries (2007-2015), both univariate and multivariate analysis adjusting for baseline comorbidities show that patients with NTM-PD had an increased risk of all-cause hospitalization vs control subjects (relative risk, 1.23; 95% CI, 1.21-1.25; P < .0001), higher annual hospitalization rates than control subjects (IRR, 1.79; 95% CI, 1.77-1.81; P < .001 for all-cause hospitalization), and a significantly greater risk for sooner all-cause hospitalization relative to control subjects at any time during follow-up (hazard ratio, 1.46; 95% CI, 1.43-1.50; P < .0001).Interpretation: Patients with NTM-PD were significantly more likely to be hospitalized, had greater annualized hospitalization rates, and had shorter time to hospitalization than age- and sex-matched control subjects without NTM-PD, highlighting the need for careful medical management of these patients and clinical management strategies that may reduce excess hospitalizations. Study Question: What is the hospitalization risk among older adults with NTM-PD? Results: In this nested case-control study of Medicare beneficiaries (2007-2015), both univariate and multivariate analysis adjusting for baseline comorbidities show that patients with NTM-PD had an increased risk of all-cause hospitalization vs control subjects (relative risk, 1.23; 95% CI, 1.21-1.25; P < .0001), higher annual hospitalization rates than control subjects (IRR, 1.79; 95% CI, 1.77-1.81; P < .001 for all-cause hospitalization), and a significantly greater risk for sooner all-cause hospitalization relative to control subjects at any time during follow-up (hazard ratio, 1.46; 95% CI, 1.43-1.50; P < .0001). Interpretation: Patients with NTM-PD were significantly more likely to be hospitalized, had greater annualized hospitalization rates, and had shorter time to hospitalization than age- and sex-matched control subjects without NTM-PD, highlighting the need for careful medical management of these patients and clinical management strategies that may reduce excess hospitalizations. Nontuberculous mycobacterial pulmonary disease (NTM-PD) is a rare, chronic, progressive, and potentially debilitating condition that has become an increasingly common diagnosis.1Park H.Y. Jeong B.H. Chon H.R. Jeon K. Daley C.L. Koh W.J. Lung function decline according to clinical course in nontuberculous mycobacterial disease.Chest. 2016; 150: 1222-1232Abstract Full Text Full Text PDF PubMed Google Scholar, 2Mehta M. Marras T.K. Impaired health-related quality of life in pulmonary nontuberculous mycobacterial disease.Respir Med. 2011; 105: 1718-1725Abstract Full Text Full Text PDF PubMed Scopus (53) Google Scholar, 3Adjemian J. Olivier K.N. Seitz A.E. Holland S.M. Prevots R.D. Prevalence of nontuberculous mycobacterial lung disease in U.S. Medicare beneficiaries.Am J Respir Crit Care Med. 2012; 185: 881-886Crossref PubMed Scopus (362) Google Scholar, 4Marras T.K. Vinnard C. Zhang Q. et al.Relative risk of all-cause mortality in patients with nontuberculous mycobacterial lung disease in a US managed care population.Respir Med. 2018; 145: 80-88Abstract Full Text Full Text PDF PubMed Scopus (11) Google Scholar In a recent analysis of a large US health insurance database, among US Medicare Advantage (Part C) patients, the annual prevalence of NTM-PD increased from 19.8 to 43.1 cases per 100,000 population from 2008 to 2015.5Winthrop K.L. Marras T.K. Adjemian J. Zhang H. Wang P. Zhang Q. Incidence and prevalence of nontuberculous mycobacterial lung disease in a large U.S. managed care health plan, 2008-2015.Ann Am Thorac Soc. 2020; 17: 178-185Crossref PubMed Scopus (37) Google Scholar NTM-PD is known to lead to impaired pulmonary function and quality of life and an increased risk of mortality.1Park H.Y. Jeong B.H. Chon H.R. Jeon K. Daley C.L. Koh W.J. Lung function decline according to clinical course in nontuberculous mycobacterial disease.Chest. 2016; 150: 1222-1232Abstract Full Text Full Text PDF PubMed Google Scholar, 2Mehta M. Marras T.K. Impaired health-related quality of life in pulmonary nontuberculous mycobacterial disease.Respir Med. 2011; 105: 1718-1725Abstract Full Text Full Text PDF PubMed Scopus (53) Google Scholar, 3Adjemian J. Olivier K.N. Seitz A.E. Holland S.M. Prevots R.D. Prevalence of nontuberculous mycobacterial lung disease in U.S. Medicare beneficiaries.Am J Respir Crit Care Med. 2012; 185: 881-886Crossref PubMed Scopus (362) Google Scholar, 4Marras T.K. Vinnard C. Zhang Q. et al.Relative risk of all-cause mortality in patients with nontuberculous mycobacterial lung disease in a US managed care population.Respir Med. 2018; 145: 80-88Abstract Full Text Full Text PDF PubMed Scopus (11) Google Scholar,6Novosad S.A. Henkle E. Schafer S. et al.Mortality after respiratory isolation of nontuberculous mycobacteria: a comparison of patients who did and did not meet disease criteria.Ann Am Thorac Soc. 2017; 14: 1112-1119PubMed Google Scholar In addition to the symptoms that affect daily life,7US Food and Drug AdministrationThe Voice of the Patient. Non-Tuberculous Mycobacterial (NTM) Lung Infection Public Meeting: October 15, 2015.https://www.fda.gov/media/96932/downloadDate accessed: July 21, 2020Google Scholar,8Henkle E. Winthrop K.L. Ranches G.P. Plinke W. Litvin H.K. Quittner A.L. Preliminary validation of the NTM module: a patient-reported outcome measure for patients with pulmonary nontuberculous mycobacterial disease.Eur Respir J. 2020; 55: 1901300Crossref PubMed Scopus (4) Google Scholar the acute worsening of symptoms and exacerbations associated with NTM-PD can lead to hospitalization, as well as prolonged treatment, both contributing to substantial health care expenditures.9Strollo S.E. Adjemian J. Adjemian M.K. Prevots R.D. The burden of pulmonary nontuberculous mycobacterial disease in the United States.Ann Am Thorac Soc. 2015; 12: 1458-1464Crossref PubMed Scopus (66) Google Scholar In an analysis of national hospital discharge data for the United States from 1998 through 2005, the average annual prevalence of non-AIDS NTM-PD-associated hospitalizations among persons aged 70 to 79 years was 7.6 per 100,000 for men and 9.4 per 100,000 for women, with lower rates observed for younger individuals.10Billinger M.E. Olivier K.N. Viboud C. et al.Nontuberculous mycobacteria-associated lung disease in hospitalized persons, United States, 1998–2005.Emerg Infect Dis. 2009; 15: 1562-1569Crossref PubMed Scopus (109) Google Scholar In a study from Germany, patients with NTM-PD had five times more hospital days compared with matched control subjects over 39 months of follow-up.11Diel R. Jacob J. Lampenius N. et al.Burden of non-tuberculous mycobacterial pulmonary disease in Germany.Eur Respir J. 2017; 49: 1602109Crossref PubMed Scopus (54) Google Scholar However, the risk of hospitalization among patients with NTM-PD remains unclear. The objective of the current study was to estimate the risk of hospitalizations associated with NTM-PD among US Medicare beneficiaries. Our null hypothesis was that the case subjects and control subjects have equal hospitalization risk, and the statistical analysis would later reject the null hypothesis. We conducted a nested case-control study using the 100% US Medicare Parts A and B administrative claims database for January 1, 2007, through December 31, 2015. This population-based database includes beneficiaries in all 50 US states. A case of NTM-PD was defined as ≥ 2 claims with a diagnostic code for NTM-PD (International Classification of Diseases, Ninth Revision, Clinical Modification [ICD-9-CM] 031.0; International Classification of Diseases, Tenth Revision, Clinical Modification [ICD-10-CM] A31.0) that were ≥ 30 days apart.5Winthrop K.L. Marras T.K. Adjemian J. Zhang H. Wang P. Zhang Q. Incidence and prevalence of nontuberculous mycobacterial lung disease in a large U.S. managed care health plan, 2008-2015.Ann Am Thorac Soc. 2020; 17: 178-185Crossref PubMed Scopus (37) Google Scholar,12Marras T.K. Mirsaeidi M. Chou E. et al.Health care utilization and expenditures following diagnosis of nontuberculous mycobacterial lung disease in the United States.J Manag Care Spec Pharm. 2018; 24: 964-974PubMed Google Scholar We also restricted our analysis to patients with NTM-PD who were aged ≥ 65 years at the time of first diagnosis of NTM-PD. Control subjects were defined as Medicare beneficiaries without any NTM-PD claims during the study period. Each case subject was matched to two control subjects according to age (±0.5 years) and sex. The index date for each NTM-PD case was defined as the date of the first NTM-PD claim; the index date for each case was assigned to the matched control subjects. Both case subjects and matched control subjects were required to have at least 12 months of continuous coverage of Medicare Parts A and B13Centers for Medicare & Medicaid ServicesMedicare Program—General Information.https://www.cms.govDate accessed: August 5, 2020Google Scholar prior to the index date. Comorbid conditions for NTM-PD case subjects and matched control subjects were identified based on ICD-9-CM and ICD-10-CM codes from Medicare Parts A and B claims during the baseline period (ie, the 12 months prior to the index date). In addition, the Charlson Comorbidity Index (CCI) was calculated based on baseline diseases and health conditions to characterize patients' overall disease burden.14Quan H. Sundararajan V. Halfon P. et al.Coding algorithms for defining comorbidities in ICD-9-CM and ICD-10 administrative data.Med Care. 2005; 43: 1130-1139Crossref PubMed Scopus (5468) Google Scholar,15Sundararajan V. Quan H. Halfon P. et al.International Methodology Consortium for Coded Health Information (IMECCHI)Cross-national comparative performance of three versions of the ICD-10 Charlson index.Med Care. 2007; 45: 1210-1215Crossref PubMed Scopus (146) Google Scholar A CCI score of zero indicates that there were no comorbidities, and a higher score predicts an increased risk of mortality and use of health resources. Hospitalizations were accrued over the follow-up period, which was defined as the interval between the index date and the end of the study period (December 31, 2015), the last day prior to enrollment in Medicare Advantage (Part C), or death, was the follow-up period, to hospitalization were the of patients with the of the risk of and the time to hospitalization, NTM-PD case subjects vs control subjects for and pulmonary hospitalizations. associated with a hospitalization were identified from the first five diagnostic codes of the claim to diagnostic codes per claim were in Medicare the first five diagnostic codes included more than of the of for that hospitalization claim the of and pulmonary to hospitalization was as the interval between the index date and the date of the first hospitalization during the follow-up period. The study includes analysis of and clinical of patients with NTM-PD and the age- and sex-matched control as well as an of hospitalizations accrued over the follow-up period. We calculated the of individuals with the annualized hospitalization rates, and the time to hospitalizations with both univariate and multivariate was at P < as the and continuous through analysis included the for and the for continuous was to estimate the annual rates of hospitalizations for NTM-PD case subjects and control subjects as well as the of case subjects vs control subjects. were for persons who the follow-up period due to in Medicare Advantage or data and who did not due to as more hospitalizations prior to observed of the NTM-PD and the for and pulmonary hospitalizations The relative risk of hospitalization was by using with the defined as a hospitalization Both and relative for all-cause hospitalization for baseline comorbidities to hospitalization was with according to vs were death, data or in Medicare The was to the of the in the time to hospitalization between the two The hazard of NTM-PD relative to control subjects was by using the with time to all-cause hospitalization as the for baseline clinical were conducted by using of the study is in through a total of Medicare Parts A and B beneficiaries the NTM-PD case 2 claims for NTM-PD ≥ 30 days among these patients, 35,444 patients were ≥ 65 years and had ≥ 12 months of continuous enrollment in Parts A and B prior to the index date and the NTM-PD The baseline of the NTM-PD and the matched control subjects in The age was 76.6 and the were and The CCI score was higher in the NTM-PD than in matched control subjects comorbidities were more common in the NTM-PD than in the matched control subjects. Baseline were for pulmonary comorbidities, with for the NTM-PD vs control vs 17.7% for vs for 44.6% vs 0.6% for vs for of respiratory disease or vs for and vs for The of patients with these comorbidities were significantly P < and Clinical the to the Index for were from the P for continuous (CCI) were from the on index or or exacerbations of respiratory lung without Lung pulmonary with and pulmonary or or comorbidities included in the multivariate and lung pulmonary with without disease or and CCI Charlson Comorbidity NTM-PD nontuberculous mycobacterial pulmonary P for were from the P for continuous (CCI) were from the in a The comorbidities included in the multivariate and lung pulmonary with without disease or and CCI Charlson Comorbidity NTM-PD nontuberculous mycobacterial pulmonary The follow-up time was years for patients with NTM-PD and years for control subjects. of individuals with annualized hospitalization rates, and time to hospitalizations accrued over the follow-up period in the following All-cause hospitalization was observed in 65.7% of patients with NTM-PD and 44.9% of control subjects during the first all-cause hospitalizations following the index were pulmonary COPD; in the NTM-PD compared with in the control COPD; The relative risk of hospitalization associated with NTM-PD relative to control subjects was CI, P < .0001), that patients with NTM-PD were two times more likely to have a hospitalization than the control subjects. for baseline comorbidities patients with NTM-PD were at a increased risk of all-cause hospitalization compared with control subjects (relative risk, 1.23; 95% CI, 1.21-1.25; P < .0001). The annual rates of hospitalization were based on the at the end of the follow-up period for both the patients with NTM-PD and the control subjects. the end of the follow-up period, of patients with NTM-PD compared with of control follow-up time was years for NTM-PD and years for control subjects. who at the end of the follow-up time was years for patients with NTM-PD and years for control subjects. the annual of hospitalizations of hospitalizations per for or pulmonary among who and who at the end of follow-up who the rates were significantly higher among patients with NTM-PD relative to control for both all-cause and hospitalizations. the of all-cause hospitalization in patients with NTM-PD was times the in control subjects per in the NTM-PD compared with per in the control 1.79; 95% CI, 1.77-1.81; P < Hospitalizations to pulmonary conditions had a significantly higher in patients with NTM-PD relative to control subjects. of significantly higher rates associated with NTM-PD were also observed among the individuals who had at the end of the annual for all-cause hospitalization was in patients with NTM-PD compared with in the control (IRR, 95% CI, P < of during in annual rates between the NTM-PD and control were or greater for hospitalizations to or pulmonary with the in hospitalization the for all-cause hospitalization, that the time to hospitalization was significantly shorter in patients with NTM-PD than in control subjects during the follow-up period. The time to all-cause hospitalizations was days among patients with NTM-PD vs days among control subjects. adjusting for baseline clinical by using the patients with NTM-PD at a 46% higher risk of all-cause hospitalization compared with control subjects (hazard ratio, 1.46; 95% CI, 1.43-1.50; P < .0001). We that among Medicare beneficiaries aged ≥ 65 the risk of all-cause hospitalization in patients with NTM-PD was significantly increased relative to age- and sex-matched control subjects. hospitalization and pulmonary hospitalization rates were higher for both patients who the follow-up period and for who during the follow-up period. comorbidities were more common in patients with NTM-PD at for more first all-cause and likely to the higher of all-cause after for baseline comorbidities, compared with the control patients with NTM-PD had a greater than increased risk of all-cause hospitalization and a 46% higher risk of all-cause hospitalization sooner than control subjects at any time following the diagnosis of NTM-PD. The increased risk of hospitalization to NTM-PD is by NTM-PD hospitalization as well as by that Hospitalizations a of disease as who hospitalized more likely to recent study that NTM can progressive, et in an of pulmonary or nontuberculous mycobacterial disease.Chest. 2012; Full Text Full Text PDF PubMed Scopus Google Scholar in a national nested case-control study of patients by the Health patients had both an increased risk of and an increased risk of after adjusting for lung and Winthrop K.L. et of nontuberculous mycobacterial in the U.S. Health 2018; PubMed Google Scholar In addition, Marras et T.K. H. et nontuberculous mycobacteria-associated Infect Dis. 2017; PubMed Scopus Google Scholar identified an mortality risk associated with NTM in a population-based study in These findings a increased risk that is to This in risk is not a of of NTM-PD. the in overall mortality likely from a in a of and increased In addition, patients identified by using diagnostic codes as well as by have an increased risk of both hospitalization and a and not a among patients identified by using diagnostic The of patients with and have in of Medicare data from an period J. Olivier K.N. Seitz A.E. Holland S.M. Prevots R.D. Prevalence of nontuberculous mycobacterial lung disease in U.S. Medicare beneficiaries.Am J Respir Crit Care Med. 2012; 185: 881-886Crossref PubMed Scopus (362) Google these higher than likely a to is defined to and conditions as and however, also as by and may have as in Medicare claims in of patients with NTM-PD identified through diagnostic et pulmonary disease States, Care. Google Scholar The risk of hospitalization among with NTM-PD indicates a burden of disease and associated Hospitalizations associated with an increased relative to and an of the risk of hospitalization to NTM-PD for a of associated S.E. Adjemian J. Adjemian M.K. Prevots R.D. The burden of pulmonary nontuberculous mycobacterial disease in the United States.Ann Am Thorac Soc. 2015; 12: 1458-1464Crossref PubMed Scopus (66) Google R. Jacob J. Lampenius N. et al.Burden of non-tuberculous mycobacterial pulmonary disease in Germany.Eur Respir J. 2017; 49: 1602109Crossref PubMed Scopus (54) Google Scholar prior national population-based have the of patients hospitalized with NTM-PD in the United M.E. Olivier K.N. Viboud C. et al.Nontuberculous mycobacteria-associated lung disease in hospitalized persons, United States, 1998–2005.Emerg Infect Dis. 2009; 15: 1562-1569Crossref PubMed Scopus (109) Google Scholar R. Jacob J. Lampenius N. et al.Burden of non-tuberculous mycobacterial pulmonary disease in Germany.Eur Respir J. 2017; 49: 1602109Crossref PubMed Scopus (54) Google et al.Burden and of associated with pulmonary non-tuberculous mycobacterial in Germany, Infect Dis. PubMed Scopus Google Scholar and S.M. S. et of nontuberculous mycobacterial lung diseases in a hospital in between and 2018; PubMed Scopus Google Scholar the risk of hospitalization and the hospitalized increased of The of hospitalization among with NTM-PD in the United States has to be US for S.E. Adjemian J. Adjemian M.K. Prevots R.D. The burden of pulmonary nontuberculous mycobacterial disease in the United States.Ann Am Thorac Soc. 2015; 12: 1458-1464Crossref PubMed Scopus (66) Google Scholar of our analysis is that population-based risk among older adults in the United The current analysis was based on Medicare Parts A and which of total Medicare enrollment in 2015; the of Medicare Parts A and B were aged ≥ 65 years in to for Medicare & Medicaid ServicesMedicare Program—General Information.https://www.cms.govDate accessed: August 5, 2020Google Scholar Our findings may not be to Medicare or health care as these were from our However, this a large population of older adults in the United The of the current study is that the codes for NTM-PD have a in The ICD-9-CM codes for NTM-PD have in and is et al.Nontuberculous mycobacterial lung disease prevalence at health care J Respir Crit Care Med. PubMed Scopus Google Henkle M. Winthrop K.L. of diagnosis claims to pulmonary NTM disease in Infect Dis. 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