Trends and seasonal variation of hospitalization and mortality of interstitial lung disease in the United States from 2006 to 2016.

doi:10.21203/rs.3.rs-18341/v2

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Trends and seasonal variation of hospitalization and mortality of interstitial lung disease in the United States from 2006 to 2016.

https://doi.org/10.21203/rs.3.rs-18341/v2

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Background: In the recent years, the overall trends in hospital admission and mortality of interstitial lung disease (ILD) are unknown. In addition, there was some evidence that interstitial lung disease death rate highest in the winter but this finding was only available in one study. This study will investigate the trend and seasonal variations in hospital admission and mortality rates of ILD from 2006 to 2016.

Method: From the Nationwide Inpatient Sample database, we collected all cases with the International Classification of Diseases (ICD)-9 or ICD-10 codes of ILD excluding identifiable external causes (drug, organic or inorganic dusts) from 2006 to 2016. Hospitalization rates of each year were calculated based on U.S Census population data. Monthly hospitalization and in-hospital mortality rates were analyzed by seasonal and trend decomposition. Subgroups of idiopathic interstitial fibrosis (IPF), acute respiratory failure (ARF), pneumonia were analyzed.

Results: From 2006 to 2016, all-cause hospital admission rate of patients with interstitial lung disease (ILD) and IPF-only subgroup declined but their overall mortality remained unchanged (except IPF subgroup and acute respiratory failure subgroup). Acute respiratory failure related admission account for 23% of all causes and pneumonia 17.6%. Mortality of ILD in general and subgroup of ILD with ARF was highest in winter, up to 8.13% ± 0.60% and 26.3% ± 10.2% respectively. The seasonal variations of hospital admission and mortality of ILD in general was not changed when infectious pneumonia cases were ruled out. All cause admission rates were highest in months from January to April. Subgroup analysis also showed seasonal variations with highest hospitalization rates for all subgroups (IPF, ARF, pneumonia) in the months from December to April (winter to early Spring).

Conclusion: From 2006 to 2016, admission rates of ILD of all causes and IPF subgroup declined but in-hospital mortality remained unchanged. Mortality of IPF subgroup and acute respiratory failure subgroup trended down. All-cause hospital admissions and mortality of ILD have a strong seasonal variation. Hospitalization rates for all subgroups (IPF, ARF, pneumonia) were highest in the months from December to April.

Infectious Diseases

interstitial lung disease

seasonal variation

mortality

hospitalization

Interstitial lung disease (ILD) is a group of lung disorderscharacterized by abnormalities within the interstitium with orwithout extensive alteration of alveoli and airways [1]. There havebeen multiple forms of interstitial lung disease described, most ofwhich lead to progressive lung scarring and dyspnea if leftuntreated [2, 3]. Idiopathic pulmonary fibrosis (IPF) is one of themost well described ILD with overall very poor prognosis and mediansurvival of 3 to 5 years [4-6]. ILD remains still one of the mostchallenging respiratory entities to fully understand effectivelytreat and requires high healthcare utilization. In the past decade,there have been multiple new treatments and knowledge of thiscomplex group of lung disorder. However, study on the overall trendof hospital admission and mortality over the last decade is stillneeded.

Seasonal variations can play a major role in the general healthand wellbeing of patients with respiratory conditions. Winterseason can impact lung function and increase the risk of acuteexacerbations[7]. The mechanisms of this observation are complexand not fully understood [8]. Pulmonary conditions other thaninterstitial lung disease such as chronic obstructive pulmonarydisease (COPD) have been well studied showing significant seasonalvariation [9-11]. Understanding how respiratory diseases changewith seasonal variation could guide medical professionals in moreeffective health resource allocation and to direct future studieson the pathogenesis of this complex entity.

Using a large administrative database, we aimed to analyze thetrends and seasonal association of hospital admission and all-causemortality of ILD in the past 10 years.

We obtained the study population from Nationwide InpatientSample (NIS) of Agency for Healthcare Resource and Quality (AHRQ)Healthcare Cost and Utilization Project, years 2006 to 2016. Alldata contained in these database files have previously beende-identified and are off public record, therefore, ourinstitutional review board decided no approval for the study wasnecessary.

Appropriate weighting was used to produce accurate nation-wideestimates.

Study population was limited to adult patients (age ≥ 18),admitted with the primary diagnosis of interstitial lung disease(ILD) of all causes excluding the identifiable external causes(drug, asbestos, silicosis, pneumoconiosis, hypersensitivitypneumonitis due to organic dusts). (International Classification ofDiseases, ninth revision, clinical modification (ICD-9-CM)diagnostic codes 516.30 through 516.37 and 515); ICD-10-CM codesJ84.1 through J84.117). A complete list of used ICD codes withdescription is available in the Appendix. Annual populationestimates were obtained from U.S Census Bureau, to account forgrowing U.S population.

Statistical Analysis

Weighted annual and monthly hospitalization and in-hospitalmortality rates were calculated. Hospitalization rates within eachyear were calculated based on U.S. Census population estimates fora given year. In-hospital mortality rates were calculated withadmission number as denominators and in-hospital death numbers asnumerators. Monthly hospitalization or mortality rates represent atime series and can be analyzed by seasonal and trend decompositionprocedures to reveal long-term trends, seasonality, and randomfluctuations. Seasons were defined in a standard manner (“winter”includes December through February, “spring” – March through May,“summer” – June through August, and “fall” – September throughNovember).

We performed multiple subgroup analyses. The first groupincluded all cases with the primary diagnoses of IDL or PF. Insecond subgroup, we included only record with interstitialpulmonary fibrosis. Interstitial pulmonary fibrosis cases wereidentified based on the broad case definition algorithm proposed byRaghu et al (see the Supplementary Appendix 2). In the thirdsubgroup, we included only record of ILD with acute respiratoryfailure. The fourth subgroup included ILD with concomitantinfectious pneumonia. Please se Appendix section for all ICDcodes.

Inter-month and inter-seasonal differences of mean number ofhospitalizations was assessed by Kruskal-Wallis rank sum test.

Significance and magnitude of observed annual trends wasevaluated by Mann-Kendall test and Sen’s slope (Sen PK, 1968).

Hospital admissions

Average monthly hospitalization rate per 1,000,000 populationranges from 6.9 ± 0.8 in July to 8 ± 1.2 in April. The months fromJanuary to April had higher number of admissions compared to theremaining months of the year (Figure 1). Seasonalpattern of hospitalization rate was the same between subgroups ofincluded and excluded pneumonia.

After merging of months into seasons, mean (±SD) number ofhospitalizations in spring, summer, fall and winter were 7447.9± 932.0, 6643.0 ± 840.5, 6551.3 ± 922.6 and 7110.3± 866.1 respectively (Figure 2).Inter-seasonal differences did not reach statistical significance(ANOVA p = 0.079). However, the difference was found to besignificant (independent samples t-test p-value = 0.035) bycomparison of number of hospitalizations during spring (7447.9± 932.0) with other seasons (summer, fall, winter) combined(6768.2 ± 884.8).

Crude monthly hospitalization rate and trend (by LOESS seasonaldecomposition) over 11 years (2006 – 2016) is demonstrated inFigure 3. The observed descending trends werestatistically significant (p < 0.001 on Mann-Kendall test) inboth subgroups (with and without exclusion of admissions with PNA).Corresponding Sen’s slopes were similar: –0.00133 in group withoutexclusion of PNA admissions and –0.001167 in group with PNAexclusion. Please note, that National Inpatient Sample switched toICD-10 system in the third quarter of 2015 database, which couldaffect reporting of multiple diseases and conditions including PF,despite careful translation of ICD-9 diagnostic codes.

Mortality

The highest mortality was noted in December and February. Thepresence or absence of diagnosis of infectious pneumonia did notsignificantly affect seasonal variation of mortality.

Mortality rate in spring, summer, fall and winter were 7.61%± 0.67%, 7.13% ± 0.79%, 7.57% ± 0.69% and 8.13% ± 0.60%respectively (Figure 4). Observed differences weresignificant (ANOVA p = 0.018). Again, the highest mortalitypredisposition to winter was re-demonstrated.

Trend in mortality rate over 11 years are demonstrated inFigure 5. Observed trends were not significant(Mann-Kendall p = 0.7144 in subgroup without exclusion of PNAadmissions, and 0.2218 in subgroup of excluded PNA admissions).

Subgroups analysis (see figures in Supplementary appendix3)Only idiopathic pulmonary fibrosis (IPF) subgroup

There was a downward trend in hospitalization and mortality ofIPF over 11 years which was statistically significant (p<0.05)(Figure 6). IPF accounts for 88% of all admission of interstitiallung disease based on our broad diagnosis algorithm.Hospitalization rate of IPF were noted to be highest in the monthsfrom January to April compared to the rest of the months but themortality rates were not different between months.Only acute respiratory failure (ARF) as the cause ofadmission subgroupAcute respiratory failure accountsfor 23% of all admission due to interstitial lung disease.Seasonality of hospitalizations and in-hospital mortality did notreach statistical significance on analysis of crude monthly rates,however, seasonal decomposition revealed hidden seasonal variationwith slightly higher admission rates in winter. Mortality rangesfrom 24.2% ± 9.6% in July to 29.1% ± 11% in February.Hospitalization rates demonstrated a strong significant up-goingtrend with almost three-fold increase during 11 years (trendp<0.001). Mortality decreased at least two-fold with monotonoussignificant trend (p<0.001) (Figure 7).

Only pneumonia as the cause of admissionsubgroupAdmission with the diagnosis of pneumonia accounts for 17.6% of alladmission due to interstitial lung disease. Hospitalization ratesin months of December to April were observed to be higher than theremaining months of the year (p=0.007) but mortality did not differbetween the months (p=0.876). Hospitalization rate of ILD patientsadmitted for pneumonia decreased (p<0.05) but mortality rateremained the same in the period from 2006 to 2016 (p=0.756).

To the best of our knowledge, our study is the first to describeboth seasonal variations of hospital admission and in-hospitalmortality for IPF and non-IPF ILD in the United States in the 11year- period from 2006 to 2016. Our primary findings are that from2006 to 2016, all-cause hospital admission rate of patients withinterstitial lung disease (all interstitial lung disease andIPF-only subgroup) declined but their overall mortality remainedunchanged (except IPF subgroup). Acute respiratory failure relatedadmission account for 23% of all causes and pneumonia 17.6%.Mortality of ILD in general and ILD with acute respiratory failureis highest in winter, up to 8.13% ± 0.60% and 26.3% ± 10.2%respectively. Admission rate for all cause admissions are highestin months from January to April. Subgroup analysis also showedseasonal variations with highest hospitalization rates for allsubgroups (IPF, ARF, pneumonia) in the months from December toApril (winter to early Spring).

Our finding of highest all-cause mortality for all causes ofadmissions and subgroup of acute respiratory failure in the winterwas similar to the findings by Olson et al which used a differentdatabase for analysis [12]. Seasonal variations were observed inhospitalization rates across all subgroups (acute respiratoryfailure, IPF, pneumonia) as well. The two most common explanationsfor winter and early Spring increase in admission rates arerespiratory infection and cold temperature. Cold air couldhypothetically induce hyperpnoea, subsequently cause drying of theairways [13] and inducing proinflammatory substances productionleading to epithelial injury [8]. Infectious etiology was suggestedbecause strong seasonal variations have been reported in COPD,pneumonia and recognized viral illness [14]. There is some evidencethat a colder environment could also prolong the life span ofviruses. Many viruses such as influenza A, RSV andmycoplasma pneumonia which cause infections in humansalmost exclusively in winter to early spring [15, 16]. Oneinteresting findings is that although winter has highest admissionrate for all subgroups (IPF, ARF, pneumonia and ILD in general),the mortality does not have strong seasonal variations inidiopathic pulmonary fibrosis and pneumonia only subgroup. Onehypothesis could be the severity of IPF related admissions andpneumonia has no weather association. We could not find literatureto explain this finding thoroughly and it could be a topic forfuture research.

Respiratory causes of death accounted for 64 %-89% in patientswith ILD [17-19]. We found that acute respiratory failure accountsfor 23% of admission of interstitial lung disease and this types ofadmission has high mortality rate of 26.3% ± 10.2%. This findingconcurs with the results of Moua et al that IPF and non-IPFinterstitial lung disease both have very high and similar mortalityrates after admission for respiratory distress [20]. Based on astudy in Finland, ischemic heart disease, heart failure and lungcancer were the other causes of death [21]. All of those conditionsalso have been reported to have higher mortality in winter time inthe general population [12, 22], which may explain the highermortality in IPF and non IPF ILD patients in winter time

Of note, the in-hospital mortality of interstitial lung diseasewas noted to be significantly higher than the similar study inchronic obstructive lung disease (COPD) and asthma patients usingthe same national database ,8% vs 2%, 8% vs 1% respectively[23,24]. interestingly enough, the mortality rate was 14% higher in thewinter compared to the summer, which was less pronounced than theseasonal variations of all cause of deaths of COPD patients (25% to50% higher in the winter) [12, 25]. Although both COPD andinterstitial lung disease are both progressive illnesses with thepathogenesis involving accelerated cellular senescence[26]. Thisfinding suggests that the impact of weather and viral illness onmortality might not be as pronounced in ILD, compared to COPD.

One of the utmost important roles of physicians is to preventhospital admission for ILD patients. ILD and especially IPF relatedadmissions are significant events after which the lung function ofpatients will significantly deteriorate with the mean survival onlyfrom 2.8 months to 27.7 months [27]. From our study, we found thatall cause admission rates in ILD patients, subgroup of only IPF,acute respiratory failure and only pneumonia in the last 11 yearswere highest in the months December to April (winter to earlySpring). Spring in general had highest admission rates compared tothe average of other seasons, even when infectious lung diseaseswere ruled out. Moineddin et al in their study in the primary caresettings found a higher office visits due to respiratory disease inthe months from December to April [28].

In the period of 11 years from 2006 to 2016, we observed adecrease in admissions rate for all cause hospital admission forILD (all types ILD and subgroup of IPF) with the rise in populationtaken into account. The sharp decrease in 2016 hospital admissionsmight be a result of incomplete report of administrative datapossibly due to the transition from ICD-10 system in the thirdquarter of 2015. In addition, many advances have been introduced indiagnosis and treatment of interstitial lung disease [29] as wellas in hospital management in reducing hospital admissions [30].

The all-cause mortality rate from interstitial lungdisease from 2006 to 2016 has been unchanged. However, theall-cause mortality rate of idiopathic pulmonary fibrosis subgroupencouragingly decreased in this 11-year period. Anti-fibrotictreatment availability could be a possible explanation. A recentlarge database study by Demsey et al reported a decreased mortalityrisk in IPF patients in the first two years of anti-fibrotictreatment [31]. However, it is challenging to pinpoint a singlefactor that lead to this encouraging result based on our studyespecially when antifibrotic therapies were only approved since2014 [32].

Our study has limitations. We did not include all types ofinterstitial lung disease We excluded the interstitial lung diseasegroup with identifiable external agents (organic dust, drug,asbestos, silicosis, pneumoconiosis) because of two reasons.Firstly, it is for the comparison with the results of the study byOlson et al for the interstitial lung disease group from 1992 to2003 [12] and secondly, including ILD group with identifiableexternal agents with different pathogenesis will create moreheterogeneity to our population. IPF cases were identified based ona broad definition algorithm which has been commonly used in theepidemiology studies. However, this algorithm was sensitive but notspecific [33], thus could overestimate the prevalence of IPF in ourILD population. Although we have included all ICD-9-CM andICD-10-CM codes for interstitial lung disease, the results areinevitably susceptible to errors from coding inaccuracies.Nevertheless, this study has provided with an important andobjective overview on the seasonal variations and trends inadmissions and mortality of this entity spectrum over a long periodof time.

All cause hospital admission and mortality of interstitial lungdisease have a strong seasonal variation in 11 years from 2006 to2016. Hospital admissions are highest in the period from January toMay, in-hospital death was highest in the winter. All- causehospital admission of patients with interstitial lung diseasedeclined but their mortality remained unchanged, with or withoutthe presence of infectious pneumonia.

Ethics approval and consent to participate: this is a studybased on large national administrative database that is availablefor public. Consent and ethics approval was waived and notapplicable.

Consent for publication: not applicable

Availability of data and materials: all data were stored in thenational inpatient sample database

Competing interests: The authors declare no conflict ofinterest

Funding: there was no funding for this study.

Authors’ contribution: all authors contributed equally to themanuscript

Acknowledgement: not available

ILD: Interstitial Lung Disease

IPF: Idiopathic Pulmonary Fibrosis

PF: Pulmonary Fibrosis

NIS: Nationwide Inpatient Sample

ICD-9CM: International Classification of Diseases, ninthrevision, clinical modification

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Table 1. Average monthly number of in-hospitaladmissions for pulmonary fibrosis, hospitalization rate (per100,000 population), and in-hospital mortality; including andexcluding cases with codes for infectious pneumonia.

Month	Including admissions with codes for infectiousPNA			Excluding admissions with codes for infectiousPNA
Month	Number of hospitalizations, monthly (mean ± SD)	Monthly hospitalization rate, per 100,000population (mean ± SD)	In-hospital mortality, % (mean ± SD)	Number of hospitalizations, monthly (mean ± SD)	Monthly hospitalization rate, per 100,000population (mean ± SD)	In-hospital mortality, % (mean ± SD)
Jan	2,437 ± 312	0.79 ± 0.11	7.81 ± 1.49	1,951 ± 253	0.63 ± 0.09	5.83 ± 1.44
Feb	2,456 ± 313	0.79 ± 0.11	8.23 ± 1.39	2,002 ± 261	0.65 ± 0.09	6.28 ± 1.16
Mar	2,458 ± 315	0.79 ± 0.11	7.87 ± 1.04	2,001 ± 277	0.65 ± 0.10	5.73 ± 0.67
Apr	2,482 ± 337	0.80 ± 0.12	7.56 ± 0.73	2,052 ± 290	0.66 ± 0.10	5.83 ± 0.75
May	2,353 ± 293	0.76 ± 0.10	7.37 ± 0.93	1,948 ± 262	0.63 ± 0.09	5.50 ± 1.31
Jun	2,202 ± 321	0.71 ± 0.11	7.25 ± 1.09	1,825 ± 270	0.59 ± 0.09	5.38 ± 0.91
Jul	2,151 ± 304	0.69 ± 0.10	6.92 ± 1.45	1,802 ± 263	0.58 ± 0.09	5.25 ± 1.23
Aug	2,149 ± 227	0.69 ± 0.08	7.23 ± 0.90	1,802 ± 199	0.58 ± 0.07	5.57 ± 0.87
Sep	2,154 ± 245	0.69 ± 0.09	6.85 ± 1.20	1,801 ± 199	0.58 ± 0.07	5.16 ± 1.20
Oct	2,197 ± 368	0.71 ± 0.13	8.12 ± 1.33	1,813 ± 308	0.58 ± 0.11	6.19 ± 1.12
Nov	2,131 ± 363	0.68 ± 0.13	7.72 ± 1.17	1,763 ± 295	0.57 ± 0.10	5.75 ± 1.01
Dec	2,207 ± 296	0.71 ± 0.10	8.45 ± 1.56	1,785 ± 258	0.57 ± 0.09	6.25 ± 1.40

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Trends and seasonal variation of hospitalization and mortality of interstitial lung disease in the United States from 2006 to 2016.

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Abstract

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Introduction

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Discussion

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References

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