Abstract
Objective:
To investigate trends and associated factors of utilization of hospital palliative care among patients with systemic lupus erythematosus (SLE) and analyze its impact on length of hospital stay, hospital charges, and in-hospital mortality.
Methods:
Using the 2005-2014 National Inpatient Sample in the United States, the compound annual growth rate was used to investigate the temporal trend of utilization of hospital palliative care. Multivariate multilevel logistic regression analyses were performed to analyze the association with patient-related factors, hospital factors, length of stay, in-hospital mortality, and hospital charges.
Results:
The overall proportion of utilization of hospital palliative care for the patient with SLE was 0.6% over 10 years. It increased approximately 12-fold from 0.1% (2005) to 1.17% (2014). Hospital palliative care services were offered more frequently to older patients, patients with high severity illnesses, and in urban teaching hospitals or large size hospitals. Patients younger than 40 years, the lowest household income group, or Medicare beneficiaries less likely received palliative care during hospitalization. Hospital palliative care services were associated with increased length of stay (β = 1.407, P < .0001) and in-hospital mortality (odds ratio, 48.18; 95% confidence interval, 41.59-55.82), and reduced hospital charge (β = −0.075, P = .009).
Conclusion:
Hospital palliative care service for patients with SLE gradually increased during the past decade in US hospitals. However, this showed disparities in access and was associated with longer hospital length of stay and higher in-hospital mortality. Nevertheless, hospital palliative care services yielded a cost-saving effect.
Keywords
Introduction
Systemic lupus erythematosus (SLE) is a systemic autoimmune rheumatic disease, which can involve any organ, compromise health-related quality of life, and finally threaten life. A prevalence of SLE was reported of 124 to 372 per 100 000 in United States. 1 Systemic lupus erythematosus ranked among the top 20 leading causes of female death between the ages of 5 and 64 years based on mortality data from the United States Centers for Disease Control and Prevention, from 2000 to 2015. 2 Patients with SLE suffer from a wide range of symptoms and have a variable prognosis depending on the severity and type of organ involvement, and are frequently hospitalized and readmitted. 3 These fact represents a significant direct and indirect charge of disease to patients and the health-care system. 1,4,5 The recent literature estimated an additional annual cost of US$34 146 for SLE patients in general, US$73 306 for patients with lupus nephritis, and between US$13 869 and US$56 882 for patients with severe or active SLE. 1,4 The mean direct costs per admission during hospitalization were US$20 934 and the mean annual cost per patient during hospitalization was US$51 808.41. 5
In recent decades, accumulating evidence of the beneficial clinical and public health outcomes has grown for early introduction of palliative care. Previous studies among patients with cancer and several noncancer chronic diseases showed favorable effects regarding health-care utilization such as hospital length of stay (LOS), in-hospital mortality, and hospital charges. 6 -9 Advancements in palliative medicine have been made in nononcologic specialties like neurology, cardiology, and nephrology, and it would be similarly important to develop palliative care in rheumatology. Nevertheless, no specific data on trends are available for patients with SLE utilizing palliative care. Using the nationally representative inpatients data, we aimed to examine the 10-year trends of utilization of palliative care services among hospitalized patients with SLE and to assess how palliative care service affected hospital utilization and charges.
Study Population
Data Collection
The 2005-2014 National Inpatient Sample (NIS) database was used to obtain a population-based estimate of national trends for SLE. The NIS database was developed as a part of the Healthcare Charge and Utilization Project (HCUP) and is sponsored by the Agency for Healthcare Research and Quality (AHRQ). A comprehensive synopsis on NIS data is available at http://www.hcup-us.ahrq.gov. 10 The immense size of the NIS database provides an exceptional sample representation of the general US population. The NIS is the largest publicly available all-payer inpatient database in the United States and includes data from over 7 million hospital inpatient stays each year. It is designed to sample approximate 20% of nonfederal community hospitals from over 40 states in the United States and was capable of estimating the delivery of approximately 96% of all hospital inpatient stays in 2014. 10 It contains information on health-care utilization of hospitalizations classified by HCUP member hospitals and stratified by geographic region, hospital ownership, location, teaching status, bed-size, and other characteristics as indicated on the American Hospital Association Annual Survey of Hospitals. The analysis of the NIS uses completely deidentified data with no risk of loss of confidentiality. We completed a data use agreement with the AHRQ prior to using the NIS database. Since the NIS database provides administrative data after a complete deidentification, the need for an institutional review board approval was waived by the University of Nevada Las Vegas.
Patient Selection Process
The patient selection process is summarized in Supplementary Figure 1. We applied survey weights and adjustment to provide annual national population estimates. We applied survey weights available in the NIS data and adjustment to arrive at the annual national population estimates. Modified discharge weights “trendwt” were used from 2005 to 2012, and redesigned discharge weights “discwt” were used from 2012 to 2014. Among 382 516 561 patients included in the 2005-2014 Weighted NIS data set, 1 736 243 (0.45%) patients were identified as having SLE as a primary or secondary diagnosis by using the International Classification of Diseases, Ninth Revision, Clinical Modification (ICD-9-CM) code 710.0. We excluded 269 117 participants with missing individual and/or hospital variables and a total of 1 467 126 patients with SLE was included in our final analysis.
Variables of Interest
Patient-level characteristics included age, sex, race, median household income, primary payer (Medicare, private insurance, Medicaid, uninsured, others), and number of comorbidities. All-patient refined diagnosis-related group (APR-DRG) was used to classify the severity of illness (0 [lowest]-4 [highest]). 11 Hospital characteristics included information regarding teaching status, location, and bed-size. The main outcomes included the trend of palliative care by year, factors affecting hospital palliative care, and associations between palliative care service in hospital and in-hospital mortality, LOS, and hospital charges. Total hospital charges were calculated after adjusting for the annual inflation rate using Centers for Medicare and Medicaid Services estimates. 12
Statistical Analysis
In order to represent the entire patients with SLE without biased estimates, sampling weights were used in all statistical analyses. The compound annual growth rate (CAGR) was used to quantify temporal trends of palliative care. Compound annual growth rate supposed that year A is x and year B is y, CAGR = (y/x)1/(B-A)−1 and its statistical significance was tested using Rao-Scott correction for χ2 tests for categorical variables and has been widely used for health-care valuation. 13,14 The patient and hospital characteristics were presented as means with standard deviation or percentages. The proportion of palliative care and the mean values of LOS and hospital charges were summarized using the general linear model for continuous variables and the χ2 tests for categorical variables across the 2005-2014 NIS phases. The odds ratios (ORs) and 95% confidence intervals (95% CIs) for receiving hospital palliative care among SLE patients were calculated using the generalized multiple logistic regression analyses. We investigated how is hospital palliative care associated with in-hospital mortality, LOS, and hospital charges using multivariate linear and logistic regression analyses. All statistical analyses were performed using SAS version 9.4 (SAS Institute Inc, Cary, North Carolina). All statistical tests were two-sided and statistical significance was determined at P < .05.
Results
Descriptive Characteristics and Annual Trend of Hospitalized Patients With SLE
From 2005 to 2014, a total of 1 467 126 patients diagnosed with SLE were discharged from US hospitals. Table 1 presents the patient and hospital demographics over the 10-year period. About 89% of the hospitalized patients were female. In the hospitalized patients, 52.3% were older than 50 years. The ages of 50 to 59 years (20.8%) was most common, followed by 40 to 49 years (19.3%), and 60 to 69 years (16.3%). White race was over 50% of the sample. Black race is around 30% and Hispanic race is around 12%; 88.9% of the hospitalized patients belonged to over the APR-DRG 2 severity of illness subclasses. The mean number of comorbidities was 3.20; 63.7% of patients were public health insurance beneficiaries (Medicare 45.7%, and Medicaid 18.0%). As year goes by, the rate of in-hospital mortality continued to decrease from 2.2% (2005) to 1.3% (2014). Figure 1 shows the annual temporal trends of palliative care utilization among inpatients during 2005-2014. The proportion of palliative care gradually increased during 2005-2014 from 0.1% to 1.2%. The compound annual growth rate of the receipt of palliative care was 30.75% over the 10-year period.
Patient and Hospital Characteristics of Hospitalizations Due to SLE (2005-2014, NIS).a
Abbreviations: APR-DRG, all-patient refined diagnosis-related group; NIS, National Inpatient Sample; SLE, systemic lupus erythematosus.
a Data are expressed as mean (standard deviation) or percentage. Percentages may not add to up to 100 due to rounding.

The trend of palliative care utilization among hospitalized patients with SLE in the United Sates, 2005-2014 (P value for trend < .001, Source: NIS). NIS indicates National Inpatient Sample; SLE, systemic lupus erythematosus.
Factors Associated With Hospital Palliative Care Among Patients With SLE
Table 2 shows the factors associated with the receipt of hospital palliative care among patients with SLE. The ORs for palliative care were lower among patients younger than 40 years than among older patients and in the Medicare beneficiaries than among patients on private insurance. Hispanic patients were less likely to receive palliative care service than white patients during the hospitalization. The lowest quartile household income group was less likely to receive hospital palliative care than the highest quartile group. Urban teaching hospitals more often provided palliative care than did nonteaching hospitals. Patient with higher severity of illness subclass, APR-DRG 3 or 4 were more likely to receive palliative care than less severe patients.
Factors Associated With Hospital Palliative Care Among Patients With SLE (2005-2014, NIS).
Abbreviations: APR-DRG, all-patient refined diagnosis-related group; CI, confidence intervals; NIS, National Inpatient Sample; SLE, systemic lupus erythematosus.
Trends of the LOS, In-Hospital Mortality, and Hospital Charges
Figure 2 illustrates the annual temporal trends of the average LOS of patients with SLE. The average LOS decreased from 5.87 days in 2005 to 5.10 days in 2014 (CAGR = −1.55%, P < .001). Figure 3 illustrates the annual temporal trends of unadjusted and annual inflation-adjusted hospital charges per discharge during 2005-2014. The crude hospital charges per hospitalization of patients with SLE appeared to increase annually, but, after adjustment for annual inflation during the 10-year period, the total charge actually decreased (CAGR = −0.43%, P < .0001).

The temporal trend of the average length of stay among hospitalization with SLE in the United Sates, 2005-2014 (P value for trend < .001, Source: NIS). NIS indicates National Inpatient Sample; SLE, systemic lupus erythematosus.

The temporal trend of total hospital cost among hospitalization with SLE in the United Sates, 2005-2014. Annual inflation-adjusted. (P value for trend < .001, Source: NIS). SLE indicates systemic lupus erythematosus.
Supplementary Tables 1, 2, and 3 show the results of multiple regression analysis of independent associations of hospital palliative care with health-care utilization and hospital charges. The relationship of hospital palliative care with LOS, in-hospital mortality and hospital charges remained after multivariate adjustment. Hospital palliative care was associated with the increased LOS (on average by 0.178 days, P < .001) and the increased rate of in-hospital mortality (OR, 48.18; 95% CI, 41.59-55.82), but it showed a cost-saving effect in hospital charges (β coefficient = −0.075, P = .009).
Discussion
Underutilization of Hospital Palliative Care for Patients With SLE
In our study, the utilization of hospital palliative care service for patents with SLE or SLE-related condition gradually increased during 2005-2014 from 0.1% to 1.2%. The CAGR of the receipt of palliative care was 30.75% over the 10-year period. However, overall proportion of palliative care service was 0.6% for 10 years.
We speculate might that there were some barriers in the access to hospital palliative care for these patients during hospitalization. The proportion of utilization was lower than other chronic noncancer disease such as chronic obstructive pulmonary disease. The patients with less severity of illness and younger patients were less likely to receive palliative care services than patients with a higher risk of in-hospital mortality and older patients. This trend results the hospital palliative care is associated with higher in-hospital mortality (OR, 48.18; 95% CI, 41.59-55.82). Cho et al indicated several reasons why palliative care has not previously been explored in the field of rheumatology. 15 Firstly, staging does not inform prognosis in SLE, unlike malignancies or organ failure. Secondly, in contrast to metastatic cancers, a long period may lapse between the diagnosis of SLE and death. Thirdly, the deaths may not be attributable to systemic rheumatic diseases themselves. 15 In most studies, the 3 major causes of death are active SLE or associated organ failure, infection, and cardiovascular disease. 16,17 Deaths from infections or cardiovascular events may outnumber deaths from the systemic rheumatic disease itself. 18,19 We identified a lower OR regarding in-hospital mortality and the primary diagnosis of SLE in our study (OR, 0.65; 95% CI, 0.57-0.75). There may be unmet needs about hospital palliative care for systemic rheumatic disease among hospitalists or physicians for the hospitalized patient.
Disparities in the Utilization of Hospital Palliative Care for Patients With SLE
In addition to underutilization, recognizable disparities in access to hospital palliative care for patients with SLE were noticed. Patients younger than 40 years, the lower household income group or lower severity of illness subclass, and Medicare beneficiaries were less likely to receive hospital palliative care.
In real practice, when the physician interviews the younger patients with nonmalignancy progressive disease, most of them might feel more difficulty to refer the patient to palliative care consultation and hospice. Yelin et al found low house hold income patients did not receive the proper treatment and services for SLE base on the result of “Lupus Outcomes Study in 2009.” 20 From our data, we conclude that hospitalized patient with SLE in low household income group less receive the palliative care service as well.
In our study, over 45% of hospitalized patient with SLE are covered by Medicare. Compared to private insurance beneficiaries, Medicare beneficiaries were less likely to receive palliative care service. The higher prevalence of SLE overall Medicare beneficiaries is seen by Medicare claim study. 21 This study showed a higher prevalence of SLE in the disabled cohort (about 1.0%) compared with the SLE patients over 65 years of age (about 0.2%). In this context, underutilization of palliative care among younger patients with SLE could explain the disparity among patients younger than 65 years with SLE who require long-term dialysis for chronic kidney disease or require kidney transplantation in Medicare disabled cohort.
Relationship of the LOS, Hospital Charges, In-Hospital Mortality, and Hospital Palliative Care for Patients With SLE
Another finding of our study is that the application of hospital palliative care for patients with SLE may be affected by health-care utilization and charges in different ways. Most previous studies have reported that early introduction of palliative care shows favorable effects on health-care utilization and charge such as decreased LOS, in-hospital mortality, and hospital charges. 7,8 Our results are consistent with those of the previous findings in terms of LOS and hospital charges but are contradictory to regarding in-hospital mortality.7 ,8 It has been estimated that the cost-savings from early palliative care accrue due to both reduced LOS and reduced intensity of treatment. In a recent meta-analysis of 6 observational studies regarding the economics of hospital palliative care, May et al reported that early hospital palliative care within 3 days of admission reduced hospital charges among patients with cancer by US$4251 and among noncancer patients with life-limiting illness by US$2105, compared to usual care. 8 By reducing hospital LOS, palliative care has been shown to reduce charges by 25% to 66%. 22 However, our findings indicate that receipt of palliative care is associated with a longer LOS among hospitalized patients with SLE. Moreover, we found that receipt of palliative care is also positively associated with in-hospital mortality even though there was a decreased in-hospital mortality rate from 2.2% (2005) to 1.3% (2014). Previous studies have shown that hospital palliative care reduced hospital LOS and in-hospital mortality in the intensive care unit for terminally ill patients. 23 These discrepancies in LOS and in-hospital mortality between our study and previous studies are not fully understood. It may be difficult to differentiate between SLE progression versus comorbidities that cause acute declines such as infections, cardiovascular disease, other steroid induced side effects, or cerebrovascular accidents which may or may not be reversible. 24,25 Thus, this may lead to late referrals during hospitalizations for hospital-based palliative care consultation which may account for the increased LOS and in-hospital mortality. 8
Limitations and Strengths of the Study
Our study has some limitations. First, we relied on the ICD-9-CM code V66.7 for palliative care, which might have limited accuracy or sensitivity for capturing inpatient palliative care due to incorrect or missing data. In a similar context, using the ICD-9-CM code 710 for SLE diagnosis could lead to misclassification of disease or low positive predictive values. However, the ICD-9-CM code for identifying lupus patient has been validated by prior studies. 26 -29 Second, our study population was limited to the hospital inpatient setting, so our findings cannot be generalized and applied to outpatient and home-based palliative care settings.
Despite these potential limitations, we believe this is the first study to report several new insights into the current state of hospital palliative care and associated with health-care utilization and hospital charges for patients with SLE. And this is a highly powered study where it is easier to find a statistical effect and multiple comparisons. The recent 10-year trends of palliative care utilization for patients with SLE based on nationally representative data will be useful for epidemiological research, health policy development, and clinical use.
In conclusion, the temporal trends of palliative care among hospitalized patients with SLE indicated a gradual increase during 2005-2014 in US hospital. However, still small proportion of the patients received palliative. And the patients with a higher risk of in-hospital mortality and older patients mainly received palliative care. So, hospital palliative care was associated with increased LOS and in-hospital mortality. Earlier referral of hospitalized patients with SLE for palliative care may improve the efficiency of the care with regard to further reducing in-hospital mortality, LOS, and total hospital charges.
Supplemental Material
Supplemental Material, FSuppl_(1) - Trends of Hospital Palliative Care Utilization and Its Associated Factors Among Patients With Systemic Lupus Erythematosus in the United States From 2005 to 2014
Supplemental Material, FSuppl_(1) for Trends of Hospital Palliative Care Utilization and Its Associated Factors Among Patients With Systemic Lupus Erythematosus in the United States From 2005 to 2014 by Kaylee G. Yu, Jay J. Shen, Pearl C. Kim, Sun Jung Kim, Se Won Lee, David Byun, Ji Won Yoo and Jinwook Hwang in American Journal of Hospice and Palliative Medicine®
Supplemental Material
Supplemental Material, Supplementary_Tables_(1) - Trends of Hospital Palliative Care Utilization and Its Associated Factors Among Patients With Systemic Lupus Erythematosus in the United States From 2005 to 2014
Supplemental Material, Supplementary_Tables_(1) for Trends of Hospital Palliative Care Utilization and Its Associated Factors Among Patients With Systemic Lupus Erythematosus in the United States From 2005 to 2014 by Kaylee G. Yu, Jay J. Shen, Pearl C. Kim, Sun Jung Kim, Se Won Lee, David Byun, Ji Won Yoo and Jinwook Hwang in American Journal of Hospice and Palliative Medicine®
Footnotes
Acknowledgments
Declaration of Conflicting Interests
The authors declared no potential conflicts of interest with respect to the research, authorship, and /or publication of this article.
Funding
The authors received no financial support for the research, authorship, and/or publication of this article.
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References
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