Inpatient palliative care in metastatic adrenocortical carcinoma: a retrospective analysis using the National Inpatient Sample database
Letizia M. JANNELLO 1, 2, 3 *, Carolin SIECH 1, 4, Andrea BAUDO 1, 5, Mario de ANGELIS 1, 6,7, Francesco DI BELLO 1, 8, Jordan A. GOYAL 1, Zhe TIAN 1, Stefano LUZZAGO 2, 9, Francesco A. MISTRETTA 2, 9, Elisa de LORENZIS 3, Fred SAAD 1, Felix K. CHUN 4, Alberto BRIGANTI 6, 7, Luca CARMIGNANI 5, 10, Nicola LONGO 8, Ottavio de COBELLI 2, 9, Gennaro MUSI 2, 9, Pierre I. KARAKIEWICZ 1
1Cancer Prognostics and Health Outcomes Unit, Division of Urology, University of Montréal Health Center, Montréal, QC, Canada; 2Department of Urology, IEO European Institute of Oncology IRCCS, Milan, Italy; 3University of Milan, Milan, Italy; 4Department of Urology, University Hospital, Goethe University Frankfurt, Frankfurt am Main, Germany; 5Department of Urology, IRCCS San Donato Polyclinic Hospital, Milan, Italy; 6Vita- Salute San Raffaele University, Milan, Italy; 7Unit of Urology, Division of Experimental Oncology, IRCCS San Raffaele Hospital, Milan, Italy; 8Department of Neurosciences, Science of Reproduction and Odontostomatology, University of Naples Federico II, Naples, Italy; 9Department of Oncology and Hemato-Oncology, University of Milan, Milan, Italy; 10Department of Urology, IRCCS Galeazzi - Sant’ Ambrogio Hospital, Milan, Italy
*Corresponding author: Letizia M. Jannello, Cancer Prognostics and Health Outcomes Unit, Division of Urology, University of Montréal Health Center, Montréal, QC, Canada. E-mail: letizia.jannello@unimi.it
ABSTRACT
BACKGROUND: The use of inpatient palliative care (IPC) in advanced cancer patients represents a well-established guideline recommendation. This study examines the utilization rates and patterns of IPC among patients with metastatic adrenocortical carcinoma (mACC).
METHODS: Relying on the Nationwide Inpatient Sample database (2007-2019), we tabulated IPC rates in mACC patients. Estimated annual percentage changes (EAPC) analyses as well as multivariable logistic regression models (MLRM) predicting IPC use were fitted.
RESULTS: Of 2040 mACC patients, 238 (12%) received IPC. Overall, the rate of IPC increased from 3.7% to 19.1% be- tween 2007 and 2019 (EAPC +9.6%, P=0.001). During the same period, in-hospital mortality remained unchanged from 12.1 to 13.8% (EAPC 0.1%; P=0.97). Younger age at admission (<60 years; MLRM OR=0.70, P=0.013), solitary meta- static site (OR=0.63; P=0.015), and non-brain metastases (OR=0.62; P=0.033) were all associated with lower IPC use. CONCLUSIONS: In mACC patients, IPC use has increased from a marginal 3.7% to a moderate annual value of 19.1% in the most recent study year. These rates were not driven by a concomitant increase in in-hospital mortality (12.1% to 13.8%; P=0.9). and may be interpreted as an improvement in quality of care. Despite this encouraging increase, some patient characteristics herald lower IPC use. In consequence, younger patients, those with solitary metastatic sites, and non-brain metastases should be carefully considered for IPC to decrease or completely reduce the IPC access barrier maximally.
(Cite this article as: Jannello LM, Siech C, Baudo A, de Angelis M, Di Bello F, Goyal JA, et al. Inpatient palliative care in metastatic adrenocortical carcinoma: a retrospective analysis using the National Inpatient Sample database. Minerva Endocri- nol 2025;50:415-22. DOI: 10.23736/S2724-6507.24.04185-X)
KEY WORDS: Palliative care; Hospital mortality; Adrenocortical carcinoma; Neoplasm metastasis.
A drenocortical carcinoma (ACC) is a rare malignancy characterized by its high ag- gressiveness and heterogeneity.1 Regardless of age, ACC shows a slight female predilection (1.5-2.5:1).2 Its reported incidence was 0.7 per million cases per year in the USA and 1 per mil- lion cases in Europe.3,4 This rarity poses signifi- cant challenges in diagnosing and managing the disease, with many medical centers having mini- mal experience in its treatment.5
In clinical practice, ACC is often discovered as a metastatic stage, where treatment options are limited, with mitotane as the cornerstone therapy. Conversely, localized disease offers the possibility of curative resection through surgery. In addition to surgical and pharmacological in- terventions, other modalities such as chemo- therapy, radiation therapy, and targeted therapies may also be employed, although their efficacy remains variable.6, 7 Despite advancements in treatment modalities, the overall prognosis for patients with ACC, particularly those with meta- static stage, remains guarded. Supportive and simultaneous approaches involve the prevention and management of the adverse events/effects of cancer and cancer-related treatment in patients with good survival prognoses in short- to mid- term periods. Palliative care plays a pivotal role in the management of ACC, particularly in the advanced stages.8, 9 It enhances their quality of life, reduces the length of their hospital stay, and decreases health expenses.4, 10, 11 Addition- ally, access to inpatient palliative care (IPC) is an indicator of high-quality care.12, 13 IPC use is recommended by the guidelines of the National Comprehensive Cancer Network (NCCN),14 the American Association of Clinical Endocrinol- ogy,15 and the European ESE/ENSAT.3 However, data regarding palliative care use in metastatic ACC (mACC) patients are rare,16 and contempo- rary rates and patterns of IPC use are unavailable. While IPC is widely recommended for advanced cancer patients, its utilization patterns in mACC remain poorly understood. This study aims to assess the rates and trends of IPC utilization in mACC patients, shedding light on factors associ- ated with its use.
We hypothesized that rates of guideline-rec- ommended IPC use may have increased over
time. Moreover, we postulated that IPC use did not differ according to hospital or patient char- acteristics. To test these hypotheses, we relied on a contemporary population-based cohort of mACC patients within the United States.
Materials and methods
Data source and study population
Relying on discharge data from the National Inpatient Sample and the Nationwide Inpatient Sample (NIS) from 2007 to 2019, we assessed IPC use in mACC patients. The NIS is a set of longitudinal hospital inpatient databases includ- ed in the Healthcare Cost and Utilization Project (HCUP) and formed by the Agency for Health- care Research and Quality (AHRQ) through a federal-state partnership.17 All diagnoses and procedures were coded using the International Classification of Disease (ICD) 9th revision Clinical Modification (ICD-9-CM), ICD 10th revision Clinical Modification (ICD-10-CM), as well as ICD 10th revision Procedure Coding Sys- tem (ICD-10-PCS).
Study population
We focused on patients aged ≥18 years with a diagnosis of adrenocortical carcinoma (ICD-9- CM codes 194.0, and ICD-10-CM codes C74, C74.0, C74.1, C74.9, C74.90) and a secondary diagnosis of metastatic cancer stage (ICD-9-CM codes 196.0-196.3, 196.5-196.9, 197.0-197.5, 1977-1978, 198.1-198.6, 1988, 1988.1-1988.2, 1988.9, and ICD-10-CM codes C77.0-C77.1, C77.3-C77.5 C77.8, C78.x, C79.x). Since the contiguous invasion of the kidney is common in mACC and does not meet the criteria for distant metastases, we excluded patients with exclusive kidney metastases (ICD-9-CM codes 198.0, and ICD-10-CM codes C79.0x).
Variables and outcome of interest
The primary endpoint of the study, IPC use, was identified by ICD-9-CM V66.7 and ICD-10-CM code Z51.5, according to prior methodology.18, 19 For each patient the following variables were recorded: age at admission (<60 versus ≥60 years), sex (male versus female), race/ethnicity
(Caucasian versus African American versus oth- ers), hospital geographical region (West versus Midwest versus Northeast versus South), teach- ing hospital status (teaching versus nonteaching), hospital size (large [≥400 beds] vs. medium [200- 399 beds] vs. small [<200 beds]), as well as num- ber (single vs. multiple metastases), and location of metastatic sites (liver [yes versus no], bone [yes versus no], lymph nodes [yes versus no], lung [yes versus no], and brain [yes versus no]).
Statistical analysis
Three analytical steps were completed. First, de- scriptive characteristics were tabulated. Medians and interquartile ranges (IQR) were reported for continuously coded variables. Wilcoxon rank sum test examined the statistical significance of medians’ differences. For categorical variables, frequencies and proportions were reported. Pear- son’s Chi-square Test assessed the statistical sig- nificance of the proportions’ differences. Second, estimated annual percentage changes (EAPC) were tested with the least squares linear regres- sion in the overall cohort and subgroup focus-
ing on hospital and patient characteristics. Third, univariable and multivariable logistic regression models (MLRM) with generalized estimation equations were fitted to predict IPC use. Ad- justment variables included patient and hospital characteristics.
All statistical tests were two-sided, with the level of significance set at P<0.05, and were per- formed with R Software Environment for Statis- tical Computing and Graphics (R version 4.1.3; R Foundation for Statistical Computing, Vienna, Austria). 20
Results
Descriptive characteristics
Within the NIS database (2007-2019), we iden- tified 2,040 mACC patients (Table I). Of those, 238 (12%) manged with IPC, and of these 62 (26%) died in hospital.
IPC patients were older (59 vs. 54 years; P<0.001) and its use was more frequent among African Americans (16%) compared to Cau- casians (12%) and other races/ethnicities (9%) (P=0.03). Moreover, patients with brain metas-
| Characteristics | IPC (N .= 238; 12%) | No IPC (N .= 1802; 88%) | P value |
|---|---|---|---|
| Age at admission (year) | 59 (47-69) | 54 (41-65) | <0.001 |
| Young (<60 years) | 125 (10%) | 1116 (90%) | |
| Old (≥60 years) | 113 (14%) | 686 (86%) | |
| Race/ethnicity | 0.03 | ||
| Caucasians | 156 (12%) | 1152 (88%) | |
| African Americans | 33 (16%) | 171 (84%) | |
| Others | 49 (9%) | 479 (91%) | |
| Year interval | <0.001* | ||
| 2007-2011 | 101 (8%) | 1105 (92%) | |
| 2012-2019 | 137 (16%) | 697 (84%) | |
| Metastatic sites | <0.001* | ||
| Solitary site | 81 (9%) | 861 (91%) | |
| Multiple sites | 157 (14%) | 941 (86%) | |
| Location of metastatic sites | |||
| Lung | 116 (13%) | 755 (87%) | 0.045* |
| Liver | 118 (13%) | 812 (87%) | 0.2 |
| Brain | 31 (18%) | 140 (82%) | 0.006* |
| Lymph nodes | 23 (9%) | 232 (91%) | 0.2 |
| Bone | 91 (14%) | 558 (86%) | 0.024* |
| In-hospital death | 62 (34%) | 119 (66%) | <0.001* |
| Median total hospital charges (US $) | 42,234 (21,324-87,849) | 40,598 (21,157-81,675) | 0.8 |
| *Statistically significant difference. |
50
45
· Mortality: 0.1% (95% CI: - 5.4 to +5.6%; P=0.97)
40
· IPC: +9.6% (95% CI:+5.7 to +14.1%; P=0.001)
35
Rates (%)
30
25
20
20.8
15
18.5
19.8
17.3
19.1
11
10
12.1
13.8
11.4
10.6
10.3
11.9
8.1
10.8
5
8.6
8.7
7.1
7
8.5
3.7
5.5
0
2007
2008
2009
2010
2011
2012
2013
2014
2015
2016
2017
2018
2019
Year
tases (18%), bone metastases (14%), lung metas- tases (13%), and multiple metastatic sites (14%) more frequently benefit from IPC (all P<0.05). Conversely, no statistically significant differ- ences were recorded according to patient sex, teaching hospital status, hospital size, and total hospital charges.
Temporal trends of IPC use and inpatient mor- tality
IPC use in mACC patients increased from 3.7% in 2007/2008 to 19.1% in 2019 (EAPC +9.6%; 95% CI: +5.7 to +14.1%; P=0.001; Figure 1). Conversely, in-hospital mortality remained sta- ble across the study period, from 12.1% in 2007 to 13.8% in 2019 (EAPC +0.1%, 95% CI: - 5.4 to +5.6%; P=0.97; Figure 1).
Regarding age categories, IPC use increased from 4.2 to 14.1% in younger patients (<60 years) (EAPC +9.2%, 95% CI +1.1 to +18.5%; P=0.08), and from 7.7% to 23% in older patients (≥60 years) (EAPC +10.5%, 95% CI +5.5 to +16.4%; P=0.01). In subgroup analyses address- ing the number of metastatic sites, IPC use in- creased from 4.1% to 12.9% in patients with a solitary metastatic site (EAPC +9.9 95% CI +2.0 to +19.8%; P=0.09), and from 6.6% to 24.5% in patients with multiple metastatic sites (EAPC +10.0%, 95% CI +4.9 to +15.8%; P=0.008). Ac- cording to teaching hospital status, IPC uses in- creased from 4.5% to 19.2% in teaching hospitals (EAPC +9.5%, 95% CI +5.5 to +14.0%; P=0.002) and from 6.8% to 16.5% in nonteaching hospitals (EAPC +9.5%, 95% CI +0.5 to +22.4%; P=0.08).
| Parameter | Univariable | Multivariable | ||||
|---|---|---|---|---|---|---|
| OR | 95% CI | P value | OR | 95% CI | P value | |
| <60 years at admission (Ref. ≥60 years) | 0.71 | 0.54, 0.95 | 0.022* | 0.70 | 0.52, 0.93 | 0.013* |
| Single metastatic sites (Ref. multiple) | 0.56 | 0.43, 0.74 | <0.001* | 0.63 | 0.44, 0.91 | 0.015* |
| No lung metastasis (Ref. yes) | 0.78 | 0.60, 1.02 | 0.068 | 0.83 | 0.61, 1.13 | 0.240 |
| No liver metastasis (Ref. yes) | 0.81 | 0.62, 1.06 | 0.118 | 0.90 | 0.66, 1.22 | 0.500 |
| No brain metastasis (Ref. yes) | 0.56 | 0.37, 0.85 | 0.006* | 0.62 | 0.40, 0.96 | 0.033* |
| No bone metastasis (Ref. yes) | 0.73 | 0.55, 0.96 | 0.024* | 0.74 | 0.55, 1.01 | 0.056 |
| *Statistically significant difference. | ||||||
Univariable and multivariable risk factors anal- yses of IPC use
In univariable logistic regression models predict- ing IPC use, four variables achieved statistical significance, namely: younger age at admission, solitary metastatic site, absence of brain metas- tases, and absence of bone metastases (Table II). In the multivariable analyses, of these four variables, only three achieved the independent predictor status. Specifically, after adjustment only younger age at admission (OR 0.70, 95% CI: 0.52-0.93, P=0.013), solitary metastatic sites (OR 0.63, 95% CI: 0.44-0.91; P=0.015), absence of brain metastases (OR 0.62, 95% CI: 0.40- 0.96; P=0.033), remained independent predictors of lower IPC use.
Discussion
Relying on a contemporary population-based cohort of mACC patients within the NIS (2007- 2019), we tested for IPC use and its temporal trends. We made several noteworthy observa- tions.
First, adrenocortical carcinoma represents a rare malignancy with a poor prognosis.1 Howev- er, within adrenocortical carcinoma of all stages, the metastatic stage accounts for one-third of all new diagnoses.21 Specifically, the largest popula- tion of mACC patients was reported by Tella et al. using the National Cancer Database (NCDB, 2004-2015), where 760 mACC patients were identified.22 The second largest population of mACC patients was reported by Kebebew et al. using the Surveillance, Epidemiology, and End Results (SEER, 1973-2000), where 262 mACC patients were identified.23 Finally, even lower numbers (N .= 101) were reported from a Euro- pean multi-institutional cohort.24 In the current study, we identified the highest number of mACC patients (N .= 2040) over a 13-year study span. In consequence, large-scale population-based data- sets such as the NIS, NCDB, or SEER are essen- tial to study rare cancers, such as mACC, espe- cially when emphasis is placed on rare endpoints such as IPC use.
Second, the overall rate of IPC use was 12%. Despite this relatively low overall rate, the an-
nual rate increased from 3.7% to 19.1% in the study period. Interestingly, in-hospital mortality rates ranged from 12.1% to 13.8% during the same period and did not increase significantly. These observations suggest that over time clini- cians become more aware of IPC use. These pro- portions of IPC use and concomitant in-hospital mortality cannot be directly compared with other studies specifically addressing mACC, since such reports do not exist. However, compared to other primaries the overall 12% IPC use is rela- tively low. Specifically, the IPC use in metastatic lung cancer (50.1%) or metastatic breast cancer (28.3%) is among the highest.25, 26 Therefore, cli- nicians and oncology nurses caring for patients with mACC should be sensitized to increase the rates of interprofessional collaboration, ideally reaching levels observed in patients with other metastatic primaries.
Third, in the current cohort of 2040 mACC patients, we identify specific patient character- istics that were associated with lower IPC use. Specifically, IPC use was lower in younger pa- tients (10 vs.14%, P<0.001), in Caucasians and other race/ethnicity compared to African Ameri- cans (12 vs. 9 vs. 16%, P=0.03), in patients with a solitary metastatic site (9 vs. 14%, P<0.001), absence of lung (10 vs. 13%, P=0.045), brain (11 vs. 18%, P=0.006), or bone metastases (11 vs. 14%, P=0.024). From a clinical perspective, these characteristics should be considered as po- tential barriers to IPC use. However, it remains challenging to determine which patient charac- teristics warrant early IPC implementation based solely on previous experiences. Therefore, our findings underscore the need for further research to ascertain IPC’s effectiveness in improving survival rates and quality of life for patients with specific characteristics, such as younger age, soli- tary metastatic site, and absence of brain, lung, or bone metastasis. This would provide more con- crete evidence to guide clinical decision-making regarding IPC utilization. Finally, although these patient characteristics represent potential barri- ers to IPC use, we did record an annual increase in IPC use even in the presence of these patient characteristics. These observations are consistent with previous studies on other primaries where an increase over time was recorded for all IPC
patients as well as for specific patient or hospital characteristics.27, 28 However, a direct compari- son with previous reports addressing IPC use in mACC could not be made as such studies have not been published.
Fourth, we examined hospital characteris- tics to test for an association with IPC use. In- terestingly, neither teaching status nor hospital size represented predictors of IPC use. Interest- ingly, IPC use was lower in small- and medium- size hospitals than in large-size hospitals, even though IPC use increased in all three hospital siz- es. However, strict statistical significance could not be recorded for these observations. Equally interestingly, the annual increase in IPC use, was higher in large-size hospitals, than in medium- size, and small-size hospitals. Conversely, when hospital teaching status was accessed, no differ- ences in overall IPC use or the annual increase rate of IPC use were recorded.
Fifth, we tested for differences in characteris- tics between IPC vs. non-IPC patients to identify predictors of IPC use. In univariable analyses, we identified younger age at admissions (OR 0.71, P=0.022), solitary metastatic site (OR 0.56, P<0.001), absence of brain (OR 0.56, P=0.006), and absence of bone metastases (OR 0.73, P=0.024), as predictor of lower IPC use. Further- more, we examined several variables that have previously been identified as potential predictors of IPC utilization in other primaries, including sex, teaching hospital status, large-size hospitals, and presence of metastasis. However, these vari- ables did not achieve statistical significance in the current study.27-29 In multivariable risk factor analyses, only three variables independently pre- dicted lower IPC use. Specifically, we identified younger ages at admission (OR 0.70, P=0.013), a single metastatic site (OR 0.63, P=0.015), and non-brain metastases (OR 0.62, P=0.033) as in- dependent predictors of lower IPC use. It should be noted that further key variables that were con- sidered important in metastatic cancer patients, such as performance status, outpatient pallia- tive referral, the difference in laboratory values, symptom scores, and opioid use are not available in the NIS database.30 Consequently, these vari- ables could not be included in the current analy- ses for formal statistical testing.
Taken together, IPC use sharply increased from a marginal value of 3.7% to 19.1%. Addi- tionally, certain patient characteristics, such as younger age at admission (<60 years), solitary metastatic site, and non-brain metastases, were independently associated with lower IPC use. In consequence, patients harboring these char- acteristics should be identified early for poten- tial IPC implementation. Additionally, a non- significant trend towards lower IPC use was recorded in small- and medium-size hospitals, relative to large-size hospitals. These observa- tions should also be considered as a potential barrier to IPC use.
Limitations of the study
Despite its novelty, the present study is not de- void of limitations. First and foremost, we relied on a large-scale retrospective database. This lim- itation applies to all studies using retrospective databases such as SEER or NCDB. Additionally, we were unable to analyze several important data elements such as survival, depression, chronic pain, anxiety, and frequency of hospitalization associated with IPC utilization due to data con- straints. Second, we relied on previously estab- lished and validated methodologies for the iden- tification of IPC use as well as the study cohort selection. IPC definition is also based on ICD-9 and ICD-10 codes.18, 19 However, different IPC definitions or methodological approaches to identifying IPC patients are possible. Therefore, the use of other approaches may result in rates of IPC use that may not be directly comparable. Fi- nally, the NIS exclusively provides inpatient data. However, palliative care can also be delivered in outpatient or home-based settings.4, 12, 13 There- fore, inpatient data may underestimate overall rates of palliative care use including outpatient and inpatient care. However, the current study adheres to the methodology of previous studies addressing IPC use.28, 31
Conclusions
In mACC patients, IPC use has increased from a marginal 3.7% to a moderate annual value of 19.1% in the most recent study year. These rates were not driven by a concomitant increase in in-
hospital mortality (12.1% to 13.8%; P=0.9). and may be interpreted as an improvement in qual- ity of care. Despite this encouraging increase, patient characteristics herald lower IPC use. In consequence, younger patients, those with solitary metastatic sites, and no brain metasta- ses should be carefully considered for IPC to decrease or completely reduce the IPC access barrier maximally.
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Conflicts of interest
The authors certify that there is no conflict of interest with any financial organization regarding the material discussed in the manu- script.
Authors’ contributions
All authors read and approved the final version of the manuscript.
History
Article first published online: September 30, 2024. - Manuscript accepted: May 21, 2024. - Manuscript revised: May 13, 2024. - Manuscript received: January 19, 2024.