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. Author manuscript; available in PMC: 2023 Dec 20.
Published in final edited form as: Int J Gynecol Cancer. 2022 Sep 6;32(9):1135–1140. doi: 10.1136/ijgc-2022-003484

Frailty is independently associated with worse outcomes and increased resource utilization following endometrial cancer surgery

Morcos Nakhla 1, Cortney M Eakin 1, Ava Mandelbaum 2, Beth Karlan 1, Peyman Benharash 2, Ritu Salani 1, Joshua G Cohen 1
PMCID: PMC9763544  NIHMSID: NIHMS1820863  PMID: 35725031

Abstract

Objective

Frailty has been associated with poorer surgical outcomes and is a critical factor in procedural risk assessment. The objective of this study is to assess the impact of frailty on surgical outcomes in patients with endometrial cancer.

Methods

Patients undergoing inpatient gynecologic surgery for endometrial cancer were identified using the 2005–2017 Nationwide Inpatient Sample database. The Johns Hopkins Adjusted Clinical Groups frailty-defining diagnosis indicator was used to designate frailty. Multivariate regression models were used to assess the association of frailty with postoperative outcomes and resource use.

Results

Of 339 846 patients, 2.9% (9868) were considered frail. After adjusting for patient and hospital characteristics, frailty was associated with a four-fold increase in inpatient mortality (adjusted OR (aOR) 4.1; p<0.001), non-home discharge (aOR 5.2; p<0.001), as well as increased respiratory (aOR 2.6; p<0.001), neurologic (aOR 3.3; p<0.001), renal (aOR 2.0; p<0.001), and infectious (aOR 3.2; p<0.001) complications. While frail patients exhibited increased mortality with age, the rate of mortality in this cohort decreased significantly over time. Compared with non-frail counterparts, frail patients had longer lengths of stay (7.6 vs 3.4 days; p<0.001) and increased hospitalization costs with surgical admission ($25 093 vs $13 405; p<0.001).

Conclusions

Frailty is independently associated with worse surgical outcomes, including increased mortality and resource use, in women undergoing surgery for endometrial cancer. Though in recent years there have been improvements in mortality in the frail population, further efforts to mitigate the impact of frailty should be explored.

INTRODUCTION

Endometrial cancer remains the most common gynecologic malignancy and the fourth most common cancer overall among women in the USA.1 Unfortunately, it is also one of the few cancers that is reported to have both an increasing incidence and mortality with a death rate that continues to rise by 2% each year. Several factors may be responsible for these trends. The staggering rise of obesity in concordance with an increasingly diverse and aging population are likely responsible for the rising number of endometrial cancer cases.2–4 Between 2010 and 2030, the number of US adults 65 years or older is anticipated to increase from 40.3 million to 73 million with a corresponding 67% increase in cancer incidence. As the majority of endometrial cancer cases occur in women over the age of 70, it is likely that endometrial cancer rates will continue to rise as the population in the USA ages.4 5

Frailty is a syndrome characterized by a loss of biological reserves resulting in decreased resilience to stress and increased vulnerability to a range of adverse outcomes.6 Frailty can be characterized by unintentional weight loss (>10 pounds (>4.5 kg) in the past year), self-reported exhaustion, weakness (assessed by grip strength), slow walking speed, and low physical activity.7 Several studies have reported increased mortality, complication rates, and costs associated with frail patients who underwent various operations when compared with same-age counterparts.8–12

While frailty and age are highly correlated, they are not equivalent. Rather, frailty is defined by the complex interplay between genes and the environment that occurs over time, resulting in molecular and cellular damage across organ systems.6 The aspects of the environment that determine physical activity, malnutrition, and social support have an impact on the level of dysfunction experienced. While the prevalence of frailty increases with age, evidence suggests that the symptoms of frailty can be reversed through interventions targeting these environmental determinants.13 Thus, addressing the needs of frail patients perioperatively presents a key clinical opportunity to address disparities and to improve surgical outcomes. In this study, we sought to assess the impact of frailty on postoperative outcomes in patients with endometrial cancer.

METHODS

Discharge information for all adult patients (age ≥18 years) undergoing surgery for endometrial cancer was obtained from the 2005–2017 Nationwide Inpatient Sample database using best practices as reported by Khera et al.14 The National Inpatient Sample is the largest, all-payer inpatient database, sampling 20% of all hospitalizations in the USA.15 16 Using validated methodology and survey-weighting algorithms, the Nationwide Inpatient Sample provides accurate national estimates for 97% of all US hospitalizations, drawing information from all states that participate in the Healthcare Cost and Utilization Project (HCUP) (47 states in 2017). This study was deemed exempt by the Institutional Review Board at the University of California, Los Angeles, given the de-identified nature of the Nationwide Inpatient Sample.

The study cohort was identified in the Nationwide Inpatient Sample using the International Classification of Diseases, 9th and 10th editions, Clinical Modification (ICD-9-CM and ICD-10-CM) codes. Patients were included if they had a diagnosis code for endometrial cancer and a procedure code for any surgery involving oophorectomy, hysterectomy, pelvic or aortic lymph node dissection, omentectomy, or trachelectomy (Online supplemental 1). Patient characteristics collected include patient age, race, income quartile of residential ZIP code, primary payer, discharge disposition, and comorbidities as included in the Nationwide Inpatient Sample. Hospital characteristics included teaching status, size, region, and urban or rural location. Hospitals were also categorized into tertiles based on operative volume using the annual number of endometrial cancer operations reported, as our group has implemented in prior database studies.17 Patients <18 years of age as well as those missing age, insurance, and survival data were excluded. We also excluded patients who were not designated as having elective admissions. Elective admissions were defined as hospitalizations for which ‘elective’ was indicated as the admission type in the Nationwide Inpatient Sample, although this is not further clarified within the database.

Patients were further categorized into frail and non-frail cohorts. Frail patients were identified using the Johns Hopkins Adjusted Clinical Groups frailty-defining diagnosis indicator. This multidimensional instrument utilizes 10 clusters of frailty-defining diagnoses (malnutrition, dementia, impaired vision, decubitus ulcer, incontinence of urine, loss of weight, poverty, barriers to access of care, difficulty in walking, and falls) to designate frailty, and has been validated for research using administrative data (Online supplemental file 1).18–20

Non-home discharge disposition as defined by the Nationwide Inpatient Sample includes patients released to a specialty hospital, skilled nursing facility, or another healthcare facility. The Elixhauser Comorbidity Index was used to assess the burden of chronic conditions. The Elixhauser Comorbidity Index algorithm uses ICD-9-CM and ICD-10-CM codes to identify 30 comorbidities thoroughly validated for use in administrative databases.17 Extended procedures were defined using methods previously published by Jones et al and encompassed any procedure involving concomitant resection of the stomach, spleen, liver, diaphragm, small or large bowel, or rectosigmoid colon, or any procedure resulting in ileostomy or colostomy.21

The primary outcome of the study was in-hospital mortality. Secondary outcomes included length of stay, procedure complications, discharge disposition, and adjusted hospitalization costs. All complications were determined using ICD-9-CM and ICD-10-CM codes. Respiratory complications include pneumonia, pneumo-thorax, respiratory failure, acute respiratory distress syndrome, and prolonged mechanical ventilation. Neurologic complications include intracranial hemorrhage, acute ischemic stroke, and other stroke complications. Renal complications include acute kidney injury and end-stage chronic kidney disease. Infectious complications include sepsis and surgical site infection. Cost analysis was performed using the ‘total charges’ variable included in the Nationwide Inpatient Sample, which accounts for charge of hospitalization and does not include professional fees or non-covered charges. The Nationwide Inpatient Sample cost-to-charge ratios were used to calculate cost, which was consequently adjusted by annual gross domestic product, as published by the US Bureau of Economic Analysis, to obtain our final estimates of hospitalization cost. The value presented represents the total cost of hospitalization. Multivariate regression models were used to assess the impact of frailty on outcomes.

All statistical analysis was performed using Stata 15.1 (StataCorp, College Station, TX). All analysis was performed on survey-weighted data to generate national estimates, as provided by the Nationwide Inpatient Sample. Adjusted Wald tests were used to perform univariate analysis of continuous variables, and χ2 analysis was used to compare categorical variables. Multivariable logistic regression was performed to assess frailty as a predictor of outcomes, reported as adjusted odds ratios (aOR). A p value <0.05 was considered statistically significant. In accordance with the journal’s guidelines, we will provide our data for the reproducibility of this study in other centers if such is requested.

RESULTS

Of 339 846 hospitalizations for endometrial cancer surgery during the study period, 9868 (2.9%) involved frail patients (Figure 1) (Online supplemental 2). Frail patients were on average older (69 vs 63 years; p<0.001) and had a greater burden of comorbidities according to the Elixhauser Comorbidity Index (4.0 vs 3.0; p<0.001). While non-frail patients exhibited an increase in average age over the study duration, from 62 years in 2005 to 64 years in 2017 (p<0.001), frail patients exhibited a decrease in age, from 73 in 2005 to 67 in 2017 (p<0.001). Frail patients were also more likely to be of Black race (13% vs 10%; p<0.001) and from the lowest income quartile (26% vs 22%; p<0.001). Compared with their non-frail counterparts, frail patients were more likely to be treated at teaching hospitals (79% vs 73%; p<0.001) and in the Southern US region (33% vs 29%; p=0.002), and were more likely to undergo open surgery (77% vs 71%; p<0.001). Table 1 shows the demographics and specific comorbidities. Of note, frail patients were more likely to be diagnosed with congestive heart failure (8% vs 3%; p<0.001), diabetes mellitus (28% vs 24%; p<0.001), and liver disease (3% vs 1%; p<0.001).

Figure 1.

Figure 1

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The study population was determined using this algorithm. Inclusion criteria included endometrial cancer diagnosis with one or more concurrent surgical procedure listed.

Table 1.

Demographics and comorbidities by frail status

Frail 9868 (2.9%) Non-frail 329 978 (97.1%) P value
Age (years) 69.0 62.6 <0.001
Elixhauser Comorbidity Index 4.0 3.0 <0.001
Comorbidities (%)
 Congestive heart failure 7.6 3.3 <0.001
 Diabetes 28.4 23.9 <0.001
 Obesity 24.7 28.3 <0.001
 Chronic lung disease 14.4 11.4 <0.001
 Obstructive sleep apnea 5.2 4.2 <0.001
Extended procedure (%) 10.1 2.5 <0.001
Minimally invasive procedure (%) 22.6 29.0 <0.001
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After adjusting for patient and hospital characteristics, frailty was associated with a four-fold increase in inpatient mortality (aOR 4.1; p<0.001). Furthermore, frailty predicted a significantly higher rate of mortality in patients with older age, even after adjusting for relevant variables (Figure 2). Specifically, frail patients >45 years of age had a significantly increased probability of in-hospital mortality compared with their non-frail counterparts, and this probability increased with age. However, throughout the study duration, mortality rates decreased significantly for frail patients, approaching the mortality rate for non-frail patients (Figure 3).

Figure 2.

Figure 2

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Frailty predicted a significantly higher rate of mortality for patients beyond their fifth decade of life even after adjustment for demographic, clinical, surgical, and hospital variables.

Figure 3.

Figure 3

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The rate of mortality decreased for frail patients throughout the study period, though it still remained significantly higher than the mortality rate for non-frail counterparts.

Frailty also independently predicted increased odds of non-home discharge (aOR 5.2; p<0.001), as well as respiratory (aOR 2.6; p<0.001), neurologic (aOR 3.3; p<0.001), renal (aOR 2.0; p<0.001), and infectious (aOR 3.2; p<0.001) complications. Compared with non-frail counterparts, frail patients also had longer lengths of stay (7.6 days vs 3.4 days; p<0.001) and increased hospitalization costs with surgical admission ($25 093 vs $13 405; p<0.001) (Table 2). On multivariate analysis, frailty independently predicted a 2.4 day longer length of stay (p<0.001) and $6676 additional hospitalization cost (p<0.001).

Table 2.

Adjusted outcomes relative to non-frail patients

aOR 95% CI P value
Mortality 4.1 2.7 to 6.1 <0.001
Non-home discharge 5.2 4.4 to 6.1 <0.001
Complications
 Neurologic 3.3 1.8 to 6.1 <0.001
 Respiratory 2.6 2.2 to 3.2 <0.001
 Infection 3.2 2.5 to 3.9 <0.001
 Renal 2.0 1.6 to 2.5 <0.001
Adjusted coefficient 95% CI P value
Incremental cost ($) 7971 6541 to 9400 <0.001
Index additional LOS (days) 2.8 2.4 to 3.2 <0.001
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LOS, length of stay.

DISCUSSION

Summary of Main Results

The present study demonstrates that frailty, as defined by the Johns Hopkins Adjusted Clinical Groups frailty-defining diagnosis indicator, is an independent risk factor for worse outcomes including mortality, increased resource use, and non-home discharge in women undergoing surgery for endometrial cancer. Specifically, frailty predicted a four-fold increased odds of mortality, as well as increased rates of various complications and thousands of dollars in additional hospitalization costs.

Results in the Context of Published Literature

A study of over 144 000 endometrial cancer cases in the Nationwide Readmission Database from 2010 to 2014 found that frailty increased 30-day readmission and mortality in both the index admission and 30-day readmission.11 Our study incorporates a longer cohort of patients from 2005 to 2017 and notably identifies that, while frailty was associated with mortality, overall mortality did decrease in the frail cohort of endometrial cancer patients over the length of the study period. This decrease in mortality is likely multifactorial, including other improvements in medical care that may impact overall survival in this population. Driver et al found frailty was a better predictor of disease-free survival and overall survival than age, grade, stage, or comorbidities alone in women over 60 years of age undergoing curative treatment for endometrial cancer.22 As the population in the USA is aging, and consequently frailty is becoming more prevalent, these findings emphasize the need to mitigate the impact of frailty.

Prehabilitation with targeted interventions for frail patients or extended postoperative rehabilitation may improve outcomes further in this at-risk population of endometrial cancer patients. However, this remains to be proven. Carli et al found that a prospective attempt at multimodal preoperative interventions involving exercise, nutritional, and psychological interventions did not show a significant reduction in postoperative complications in a group of frail patients undergoing colorectal cancer resection compared with those who underwent postoperative rehabilitation.23 The lack of benefit may have been partly due to a limited prehabilitiation of 4 weeks as well as an optimized enhanced recovery after surgery protocol for all patients in the study. More recently, van der Hulst et al found that physical prehabilitation did reduce postoperative complications in an older frail population of colorectal cancer patients.24 This growing body of literature supports the need for a prospective study of targeted interventions in frail endometrial cancer patients.

The current findings also emphasize that frailty and aging, while related, are mutually exclusive risk factors for endometrial cancer morbidity and mortality. While frail patients overall were older, at the beginning of the study period in 2005 the average age of non-frail and frail patients differed by 11 years. At the end of the study period, non-frail and frail patients differed in age by only 3 years. This may reflect the impact of obesity and metabolic syndrome on frailty that cannot be captured by age alone. An analysis of the US National Health and Nutrition Examination Survey (NHANES) by Kane et al found that while frailty predicted mortality in all adults regardless of age, metabolic syndrome was correlated with frailty in younger patients alone.25 Thus, the impact of metabolic syndrome on endometrial cancer may account for the discordance between frailty and age in disease outcomes, particularly in younger populations.

Our findings demonstrate that frail patients were more likely to be of Black race and of the lowest income quartile, the same risk factors known to increase cancer care inequalities across various sites, including endometrial cancer.26–32 Lee et al showed that the overall prevalence of frailty was 14.3%, higher for women than men, increased with age, and was more common among those with low levels of education and income.33 Healthcare inequalities reach across systems even with universal healthcare coverage, suggesting that these risk factors are not only caused by a lack of access to care.26 29 For example, one study in Ontario, Canada concluded that social determinants of health such as material deprivation, residential instability, and ethnic concentration were associated with advanced disease at the time of diagnosis.34 While late stage at diagnosis may play a role in disease morbidity and mortality, another proposed mechanism suggested that chronic stress due to disadvantaged social environments and the resulting increased hypothalamic–pituitary–adrenal dysfunction negatively impacts health outcomes.35 Improvement in the underlying social determinants of health is vital to ultimately address inequities in care and address disparities that exist among patients of diverse backgrounds.

Strengths and Weaknesses

While similar findings have been replicated in several studies across multiple specialties, we present the largest cohort of endometrial cancer patients undergoing surgery utilizing a nationwide dataset which reliably estimates all inpatient hospital encounters in the USA. This dataset covers a larger cohort of patients, from 2005 to 2017, than the existing literature. Limitations of this study are inherent to its retrospective nature. Given the nature of this study, patients were assigned a frailty status retrospectively. This may impact outcomes and treatment variables in this patient population. While we made an attempt to control for this via our logistical regression analyses, this is a limitation of the study. Prospective evaluation of frailty as a pre-existing stratification group will allow for more accurate assessment with regard to cancer outcomes. In addition, consensus on the use of specific frailty scores would allow for more generalizable conclusions in our patient population.

All diagnoses and outcomes were obtained from a coding database and were therefore reliant on the accuracy of documentation and coding. There is also a lack of key clinical information including stage, body mass index, and histopathology data which may impact study results. For example, despite adjusting for extended procedures such as bowel resection, the current study found that frail patients were more likely to undergo open procedures. This may indicate that frail patients were more likely to have higher stage disease in which a minimally invasive approach was not technically feasible. As such, future studies should determine whether frailty is an independent risk factor for surgical outcomes after adjusting for stage of disease and surgical approach (minimally invasive vs exploratory laparotomy). In addition, with more endometrial cancer patients undergoing same day surgery or overnight stay in recent years, all patients undergoing surgery for endometrial cancer may not have been captured towards the end of the study period.

Implications for Practice and Future Research

Our findings highlight the impact of frailty on surgical outcomes and mortality for patients with endometrial cancer and emphasize the importance of frailty risk assessment in supplementing the perioperative evaluation of patients. Research into the biological changes associated with frailty may provide novel treatment targets to improve outcomes for this patient population. Targeted interventions such as prehabilitation and postoperative nutritional support for at-risk patients may also provide means of mitigating frailty.36 Impact on social determinants of health is necessary to mitigate disparities given their direct association with frailty. Prospective study of frail patients with endometrial cancer may prove critical for developing perioperative guidelines that reduce frailty’s effect.

Supplementary Material

Supplementary

HIGHLIGHTS.

⇒ Frailty predicted increased mortality for patients beyond their fifth decade of life.

⇒ The rate of mortality decreased for frail patients throughout the study period.

⇒ Frailty was associated with increased length of stay and hospitalization costs.

WHAT IS ALREADY KNOWN ON THIS TOPIC

⇒Frailty has been shown to influence surgical out-comes in gynecologic cancer, including increased risk of 30-day postoperative readmission for patients with endometrial cancer.

WHAT THIS STUDY ADDS

⇒While frailty is associated with increased mortality, risk of postoperative complications, and hospitalization cost, the mortality rate for these patients has improved over time.

HOW THIS STUDY MIGHT AFFECT RESEARCH, PRACTICE AND/OR POLICY

⇒This study emphasizes the need for frailty mitigation factors in order to continue to improve surgical out-comes for this patient population over time.

Funding

The authors have not declared a specific grant for this research from any funding agency in the public, commercial or not-for-profit sectors.

Footnotes

Twitter Joshua G Cohen @JCohenMD

Competing interests None declared.

Patient consent for publication Not applicable.

Ethics approval Not applicable.

Provenance and peer review Not commissioned; externally peer reviewed.

Supplemental material This content has been supplied by the author(s). It has not been vetted by BMJ Publishing Group Limited (BMJ) and may not have been peer-reviewed. Any opinions or recommendations discussed are solely those of the author(s) and are not endorsed by BMJ. BMJ disclaims all liability and responsibility arising from any reliance placed on the content. Where the content includes any translated material, BMJ does not warrant the accuracy and reliability of the translations (including but not limited to local regulations, clinical guidelines, terminology, drug names and drug dosages), and is not responsible for any error and/or omissions arising from translation and adaptation or otherwise.

Data availability statement

Data are available in a public, open access repository. Data obtained from the 2005–2017 National Inpatient Sample (NIS) database developed for the Healthcare Cost and Utilization Project (HCUP) and sponsored by the Agency for Healthcare Research and Quality (AHRQ). Data available at https://www.hcup-us.ahrq.gov/

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Associated Data

This section collects any data citations, data availability statements, or supplementary materials included in this article.

Supplementary Materials

Supplementary
NIHMS1820863-supplement-Supplementary.pdf (49.9KB, pdf)

Data Availability Statement

Data are available in a public, open access repository. Data obtained from the 2005–2017 National Inpatient Sample (NIS) database developed for the Healthcare Cost and Utilization Project (HCUP) and sponsored by the Agency for Healthcare Research and Quality (AHRQ). Data available at https://www.hcup-us.ahrq.gov/

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