Longitudinal Analysis of Mental Disorder Burden Among Elderly Patients With Gastrointestinal Malignancies

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  • 1 Department of Radiation Oncology, University of California, Irvine, Orange;
  • 2 Department of Radiation Oncology, Stanford University, Stanford; and
  • 3 Division of Palliative Medicine, Department of Medicine, University of California, San Francisco, San Francisco, California.

Background: Patients with cancer are at high risk for having mental disorders, resulting in widespread psychosocial screening efforts. However, there is a need for population-based and longitudinal studies of mental disorders among patients who have gastrointestinal cancer and particular among elderly patients. Patients and Methods: We used the SEER-Medicare database to identify patients aged ≥65 years with colorectal, pancreatic, gastric, hepatic/biliary, esophageal, or anal cancer. Earlier (12 months before or up to 6 months after cancer diagnosis) and subsequent mental disorder diagnoses were identified. Results: Of 112,283 patients, prevalence of an earlier mental disorder was 21%, 23%, 20%, 20%, 19%, and 26% for colorectal, pancreatic, gastric, hepatic/biliary, esophageal, and anal cancer, respectively. An increased odds of an earlier mental disorder was associated with pancreatic cancer (odds ratio [OR], 1.17; 95% CI, 1.11–1.23), esophageal cancer (OR, 1.10; 95% CI, 1.02–1.18), and anal cancer (OR, 1.17; 95% CI, 1.05–1.30) compared with colorectal cancer and with having regional versus local disease (OR, 1.09; 95% CI, 1.06–1.13). The cumulative incidence of a subsequent mental disorder at 5 years was 19%, 16%, 14%, 13%, 12%, and 10% for patients with anal, colorectal, esophageal, gastric, hepatic/biliary, and pancreatic cancer, respectively. There was an association with having regional disease (hazard ratio [HR], 1.08; 95% CI, 1.04–1.12) or distant disease (HR, 1.36; 95% CI, 1.28–1.45) compared with local disease and the development of a mental disorder. Although the development of a subsequent mental disorder was more common among patients with advanced cancers, there continued to be a significant number of patients with earlier-stage disease at risk. Conclusions: This study suggests a larger role for incorporating psychiatric symptom screening and management throughout oncologic care.

Background

Patients with cancer who have a mental disorder at cancer diagnosis or who develop new mental disorders later in the oncologic course represent a particularly vulnerable subgroup at risk for worse cancer outcomes.13 A comorbid mental disorder is a known risk factor for inferior oncologic outcomes.4 Thus, efforts to integrate symptom management, palliative care, and psycho-oncologic care have been introduced into consensus guidelines.5,6 Similarly, the American College of Surgeons Commission on Cancer standards require accredited cancer centers to provide psychosocial distress screening to identify patients at high risk for a mental disorder and to monitor the referral for psychosocial care.7 These efforts are more often aimed at patients earlier in their cancer diagnosis and treatment. However, it has been shown that there is a sharp increase in mental disorder diagnoses not only leading up to a cancer diagnosis but also in the following months and years of the oncologic course.8 For patients with a gastrointestinal cancer, population-based estimates and longitudinal studies of mental disorders remain lacking.9

In addition, despite the fact that most patients with cancer are aged ≥65 years, there remains a need for behavioral and psychological studies in this population.10 Unfortunately, elderly patients have many mental disorder risk factors, including having less-aggressive oncologic management, baseline cognitive deficits, poor functional status, and a greater number of medical comorbidities.10 Thus, we set out to perform a longitudinal study of mental disorders among elderly patients with gastrointestinal cancers.

Patients and Methods

Data Source

We used the SEER-Medicare linked database and identified patients whose first cancer was a primary colorectal, pancreatic, gastric, hepatic/biliary, esophageal, or anal cancer during 2004 through 2013. SEER-Medicare is a large dataset maintained by the NCI that details inpatient and outpatient medical claims from Medicare beneficiaries who are included in the SEER registry.11,12

Patient Selection

The cohort included patients aged ≥65 years with Medicare Parts A and B enrollment without HMO coverage starting 12 months before cancer diagnosis to ensure completeness of claims data. Only patients with complete staging information were included. Censoring occurred at the end of December 2014 or when Medicare coverage was lost.

Mental Disorder Identification

Medicare billing claims were used to identify mental disorders and professional management for a mental disorder (see supplemental eAppendix 1, available with this article at JNCCN.org). Mental disorders included depressive, anxiety, psychotic, and bipolar disorders. An early mental disorder was limited to 12 months before and up to 6 months after cancer diagnosis, and a subsequent mental disorder was at any point after 6 months from cancer diagnosis. Given the limitations of the data, the exact timeline between mental disorder development and cancer diagnosis was impossible to entirely tease apart. Earlier mental disorders were intended to include diagnoses made throughout the diagnostic workup, the information-sharing period regarding diagnosis and prognosis, and treatment initiation. This is the period during which mental disorders may be diagnosed as a result of psychosocial distress screening occurring as part of the comprehensive oncologic care model.7 Subsequent mental disorders included those overlapping with cancer progression and additional treatments.

Demographic and Clinical Characteristics

Using data from the SEER registry, we determined age, sex, race, Hispanic ethnicity, marital status, area income, cancer stage, and disease subsite.13 Dual Medicaid insurance and Charlson comorbidity score modified for patients with cancer were determined through claims data.14,15

Statistical Analysis

Clinical and demographic characteristics were compared between groups using chi-square tests. A multivariate logistic regression model was used to determine associations with early mental disorders. We calculated the cumulative incidence of subsequent mental disorders among those without an early mental disorder. Multivariate subdistribution hazard models (Fine-Gray regressions) were used to determine risk factors for the development of a subsequent mental disorder. We also performed sensitivity testing limited to persons who had received an influenza vaccination (supplemental eAppendix 1). Influenza vaccination has previously been used to determine use of routine preventive services, because it is recommended for all adults.16,17

Statistical significance was set at 0.05, and all tests were 2-tailed. Data analysis and statistical testing was performed using R version 3.5 (R Foundation for Statistical Computing).

Results

We identified 112,283 patients who met inclusion criteria (Figure 1), including 76,421 with colorectal, 10,378 with pancreatic, 8,996 with gastric, 9,404 with hepatic/biliary, 5,159 with esophageal, and 1,925 with anal cancer. A total of 23,726 patients (21%) had an early mental disorder, comprising 16,138 (21%) of the colorectal cohort, 2,401 (23%) of the pancreatic cohort, 1,792 (20%) of the gastric cohort, 1,891 (20%) of the hepatic/biliary cohort, 1,001 (19%) of the esophageal cohort, and 503 (26%) of the anal cancer cohort (Table 1). A comparison of patients included and excluded from the study is presented in supplemental eAppendix 2. The included cohort had more patients who were married (52% vs 43%) and fewer with dual Medicaid insurance (23% vs 29%).

Figure 1.
Figure 1.

Cohort selection from the SEER-Medicare database.

Citation: Journal of the National Comprehensive Cancer Network J Natl Compr Canc Netw 2021; 10.6004/jnccn.2020.7620

Table 1.

Patient Characteristics According to Early Mental Disorder Status

Table 1.

Early mental disorders were more likely in patients who were older (24% of those aged ≥85 years), female (26%), White (22%), unmarried, and from a lower income area, and those with dual Medicaid insurance (29%), more comorbidities (Charlson comorbidity index score ≥1), and regional disease (22%), and were less likely in those with distant disease at diagnosis (19%).

Multivariate logistic regression analysis showed that increased odds of an early mental disorder were associated with pancreatic cancer (odds ratio [OR], 1.17; 95% CI, 1.11–1.23), esophageal cancer (OR, 1.10; 95% CI, 1.02–1.18), and anal cancer (OR, 1.17; 95% CI, 1.05–1.30) compared with colorectal cancer (Table 2). We also found an association between an early mental disorder and younger age (OR, 0.94; 95% CI, 0.90–0.97 for age 75–84 vs 65–74 years), female sex (OR, 1.81; 95% CI, 1.76–1.87), White race and non-Hispanic ethnicity, being unmarried, being from a lower income area, having dual Medicaid insurance (OR, 1.73; 95% CI, 1.67–1.80), having more comorbidities, and having regional disease.

Table 2.

Multivariate Logistic Regression Analysis of Characteristics Associated With an Early Mental Disorder

Table 2.

The cumulative incidence of developing a subsequent mental disorder at 5 years was 19%, 16%, 14%, 13%, 12%, and 10% for patients with anal, colorectal, esophageal, gastric, hepatic/biliary, and pancreatic cancer, respectively (Figure 2). On multivariate analysis, there was an association between a subsequent mental disorder and esophageal cancer (hazard ratio [HR], 1.61; 95% CI, 1.48–1.75), gastric cancer (HR, 1.15; 95% CI, 1.08–1.23), hepatic/biliary (HR, 1.29; 95% CI, 1.20–1.38), and pancreatic cancer (HR, 1.39; 95% CI, 1.29–1.50) compared with colon cancer (Table 3). In addition, there was an association with having regional or distant disease at the time of diagnosis.

Figure 2.
Figure 2.

Development of a subsequent mental disorder following a gastrointestinal cancer diagnosis among patients without an early mental disorder. The reference time point is the cancer diagnosis, with a subsequent mental disorder defined as occurring at least 6 months after the cancer diagnosis.

Citation: Journal of the National Comprehensive Cancer Network J Natl Compr Canc Netw 2021; 10.6004/jnccn.2020.7620

Table 3.

Characteristics Associated With Development of a Subsequent Mental Disordera

Table 3.

We investigated the number of patients with an early or subsequent mental disorder receiving outpatient treatment from a mental health professional. There were 6,497 patients (27%) who received treatment from a mental health professional (Table 4). No significant differences by disease subtype or stage were seen, but older patients, men, those with dual Medicaid insurance, and those with more comorbidities were more likely to have received treatment from a mental health professional.

Table 4.

Patient Characteristics According to Receipt of Psychiatric/Psychological Treatmenta

Table 4.

We performed secondary analyses limited to patients who had routine interaction with the healthcare system, defined as receiving the influenza vaccination (supplemental eAppendix 3). Cancer subsite and demographic findings were consistent with the primary analysis. The incidence of developing a subsequent mental disorder at 5 years was 11% to 23% depending on cancer subsite. Another secondary analysis was performed classifying an early mental disorder as a condition identified in any billing claim 12 months before the date of cancer diagnosis (supplemental eAppendix 4). We found that fewer patients met criteria for an early mental disorder diagnosis (11%), whereas the 5-year incidence of a subsequent mental disorder was higher (21%–30% depending on cancer subsite).

Lastly, we performed additional analyses of mental disorder subcategories (supplemental eAppendix 5). The most common early and subsequent diagnoses were depressive disorders, followed by anxiety, psychotic, and bipolar disorders. Having any subsequent mental disorder was also more likely for those with a different, earlier mental disorder. The pattern of clinical and demographic associations in the primary analysis were generally consistent across this secondary analysis (supplemental eAppendix 5).

Discussion

We conducted a population-based study to determine the burden of mental disorders among elderly patients with gastrointestinal cancers in the United States. Depending on the cancer subsite, 19% to 26% of patients had a diagnosed early mental disorder, and an additional 10% to 19% of patients developed a subsequent mental disorder. These diagnoses were more likely among patients with more advanced disease, but rates were substantial among all subgroups.

Our estimates for the rates of early and subsequent mental disorders are similar to prior liturature.8,1822 However, one limitation of registry studies is the reliance on accurate diagnostic coding by health practitioners, which can result in an underrepresentation of the true prevalence of comorbidities because there is no guarantee that patients interact with the healthcare system and receive accurate diagnostic codes.23,24 We used strategies to address this known issue, including defining an early mental disorder as one diagnosed 12 months before or up to 6 months after the cancer diagnosis to account for patients who have more limited interactions with the healthcare system.8 Second, we performed an analysis limited to patients receiving routine influenza vaccinations. Because influenza vaccination is recommended universally for adults, all patients should be interacting with the healthcare system on at least an annual basis, and hence this surrogate has been used previously.16,17 Third, we investigated the number of patients receiving care from a mental health professional, which more accurately identifies patients with more severe psychiatric burden.25

The explanation for the high rates of early mental disorders among patients with gastrointestinal cancer in the current study is likely multifactorial. Several studies have shown that rates of mental disorders begin to increase before the cancer diagnosis, with the thought that the initial symptoms and diagnostic workup induce a stress response that can trigger a mood disorder.8,2628 For other patients with a longstanding mental disorder, there has been great heterogeneity among studies to determine whether there is an increased risk for cancer or if other modifying factors and behaviors are responsible.29 Patients with mental disorders are more likely to have certain cancer risk factors, such as metabolic syndrome, a smoking history, and worse healthcare access.3033 Detangling the causality in the precancer diagnosis period remains challenging.

There are also many explanations for the high rates of subsequent mental disorder diagnoses found in the current study. Cancer diagnosis, treatment, and progression are all major stressors. These stressors can result in an inflammatory response and immune system activation, which is well-known to be associated with mental disorders.34 Elevations in inflammatory markers such as C-reactive protein and cytokines, including IL-6, IL-8, and tumor necrosis factor-α, have been associated with many mental disorders.3537 For some patients, the cancer-related inflammatory response can cause certain mental disorders, but mental disorders themselves can also increase systemic inflammation.38

With regard to determining the patients at highest risk for mental disorders, a multitude of clinical factors play a role. We found that having more advanced disease was associated with an early mental disorder. One reason is that among patients with mental disorders, routine medical care and screening are much lower than the general population.2,3 We also found that patients with more advanced disease were more likely to develop subsequent mental disorders. The explanation may be that a poorer prognosis and disease recurrence trigger significantly more psychological stress.39,40

On one hand, we found that the highest risk factor for a subsequent mental disorder was having esophageal or pancreatic cancer. On the other hand, the associations with having an early mental disorder were much less pronounced, albeit highest for patients with pancreatic or anal cancer. To make a generalization, patients with esophageal or pancreatic cancer tend to have a worse overall prognosis and more devastating treatment effects, resulting in worse health-related quality of life compared with those with colorectal cancer.4143 This is consistent with our finding of advanced disease as a risk factor for developing a mental disorder. As for the risk of having an early mental disorder, it is thought that those with pancreatic cancer may develop symptoms of anxiety or depression prodromal to the diagnosis.44 In some cases the psychological symptoms, including appetite loss, weight loss, or fatigue, may be early cancer symptoms, but other theories have suggested immunologic, paraneoplastic, biochemical, and hormonal explanations connecting the cancer to depression.44 For patients with anal cancer, the workup and diagnostic procedures put patients at particular risk for significant psychological stress.45,46

With regard to other clinical and demographic characteristics, we found that mental disorders were more common among patients with a greater number of medical comorbidities. Similar to the relationship between poorer oncologic outcome and subsequent mental disorder development, the association between mental disorders, physical comorbidities, and negative health behaviors may be responsible.3033

Another finding was that lower income, as measured by dual Medicaid insurance and living in a lower income area, was a risk factor for having a mental disorder. Potential explanations include that lower socioeconomic position is associated with access to fewer healthcare resources and with unhealthy behaviors, such as smoking and obesity, which are associated with developing a mental disorder.2933,47

Our study found that women were at higher risk for having a mental disorder, which is consistent with prior reports.48 One thought is that rather than having biologic or hormonal underpinnings, the explanation has more to do with social disadvantages, such as intimate-partner violence putting women at risk for mental disorders, women being more likely to have mental disorders at a young age, women having a different set of cultural norms with associated role limitations and economic discrimination, and women being more likely to report psychological symptoms and receive a mental disorder diagnosis from a practitioner.49

In addition, our study found that White and non-Hispanic patients were more likely to have an early or subsequent mental disorder, which is a well-recognized finding.50,51 However, we caution against overinterpretation of these results, because disparities may exist despite our findings. For example, one well-known exception is that Black Americans tend to have higher rates of schizophrenia.52 In addition, despite lower rates overall, it is thought that non-White Americans have higher psychological symptom burden, have less access to mental care, and are less likely to receive a mental disorder diagnosis because of practitioner bias and discrimination.53

Our study found that patients aged >75 years were less likely to have an early mental disorder, but more likely to go on to develop a subsequent mental disorder. In general, most literature supports the finding that older age is protective against having a mental disorder, although debate exists.54 Older patients tend to have more comorbidities and are less likely to receive aggressive cancer treatment.10 However, whether our finding that older age was associated with a subsequent mental disorder among patients with gastrointestinal cancer is related to the interplay between cancer prognosis, treatment, and age needs to be further explored.

Interestingly, the analysis of patients receiving management from a mental healthcare professional showed a somewhat different pattern of demographic risk factors. This finding may have been partly because patients with more severe mental disorders received professional psychiatric/psychological care, given that we found it to be associated with many demographic characteristics that were also associated with having an early or subsequent mental disorder (single marital status, dual Medicaid insurance, more medical comorbidities). However, there are many confounders; for example, the association with living in an affluent area or being older and receiving professional mental healthcare may be a marker for access. Thus, the findings are likely multifactorial and need to be better elucidated in future studies.

Limitations of this study include that it uses administrative billing claims to define the endpoint of mental disorder. Medicare claims were created and used for physician and institutional payment rather than research purposes. Ideally, diagnoses would be in accordance with the Diagnostic and Statistical Manual of Mental Disorders (Fifth Edition; DSM-5).55 However, diagnostic codes in billing claims rely on practitioner familiarity with the diagnosis of these disorders. As we have shown in our study, most patients with cancer who have a mental disorder are not receiving care from a mental health professional, and therefore the mental disorder diagnosis often falls to a general practitioner or oncologist who is likely less familiar with the specific DSM-5 criteria for a diagnosis of depressive, anxiety, psychotic, or bipolar disorder. As discussed previously, reliance on diagnostic and procedure codes can result in an underrepresentation of mental disorders. Despite our use of contemporary methods for analyzing healthcare claims, there will continue to be discrepancies with determining the number of mental disorders.56

Furthermore, there is some amount of uncertainty regarding the timing of mental disorder development and cancer diagnosis. For some patients, the cancer, its psychological burden, and resultant treatment toxicities may contribute to a new mental disorder, whereas for other patients there is an association between longstanding mental disorder and having risk factors for the development and asymptomatic progression of cancer. In the current study we used a generous window to define an early mental disorder (12 months before and up to 6 months after cancer diagnosis), although conclusions were similar when a shorter window was used (12 months before or up to the date of cancer diagnosis). In addition, we were not able to control for cancer treatments, laboratory or imaging tests, clinical performance status, or behavioral practices such as smoking or substance use, which can result in residual confounding.

Similar to other retrospective studies, there can be selection bias, and prospective cohort studies would be needed to confirm the results of this study. Excluded patients were more likely to be unmarried and have dual Medicaid insurance, and hence may be more likely to have mental disorders. In addition, the patients in our cohort were from an elderly Medicare population, which may not accurately represent younger patients or those with different or inadequate insurance. Similarly, racial minorities were underrepresented, a common issue among similar studies that makes generalization to those populations challenging.9

Conclusions

This population-based study of patients with gastrointestinal malignancies described the current burden of mental disorders in the Medicare population. Although we found that comorbid mental disorders were more common among patients with more advanced cancers, there continues to be a significant number of patients with early-stage disease who are at risk.

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Submitted November 18, 2019; accepted for publication July 14, 2020.

Author contributions: Study concept and design: Harris, Chang, Pollom. Data acquisition: Harris, Chang, Pollom. Data analysis and interpretation: All authors. Statistical analysis: Harris. Manuscript preparation: All authors. Critical revision of the manuscript for important intellectual content: All authors. Study supervision: Harris, Chang, Pollom.

Disclosures: The authors have disclosed that they have not received any financial consideration from any person or organization to support the preparation, analysis, results, or discussion of this article.

Correspondence: Jeremy P. Harris, MD, MPhil, Department of Radiation Oncology, University of California, Chao Family Comprehensive Cancer Center, 101 The City Drive, Building 23, Orange, CA 92868. Email: jeremy.harris@uci.edu

Supplementary Materials

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    Cohort selection from the SEER-Medicare database.

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    Development of a subsequent mental disorder following a gastrointestinal cancer diagnosis among patients without an early mental disorder. The reference time point is the cancer diagnosis, with a subsequent mental disorder defined as occurring at least 6 months after the cancer diagnosis.

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