Abstract
Background:
A majority of older adults with cancer develop malnutrition; however, its implications among this vulnerable population is poorly understood. We aimed to quantify the prevalence of nutrition related-symptoms and malnutrition among older adults with gastrointestinal (GI) malignancies and its association with geriatric assessment (GA) impairment, health-related quality of life (HRQOL), and healthcare utilization.
Methods:
Cross-sectional study of older adults (≥60 years) who were referred to the GI Oncology clinic at the University of Alabama at Birmingham. Participants underwent the Cancer & Aging Resilience Evaluation (CARE) survey that includes the abbreviated Patient-Generated Subjective Global Assessment (abPG-SGA) of nutrition. Nutrition scores were dichotomized into normal (0–5) and malnourished (≥6), and multivariate analyses, adjusting for demographics, cancer type, and cancer stage were used to examine associations with GA impairment, HRQOL and healthcare utilization.
Results:
336 participants were included, with mean age of 70 ± 7.2y, 56.8% male, with colorectal (33.6%) and pancreatic cancer (24.4%) being the most common diagnoses. Overall, 52.1% of participant were identified as malnourished. Malnutrition was associated with a higher prevalence of several GA impairments including ≥1 falls (adjusted odds ratio [aOR] = 2.1), instrumental Activities of Daily Living (iADL) impairment (aOR = 4.1), and frailty (aOR 8.2). Malnutrition was also associated with impaired HRQOL domains; both physical (aOR = 8.7) and mental (aOR = 5.0), and prior hospitalizations (aOR = 2.2).
Conclusions:
We found a high prevalence of malnutrition among older adults with GI malignancies that was associated with increased GA impairments, reduced HRQOL, and increased healthcare utilization.
Keywords: malnutrition, geriatric assessment, cancer, aging, geriatric oncology
Precis:
Over half (52.1%) of older adults with gastrointestinal malignancies were malnourished with poor appetite and early satiety the most common nutrition related symptoms.
Malnutrition was associated with a higher prevalence of several GA impairments including ≥1 falls, instrumental Activities of Daily Living impairment, and frailty, as well as reduced health-related quality life and prior hospitalizations.
INTRODUCTION
Cancer is predominantly a disease of aging. The vast majority of cancer diagnoses and cancer deaths occurs in adults over the age of 65, and given the changing demographics, it is estimated that nearly 70% of all new cancer diagnoses in 2030 will be in older adults.1 The health status of older adults with cancer is highly variable with wide variations in individuals of the same chronological age.2 The use of a geriatric assessment (GA) has been recommended to evaluate the health status of older adults to identify health impairments and better assess the risk/benefit ratio of treatment decisions in order to develop individualized treatment plans.3–5
All adults with cancer are at risk of malnutrition due to cancer and treatment related factors, but older adults are at particularly increased risk. Nearly 66% of older adults with cancer are malnourished, and the cancer diagnosis increases the risk of malnutrition 14-fold higher.6,7 Furthermore, the risk of malnutrition is notably even higher for older patients with gastrointestinal (GI) malignancies.8 Malnutrition can undermine the older adult’s health status, ultimately resulting in sarcopenia and frailty.7,9 The presence of malnutrition or weight loss has been associated with increased chemotherapy toxicities and reduced survival in older adults.10–13
In a recent conference focused on the future directions in geriatric oncology research sponsored by the National Cancer Institute and the National Institute on Aging, nutritional research was highlighted as a major area of concern, as the majority of nutrition related research has been among younger populations and there is limited evidence to guide the management of nutrition issues in older adults with cancer.14 More specifically, the prevalence of malnutrition and specific nutrition related symptoms among older adults with GI malignancies and its relationship to health-related quality of life (HRQoL), GA-identified impairments, and healthcare utilization remains poorly understood. Regular screening for the presence of malnutrition is recommended for all adults with cancer as many potential nutritional interventions exist, yet it remains under recognized.8,15
Using the University of Alabama at Birmingham (UAB) Cancer and Aging Resilience Evaluation (CARE) Registry,16 we aimed to 1) describe the prevalence of and factors associated with malnutrition in older adults with GI malignancies, 2) describe nutrition-related symptoms in older adults with GI malignancies and 3) examine the relationship of malnutrition with HRQoL, GA impairments, and healthcare utilization.
METHODS
Study Population
The CARE registry is an ongoing, prospective registry of all older adults with cancer. The development and integration of the CARE registry into routine clinical practice at UAB is described elsewhere, but in brief all older adults with cancer (≥age 60 years) complete a patient-reported GA questionnaire at the time of check-in that is later collected by nursing staff during triage and given to the clinical team.16 Patients are approached for consent to have their information stored in the CARE Registry. For the purpose of this study, we included patients enrolled from September 2017 through January 2020, limited our cohort to only those patients that had a GI malignancy, and had performed a GA prior to any potentially planned chemotherapy. The University of Alabama at Birmingham Institutional Review Board approved this study.
Nutrition Assessment
The CARE survey utilizes an abridged version of the Patient-Generated Subjective Global Assessment (abPG-SGA) as a nutritional screening tool.17,18 The PG-SGA tool is a recommended and accepted tool for nutrition assessment in oncology, but given the time required and necessary training to complete the PG-SGA, implementation in routine care has been limited.19,20 Therefore, the abPG-SGA was developed that forgoes the physical exam, disease/condition, and metabolic considerations, and relies on four patient report domains related to malnutrition (summed scores range from 0–35, with higher scores indicating higher probability of malnutrition).17 The four domains include an assessment of height and weight (day of exam, 1 and 6 months prior to study participation), food intake, nutrition-related symptoms, and activities and function. The abPG-SGA has been validated in the outpatient oncology clinic and a cut-off score of ≥6 has been identified as the optimal cut-off to identify malnutrition.17
Geriatric Assessment
The CARE survey is patient-reported modified from the Cancer and Aging Research Group (CARG) GA.21–23 The CARE survey includes a systematic assessment of falls, physical function, functional status, nutrition, social support, psychological health, patient-reported cognitive complaints, social activities, patient-reported eastern cooperative oncology group (ECOG) performance status, polypharmacy (dicotomoized as <9 or ≥9 medications), and comorbid conditions (dichtomized as <3 or ≥3).2,16,24 Domain-specific cut-offs were utilized in accordance with prior literature.2,16,23 In addition, the CARE survey includes a single-item measure of financial distress (as developed in the Patient Satisfaction Questionnaire) that has previously been demonstrated to be associated with adverse financial outcomes and medical non-compliance.25 Frailty was calculated using 44-items in the GA to develop a frailty index based on the principles of deficit accumulation; standard threshold scoring was applied (frail >0.35).26–28
Other Measures
The CARE survey includes the National Institutes of Health’s Patient-Reported Outcomes Measurement Information System® (PROMIS®) Global Health short-form to assess HRQoL. The PROMIS Global Health 10-item scale includes separate scoring for physical and mental health subscales and has been previously tested in large samples of adults in the US.29,30 The item responses were converted to t-scores with a standardized mean score of 50 and a standard deviation of 10. The minimal clinically-relevant difference for PROMIS ranges from 2 to 6 points, and a score of 40 or less (1 standard deviation) is considered impaired for the physical and mental subscales.31 Lastly, the CARE survey includes two questions regarding prior healthcare utilization and whether participants have been seen in the emergency room (ER) or hospitalized in the past year. Race, ethnicity, education level, employment, and marital status were obtained by self-report and as part of the CARE survey, while cancer stage, cancer type, date of diagnosis, and treatment phase (i.e. pre-chemotherapy) were chart abstracted from within the electronic medical record.
Statistical Analyses
Descriptive statistics were used to characterize the population at baseline. We defined malnutrition as a score of ≥6 on the abPG-SGA questionnaire. We estimated the prevalence of specific nutrition-related symptoms. Bivariate comparisons were made using Fisher’s Exact and Wilcoxon Rank Sum tests to study the association of malnutrition with baseline characteristics as well as HRQoL, GA impairments, and healthcare utilization. We used multivariable logistic regression modeling controlling for age at study, sex, education, marital status, employment, cancer type, and cancer stage to further explore the associations between malnutrition and other outcome variables. All statistical tests were two-sided and the level of significance was chosen as 0.05. All analyses were conducted using SAS statistical software version 9.4 (SAS Institute Inc., Cary, NC).
RESULTS
During the study time window, 650 new older patients with GI malignancies were seen in the clinic, with 571 (87.7%) having consented and completed the CARE survey. Of these, a total of 336 study participants (51.7% of overall) met our inclusion criteria (pre-chemotherapy treatment) and are a focus of our study. Median age at study was 70.1 years (range, 60–96). Majority of participants were male (56.8%), White (75.6%), Non-Hispanic (98%), retired (61.6%), and married (65.1%) (Table 1). Most common cancer types included colorectal (33.6%), pancreatic (24.4%), and hepatobiliary (17.0%) cancers with the majority of participants having advanced stage cancers (71.7% with stage III/IV). The median time interval between cancer diagnosis and study participation was 1 month (interquartile range 1–2 months).
Table 1.
Demographic and Cancer Characteristics, Overall and by Malnutrition Status
| All | Malnourished | p-value* | ||
|---|---|---|---|---|
| No |
Yes |
|||
| Total Patients | N= 336 | N= 161 | N= 175 | |
| Age, mean (SD) | 70.1 (7.2) | 70.1 (7.3) | 70.1 (7.1) | 0.9704 |
| 60–64 | 86 (25.6) | 45 (28.0) | 41 (23.4) | 0.5797 |
| 65–69 | 83 (24.7) | 36 (22.4) | 47 (26.9) | |
| 70–74 | 76 (22.6) | 35 (21.7) | 41 (23.4) | |
| 75–79 | 48 (14.3) | 21 (13.0) | 27 (15.4) | |
| 80+ | 43 (12.8) | 24 (14.9) | 19 (10.9) | |
| Sex, n (%) | ||||
| Male | 191 (56.8) | 90 (55.9) | 101 (57.7) | 0.7374 |
| Race, n (%) | ||||
| White | 254 (75.6) | 122 (75.8) | 132 (75.4) | 0.9923 |
| Black | 78 (23.2) | 37 (23.0) | 41 (23.4) | |
| Other | 4 (1.2) | 2 (1.2) | 2 (1.1) | |
| Ethnicity, n (%) | ||||
| Hispanic | 7 ( 2.1) | 3 (1.9) | 4 (2.3) | 0.7866 |
| Educational Level, n (%) | ||||
| Less than high school | 59 (17.6) | 28 (17.4) | 31 (17.7) | 0.9946 |
| High school graduate | 90 (26.8) | 45 (28.0) | 45 (25.7) | |
| Some college | 62 (18.5) | 29 (18.0) | 33 (18.9) | |
| Associate/Bachelors | 91 (27.1) | 43 (26.7) | 48 (27.4) | |
| Advanced Degree | 34 (10.1) | 16 (9.9) | 18 (10.3) | |
| Employment, n (%) | ||||
| Retired | 207 (61.6) | 101 (62.7) | 106 (60.6) | 0.0016 |
| Disabled | 45 (13.4) | 20 (12.4) | 25 (14.3) | |
| Part-time (<32hr/wk) | 8 (2.4) | 7 (4.3) | 1 (0.6) | |
| Full-time (>32hr/wk) | 36 (10.7) | 23 (14.3) | 13 (7.4) | |
| Other | 40 (11.9) | 10 (6.2) | 30 (17.1) | |
| Marital Status, n (%) | ||||
| Single | 22 (6.5) | 11 (6.8) | 11 (6.3) | 0.9754 |
| Widowed/Divorced | 95 (28.3) | 45 (28.0) | 50 (28.6) | |
| Married | 219 (65.2) | 105 (65.2) | 114 (65.1) | |
| Cancer Type, n (%) | ||||
| Colorectal | 113 (33.6) | 67 (41.6) | 46 (26.3) | 0.0012 |
| Pancreatic | 82 (24.4) | 26 (16.1) | 56 (32.0) | |
| Hepatobiliary | 57 (17.0) | 32 (19.9) | 25 (14.3) | |
| Gastroesophageal | 36 (10.7) | 13 (8.1) | 23 (13.1) | |
| Other (NEC, GIST, Anal) | 48 (14.3) | 23 (14.3) | 25 (14.3) | |
| Cancer Stage, n (%) | ||||
| 0-II | 95 (28.3) | 43 (26.7) | 52 (29.7) | 0.0079 |
| III | 89 (26.5) | 55 (34.2) | 34 (19.4) | |
| IV | 152 (45.2) | 63 (39.1) | 89 (50.9) | |
based on comparison between malnourished and non-malnourished participants
The median abPG-SGA nutrition measure score was 6 (interquartile range [IQR] of 2–12); 52.1% of the study population was identified to have malnutrition with an abPG-SGA score of ≥6. There were no differences in age, sex, race, ethnicity, or education level between those with and without malnutrition (Table 1). A larger proportion of malnourished patients were disabled, while a larger proportion of those without malnutrition were employed either part- or full-time. Malnourished patients had a higher proportion of pancreatic (32.0% vs. 16.1%) and gastroesophageal (13.1% vs. 8.1%) cancers as well as stage IV (50.9% vs. 39.1%) disease (Table 1).
The prevalence of specific nutrition-related symptoms varied among GI cancer types. Overall, lack of appetite (31.5%) was the most prevalent nutrition-related symptom, followed by feeling full quickly (29.1%), nausea (22.1%), fatigue (20.9%) and pain (20.9%) (Figure 1). Nausea, vomiting, constipation, dry mouth, being bothered by certain smells, the sensation of feeling full quickly, problems swallowing, feeling fatigued and pain were all nutrition related symptoms with a statistical difference between GI cancer types. Over half (52.4%) of patients with pancreatic cancer and approximately a third (36.1) of patients with gastroesophageal cancer reported early satiety (p <.0001). Among the reported GI cancer types, symptoms of nausea, vomiting, constipation, dry mouth, no taste, feeling full quickly, fatigue and pain were also most common in patients diagnosed with pancreatic cancer. Patients with gastroesophageal cancer reported problems swallowing and early satiety more frequently than other symptoms.
Figure 1.
Prevalence of nutrition related symptoms, both overall and by cancer types.
When examining differences in GA impairments between those with and without malnutrition, study participants who were malnourished were more likely to have falls, an impaired performance status, limitations when walking one block, impairments in instrumental activities of daily living (IADL) and activities of daily living (ADL), cognitive complaints, ≥3 comorbidities, limitations in social activities, anxiety, depression, fatigue, and pain (Table 2). There were no significant differences in the proportions with ≥9 medications, financial distress, or those with either hearing or vision impairments between those with and without malnutrition. Those who were malnourished had lower physical health HRQoL sub-scores (37.6 vs. 48.9, p <0.001) and mental health HRQoL sub-scores (44.3 vs. 52.0, p <0.001) (Table 2). Lastly, significantly more participants with malnutrition reported an emergency room visit (70.5 vs 55.7%, p =0.005) or hospitalization in the last 6 months (64.3 vs. 45.9%, p <0.001).
Table 2:
Differences in geriatric assessment, health-related quality of life, and prior healthcare utilization by nutrition status
| Malnourished |
|||
|---|---|---|---|
| No | Yes | p-value | |
| Geriatric Assessment Domains | |||
| ≥1 falls, n (%) | 23 (14.7) | 41 (24.6) | 0.0271 |
| Impaired (≥2) performance status, n (%) | 15 (9.3) | 95 (54.3) | <0.001 |
| Reported limitations in walking one block, n (%) | 58 (36.5) | 120 (69.0) | <0.001 |
| Any IADL dependence, n (%) | 50 (32.1) | 115 (67.3) | <0.001 |
| Any ADL dependence, n (%) | 11 (7.0) | 46 (26.7) | <0.001 |
| Moderate/Severe Cognitive Dysfunction, n (%) | 4 (2.6) | 18 (10.4) | 0.0051 |
| ≥3 comorbidities other than cancer, n (%) | 73 (45.6) | 102 (59.0) | 0.0149 |
| ≥9 medications daily, n (%) | 37 (23.4) | 37 (21.5) | 0.6783 |
| Limitations in social activities, n (%) | 12 (7.5) | 68 (39.5) | <0.001 |
| Moderate/Severe Anxiety, n (%) | 16 (10.3) | 44 (25.9) | 0.0003 |
| Moderate/Severe Depression, n (%) | 7 (4.5) | 37 (21.5) | <0.001 |
| Vision impairment, n (%) | 33 (20.6) | 50 (29.2) | 0.0708 |
| Hearing impairment, n (%) | 37 (23.3) | 52 (30.2) | 0.1535 |
| Moderate/severe Fatigue, n (%) | 64 (40.0) | 128 (74.0) | <0.001 |
| Moderate/severe Pain, n (%) | 42 (26.6) | 106 (60.9) | <0.001 |
| Frail, n (%) | 21 (13.0) | 95 (54.3) | <0.001 |
| Health-Related Quality of Life | |||
| Physical Health Score, mean (SD) | 48.9 (9.2) | 37.6 (9.0) | <0.001 |
| Mental Health Score, mean (SD) | 52.0 (8.6) | 44.3 (8.7) | <0.001 |
| Healthcare Utilization | |||
| Emergency Room visit, n (%) | 88 (55.7) | 122 (70.5) | 0.0052 |
| Hospitalized at least one night, n (%) | 72 (45.9) | 110 (64.3) | 0.0008 |
Abbreviations: IADL, Instrumental Activities of Daily Living; ADL, Activities of Daily Living. SD, standard deviation.
In our unadjusted odds ratios of demographic and clinical variables with the presence of malnutrition, we found no differences by age, sex, or race; however, older patients with pancreatic cancer and gastroesophageal cancers were 3.1 (odds ratio [OR] 1.7–5.7) and 2.6 (1.2–5.6) times more likely to have malnutrition, respectively (Table 3). In multivariable analyses, malnutrition was independently associated with falls (adjusted OR [aOR] = 2.1, 95% CI 1.1–4.0), impaired performance status (aOR = 12.8, 95% CI 6.5–25.2), limitations in walking one block (aOR = 4.0, 95% CI 2.3–6.8), IADL impairment (aOR = 4.1, 95% CI 2.4–7.0), ADL impairment (aOR = 4.83, 95% CI 2.25–10.4), cognitive complaints (aOR = 7.2, 95% CI 1.9–27.8), limitations in social activities (aOR = 7.7, 95% CI 3.8–15.9), anxiety (aOR = 3.0, 95% CI 1.5–6.1), depression (aOR = 5.1, 95% CI 2.0–12.8), fatigue (aOR = 4.8, 95% CI 2.8–8.2), pain (aOR = 4.9, 95% CI 2.9–8.6), and frailty (aOR 8.2, 95% CI 4.4–15.3) (Table 4). Malnutrition was also associated with reduced physical (aOR = 8.7, 95% CI 4.6–16.3) and mental (aOR = 5.0, 95% CI 2.6–9.6) HRQoL, as well as increased prior ER visits (aOR = 2.4, 95% CI 1.4–3.9) and hospitalizations (aOR = 2.2, 95% CI 1.3–3.7).
Table 3:
Unadjusted Odds Ratios of demographics and clinical variables to malnutrition
| Demographics | Unadjusted Odds, 95% CI |
|---|---|
| Age group | |
| 60–64 | REF |
| 65–69 | 1.43 (0.78–2.63) |
| 70–74 | 1.29 (0.69–2.39) |
| 75–79 | 1.41 (0.69–2.87) |
| 80+ | 0.87 (0.42–1.81) |
| Sex | |
| Female | REF |
| Male | 1.08 (0.70–1.66) |
| Race | |
| White | REF |
| Black | 1.02 (0.62–1.70) |
| Other | 0.92 (0.13–6.66) |
| Educational level | |
| Less than high school | REF |
| High school graduate | 0.90 ( 0.47–1.74 ) |
| Some college | 1.03 ( 0.50–2.10 ) |
| Associate/Bachelors | 1.01 ( 0.52–1.94 ) |
| Advanced Degree | 1.02 ( 0.44–2.37 ) |
| Marital status | |
| Single | REF |
| Widowed/Divorced | 1.11 ( 0.44–2.81 ) |
| Married | 1.09 ( 0.45–2.61 ) |
| Clinical | |
| Cancer Type | |
| Colorectal | REF |
| Pancreatic | 3.14 (1.73–5.70) |
| Hepatobiliary | 1.14 (0.60–2.17) |
| Gastroesophageal | 2.58 (1.19–5.60) |
| Other | 1.58 (0.80–3.12) |
| Cancer Stage | |
| I/II | REF |
| III | 0.51 (0.28–0.92) |
| IV | 1.17 (0.70–1.96) |
Table 4:
Unadjusted and adjusted Odds Ratios of malnutrition to geriatric assessment impairments, health-related quality of life, and prior healthcare utilization
| Geriatric Assessment | Unadjusted Odds, 95% CI | Adjusted Odds*, 95% CI |
|---|---|---|
| ≥1 fall | 1.88 (1.07–3.31) | 2.10 (1.11–3.97) |
| Impaired (≥2) ECOG performance status | 11.6 (6.29–21.3) | 12.8 (6.50–25.2) |
| Reported limitations in walking one block | 3.87 (2.45–6.10) | 3.97 (2.32–6.80) |
| IADL dependence | 4.35 (2.74–6.92) | 4.09 (2.40–6.98) |
| ADL dependence | 4.88 (2.42–9.82) | 4.83 (2.25–10.4) |
| Moderate/Severe Cognitive Dysfunction | 4.33 (1.43–13.1) | 7.22 (1.87–27.8) |
| ≥3 comorbidities other than cancer | 1.71 (1.11–2.64) | 1.61 (0.97–2.67) |
| ≥9 daily medications | 0.90 (0.53–1.50) | 0.91 (0.51–1.62) |
| Limitations in social activities | 8.01 (4.13–15.5) | 7.73 (3.77–15.9) |
| Moderate/Severe Anxiety | 3.03 (1.63–5.64) | 3.03 (1.52–6.06) |
| Moderate/Severe Depression | 5.87 (2.53–13.6) | 5.06 (2.00–12.8) |
| Vision impairment | 1.59 (0.96–2.64) | 1.58 (0.89–2.79) |
| Hearing impairment | 1.43 (0.87–2.33) | 1.52 (0.86–2.71) |
| Moderate/severe Fatigue | 4.27 (2.68–6.78) | 4.81 (2.81–8.24) |
| Moderate/severe Pain | 4.31 (2.70–6.86) | 4.94 (2.85–8.58) |
| Frail | 7.92 (4.58–13.7) | 8.18 (4.37–15.3) |
| Financial Distress | 1.85 (0.83–4.11) | 1.94 ( 0.75–5.02 ) |
| Health-Related Quality of Life | ||
| Physical Health Score, ≤40 | 7.62 (4.44–13.1) | 8.67 (4.62–16.3) |
| Mental Health Score, ≤40 | 4.68 (2.70–8.12) | 5.01 (2.63–9.55) |
| Healthcare Utilization | ||
| ER visit | 2.13 (1.37–3.32) | 2.37 (1.43–3.94) |
| Hospitalization | 1.90 (1.21–2.99) | 2.22 (1.32–3.73) |
adjusted for age, sex, education, marital status, employment, cancer type, and cancer stage.
DISCUSSION
In this study, we found that nearly half of all older adults with GI malignancies have evidence of malnutrition with a significant variation in the prevalence and type of nutrition related symptoms across the GI cancer types. Furthermore, presence of malnutrition was associated with GA impairments, reduced HRQoL and increased odds of prior healthcare utilization. Our findings can be used to inform interventions adapted according to cancer type and stage.
Older adults with GI cancers, particularly gastroesophageal and pancreatic, have a higher risk of malnutrition compared to those with other cancers, including lung or head and neck.32 The prevalence of malnutrition in our study is consistent with the few other studies of older adults with cancer. In a recent study by Pinho et al., 55% of older adults had moderate/severe malnutrition and loss of appetite was most strongly associated with the odds of malnutrition.33 Similar to our findings, advanced stage has previously been shown to be a risk factor for malnutrition across most cancers.34 Interestingly, the association of malnutrition with cancer stage went away after adjustment of covariates, suggesting possible confounding by another variable within the model, such as cancer type. As the sample was obtained from new consultations within GI medical oncology, it could be that certain cancer types, such as pancreatic cancer, are seen at earlier stages than other cancer types within medical oncology at our academic center, particularly given the shift towards neoadjuvant therapy for nearly all new pancreatic cancer diagnoses regardless of stage. Thus the earlier staged patients may have cancer diagnoses with higher risks of malnutrition such as pancreatic cancer, hence obscuring the typical association of malnutrition with more advanced stages of cancer. Of note, pancreatic cancer is typically diagnosed at later stages, rather than early stages, but our sample is likely biased towards more early pancreatic diagnoses as these are more often managed in-house given the needed collaboration of our specialized surgical oncologist, whereas many patients with metastatic pancreatic cancer are managed within local community centers.
Nutritional symptoms, routinely assessed by the patient-reported portion of the PG-SGA, are commonly reported by patients with cancer. One study used the PG-SGA to examine symptom burden among patients with newly-diagnosed GI cancers, and found loss of appetite, early satiety and pain to be the most frequently reported symptoms.35 Moreover, cancers of the upper GI tract, especially pancreatic cancer, had a significantly higher number of symptoms reported compared to those with lower GI tumors, liver and biliary cancer who reported a median number of zero symptoms.35 Although our study is one of the first to report on these nutrition related symptoms in older adults with GI malignancies, these results are similar to our findings using the abPG-SGA where the most common symptoms reported included early satiety and lack of appetite especially among our pancreatic and gastroesophageal cohorts.
The association of malnutrition with GA impairments is less well-studied, particularly amongst GI malignancies. One large study of over 800 patients demonstrated that malnutrition, as measured by the mini-nutritional assessment (MNA), was associated with over 65% of fallers compared to 45% of non-fallers, while another study found no association with weight loss and falls.36,37 A study of over 400 older adults with cancer recently showed a 3.8-fold higher odds of having frailty, as measured by the Fried Frailty Phenotype, in those who screened positive with the MNA.38 Our results suggest an even stronger association between malnutrition and frailty (aOR 8.2) in our sample of older adults with GI malignancies, but this difference may in part be due to a different definition of frailty employed and differing study populations. Another longitudinal study by Tong et al also using the PG-SGA, found that nutrition-related symptoms may contribute to decreased performance status and HRQoL in adults with cancer.39 Of note, after adjustment of covariates, we found no association between malnutrition and comorbid conditions or hearing/vision impairments. This may in part be due to our use of the number of comorbidities rather than specific comorbid conditions, as we did see a strong association with the comorbid conditions of anxiety and depression. Furthermore, the comorbidity tool used in this study (the Older Americans Resources Services (OARS) comorbidity questionnaire) only includes 13 comorbid conditions and is not an exhaustive list of conditions.40,41
Psychological distress, manifesting commonly as depression and/or anxiety has also been implicated in one Chinese study of adult patients using the PG-SGA, but importantly participants were younger (mean age of 50y).42 Pain and/or somatization, in conjunction with depression and anxiety, in patients with lung cancer has also been reported with malnutrition similar to our study.43 Finally, cognitive impairment, another common age-related concern assessed by the GA, was previously associated with malnutrition (OR 1.77 (1.07–2.93) p = 0.027) in one Portuguese study.44
Given the strong association between malnutrition and depression and anxiety, our observed association between malnutrition and reduced HRQoL is not surprising. A systematic review by Lis et al in 2012 of 8 studies involving patients with GI cancers concluded that better nutritional status was associated with better HRQoL; however, none of these included studies specifically focused on older adults with GI malignancies.45 With regards to health care utilization, we reported increased hospitalization rates among those with malnutrition. A systematic review by Hazzard et al similarly found that nutrition-related problems were associated with unplanned admissions in patients with cancer undergoing radiotherapy.46 Another more recent study identified older age, >5% weight loss, hospital admission and metastatic disease as factors significantly associated with malnutrition.47
Nutrition is a recognized and critical domain within the GA based on the results of a Delphi consensus of geriatric oncology experts.48 From the origins of the development of a cancer-specific GA, nutrition assessment was included; however, how best to assess this domain remains unclear.22 Some have included nutrition assessment as a simple measure of unintentional weight loss along with measuring Body Mass Index (BMI), while others have utilized other standardized screening tools such as the MNA or the Nutritional Risk Screening (NRS).3,22,49–51 Although the PG-SGA is a commonly employed measure of nutrition, to our knowledge, this is the first study to employ this instrument as part of a routine GA for older adults with cancer. This measure was chosen given its common use in GI cancers and in the field of cancer cachexia research as well as its breadth of symptom assessment, which is critically important when considering nutritional interventions. The abbreviated version of this tool was utilized in order minimize staff time required to administer the longer assessment and to maintain a completely patient-reported assessment. Once a concern for malnutrition has been identified, a more thorough assessment of dietary intake, physical examination, and anthropometrics performed by a dietician should be performed, and a tailored nutrition intervention should be developed in conjunction with the clinical team.
This study should be considered in the context of its limitations. Due to the cross-sectional study design of our study, no causal inferences or directionality can be drawn between associations with malnutrition. Additionally, the study was limited to a single site in the southeastern United States (UAB), potentially limiting the external validity of our results. Although we had several significant predictors, our study results are based on a small sample size (N=336), thereby necessitating larger multi-center studies to further validate the results. Our study did not collect objective nutritional data (height, weight, BMI, laboratory results etc.) and defined malnutrition based completely on the abPG-SGA nutrition measure, which is a solely patient-reported measure. Our study also has several strengths. Although malnutrition has been thoroughly examined in GI cancers, very little data is available specific to the older adult and very few to date have incorporated a comprehensive GA.
In conclusion, our study highlights the potential impact and importance of nutrition and nutrition-based assessments in older adults with cancer, specifically those with gastrointestinal malignancies. With a majority of cancer diagnoses occurring in older patients and most nutritional cancer research being conducted in younger populations, there is a strong need for more studies aimed at investigating this population.5,12,24 In a world with an aging population, implementing nutritional assessments and GAs in order to develop personalized oncologic treatment plans is critical to improving outcomes and oncology care.
Acknowledgments:
This work was supported in part by grants from the National Institutes of Health (K08CA234225, G.W.). The content is solely the responsibility of the authors and does not necessarily represent the official view of the National Institutes of Health.
Footnotes
Conflict-of-interest disclosure: The authors declare no competing financial interests.
References:
- 1.Smith BD, Smith GL, Hurria A, Hortobagyi GN, Buchholz TA. Future of cancer incidence in the United States: burdens upon an aging, changing nation. Journal of clinical oncology : official journal of the American Society of Clinical Oncology. 2009;27(17):2758–2765. [DOI] [PubMed] [Google Scholar]
- 2.Jolly TA, Deal AM, Nyrop KA, et al. Geriatric assessment-identified deficits in older cancer patients with normal performance status. The oncologist. 2015;20(4):379–385. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 3.Mohile SG, Dale W, Somerfield MR, et al. Practical Assessment and Management of Vulnerabilities in Older Patients Receiving Chemotherapy: ASCO Guideline for Geriatric Oncology. Journal of clinical oncology : official journal of the American Society of Clinical Oncology. 2018;36(22):2326–2347. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 4.Wildiers H, Heeren P, Puts M, et al. International Society of Geriatric Oncology consensus on geriatric assessment in older patients with cancer. Journal of clinical oncology : official journal of the American Society of Clinical Oncology. 2014;32(24):2595–2603. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 5.Williams GR. Geriatric Assessment: Precision Medicine for Older Adults With Cancer. Journal of oncology practice / American Society of Clinical Oncology. 2018;14(2):97–98. [DOI] [PubMed] [Google Scholar]
- 6.Van Den Broeke C, De Burghgraeve T, Ummels M, et al. Occurrence of Malnutrition and Associated Factors in Community-Dwelling Older Adults: Those with a Recent Diagnosis of Cancer Are at Higher Risk. The journal of nutrition, health & aging. 2018;22(2):191–198. [DOI] [PubMed] [Google Scholar]
- 7.Zhang X, Edwards BJ. Malnutrition in Older Adults with Cancer. Curr Oncol Rep 2019;21(9):80. [DOI] [PubMed] [Google Scholar]
- 8.Mislang AR, Di Donato S, Hubbard J, et al. Nutritional management of older adults with gastrointestinal cancers: An International Society of Geriatric Oncology (SIOG) review paper. Journal of geriatric oncology. 2018;9(4):382–392. [DOI] [PubMed] [Google Scholar]
- 9.Williams GR, Rier HN, McDonald A, Shachar SS. Sarcopenia & aging in cancer. Journal of geriatric oncology. 2018. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 10.Nishijima TF, Deal AM, Lund JL, Nyrop KA, Muss HB, Sanoff HK. The incremental value of a geriatric assessment-derived three-item scale on estimating overall survival in older adults with cancer. Journal of geriatric oncology. 2018;9(4):329–336. [DOI] [PubMed] [Google Scholar]
- 11.Zhang X, Tang T, Pang L, et al. Malnutrition and overall survival in older adults with cancer: A systematic review and meta-analysis. Journal of geriatric oncology. 2019. [DOI] [PubMed] [Google Scholar]
- 12.Extermann M, Boler I, Reich RR, et al. Predicting the risk of chemotherapy toxicity in older patients: the Chemotherapy Risk Assessment Scale for High-Age Patients (CRASH) score. Cancer. 2012;118(13):3377–3386. [DOI] [PubMed] [Google Scholar]
- 13.Dotan E, Tew WP, Mohile SG, et al. Associations between nutritional factors and chemotherapy toxicity in older adults with solid tumors. Cancer. 2020. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 14.Presley CJ, Dotan E, Soto-Perez-de-Celis E, et al. Gaps in nutritional research among older adults with cancer. Journal of geriatric oncology. 2016;7(4):281–292. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 15.Arends J, Bachmann P, Baracos V, et al. ESPEN guidelines on nutrition in cancer patients. Clin Nutr 2017;36(1):11–48. [DOI] [PubMed] [Google Scholar]
- 16.Williams GR, Kenzik KM, Parman M, et al. Integrating geriatric assessment into routine gastrointestinal (GI) consultation: The Cancer and Aging Resilience Evaluation (CARE). Journal of geriatric oncology. 2020;11(2):270–273. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 17.Gabrielson DK, Scaffidi D, Leung E, et al. Use of an abridged scored Patient-Generated Subjective Global Assessment (abPG-SGA) as a nutritional screening tool for cancer patients in an outpatient setting. Nutr Cancer. 2013;65(2):234–239. [DOI] [PubMed] [Google Scholar]
- 18.Vigano AL, di Tomasso J, Kilgour RD, et al. The abridged patient-generated subjective global assessment is a useful tool for early detection and characterization of cancer cachexia. J Acad Nutr Diet 2014;114(7):1088–1098. [DOI] [PubMed] [Google Scholar]
- 19.Abbott J, Teleni L, McKavanagh D, Watson J, McCarthy AL, Isenring E. Patient-Generated Subjective Global Assessment Short Form (PG-SGA SF) is a valid screening tool in chemotherapy outpatients. Support Care Cancer. 2016;24(9):3883–3887. [DOI] [PubMed] [Google Scholar]
- 20.Bauer J, Capra S, Ferguson M. Use of the scored Patient-Generated Subjective Global Assessment (PG-SGA) as a nutrition assessment tool in patients with cancer. Eur J Clin Nutr 2002;56(8):779–785. [DOI] [PubMed] [Google Scholar]
- 21.Hurria A, Cirrincione CT, Muss HB, et al. Implementing a geriatric assessment in cooperative group clinical cancer trials: CALGB 360401. Journal of clinical oncology : official journal of the American Society of Clinical Oncology. 2011;29(10):1290–1296. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 22.Hurria A, Gupta S, Zauderer M, et al. Developing a cancer-specific geriatric assessment: a feasibility study. Cancer. 2005;104(9):1998–2005. [DOI] [PubMed] [Google Scholar]
- 23.Williams GR, Deal AM, Jolly TA, et al. Feasibility of geriatric assessment in community oncology clinics. Journal of geriatric oncology. 2014;5(3):245–251. [DOI] [PubMed] [Google Scholar]
- 24.Williams GR, Deal AM, Lund JL, et al. Patient-Reported Comorbidity and Survival in Older Adults with Cancer. The oncologist. 2018;23(4):433–439. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 25.Knight TG, Deal AM, Dusetzina SB, et al. Financial Toxicity in Adults With Cancer: Adverse Outcomes and Noncompliance. Journal of oncology practice / American Society of Clinical Oncology. 2018:JOP1800120. [DOI] [PubMed] [Google Scholar]
- 26.Rockwood K, Mitnitski A. Frailty in relation to the accumulation of deficits. The journals of gerontology Series A, Biological sciences and medical sciences. 2007;62(7):722–727. [DOI] [PubMed] [Google Scholar]
- 27.Guerard EJ, Deal AM, Chang Y, et al. Frailty Index Developed From a Cancer-Specific Geriatric Assessment and the Association With Mortality Among Older Adults With Cancer. Journal of the National Comprehensive Cancer Network : JNCCN 2017;15(7):894–902. [DOI] [PubMed] [Google Scholar]
- 28.Williams GR, Deal AM, Sanoff HK, et al. Frailty and health-related quality of life in older women with breast cancer. Support Care Cancer. 2019;27(7):2693–2698. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 29.Hays RD, Bjorner JB, Revicki DA, Spritzer KL, Cella D. Development of physical and mental health summary scores from the patient-reported outcomes measurement information system (PROMIS) global items. Quality of life research : an international journal of quality of life aspects of treatment, care and rehabilitation. 2009;18(7):873–880. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 30.Pergolotti M, Deal AM, Williams GR, et al. Activities, function, and health-related quality of life (HRQOL) of older adults with cancer. Journal of geriatric oncology. 2017. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 31.Yost KJ, Eton DT, Garcia SF, Cella D. Minimally important differences were estimated for six Patient-Reported Outcomes Measurement Information System-Cancer scales in advanced-stage cancer patients. Journal of clinical epidemiology. 2011;64(5):507–516. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 32.Muscaritoli M, Lucia S, Farcomeni A, et al. Prevalence of malnutrition in patients at first medical oncology visit: the PreMiO study. Oncotarget. 2017;8(45):79884–79896. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 33.de Pinho NB, Martucci RB, Rodrigues VD, et al. High prevalence of malnutrition and nutrition impact symptoms in older patients with cancer: Results of a Brazilian multicenter study. Cancer. 2020;126(1):156–164. [DOI] [PubMed] [Google Scholar]
- 34.Wie GA, Cho YA, Kim SY, Kim SM, Bae JM, Joung H. Prevalence and risk factors of malnutrition among cancer patients according to tumor location and stage in the National Cancer Center in Korea. Nutrition. 2010;26(3):263–268. [DOI] [PubMed] [Google Scholar]
- 35.Khalid U, Spiro A, Baldwin C, et al. Symptoms and weight loss in patients with gastrointestinal and lung cancer at presentation. Support Care Cancer. 2007;15(1):39–46. [DOI] [PubMed] [Google Scholar]
- 36.Vande Walle N, Kenis C, Heeren P, et al. Fall predictors in older cancer patients: a multicenter prospective study. BMC geriatrics. 2014;14:135. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 37.Williams GR, Deal AM, Nyrop KA, et al. Geriatric assessment as an aide to understanding falls in older adults with cancer. Support Care Cancer. 2015;23(8):2273–2280. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 38.Zhang X, Pang L, Sharma SV, Li R, Nyitray AG, Edwards BJ. Prevalence and factors associated with malnutrition in older patients with cancer. Journal of geriatric oncology. 2019;10(5):763–769. [DOI] [PubMed] [Google Scholar]
- 39.Tong H, Isenring E, Yates P. The prevalence of nutrition impact symptoms and their relationship to quality of life and clinical outcomes in medical oncology patients. Support Care Cancer. 2009;17(1):83–90. [DOI] [PubMed] [Google Scholar]
- 40.Fillenbaum GG, Smyer MA. The Development, Validity, and Reliability of the Oars Multidimensional Functional Assessment Questionnaire. J Gerontol 1981;36(4):428–434. [DOI] [PubMed] [Google Scholar]
- 41.Williams GR, Mackenzie A, Magnuson A, et al. Comorbidity in older adults with cancer. Journal of geriatric oncology. 2016;7(4):249–257. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 42.Zhu C, Wang B, Gao Y, Ma X. Prevalence and relationship of malnutrition and distress in patients with Cancer using questionnaires. BMC Cancer. 2018;18(1):1272. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 43.Chabowski M, Polanski J, Jankowska-Polanska B, Janczak D, Rosinczuk J. Is nutritional status associated with the level of anxiety, depression and pain in patients with lung cancer? J Thorac Dis 2018;10(4):2303–2310. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 44.Dos Santos CA, Ribeiro AQ, Rosa Cde O, Ribeiro Rde C. [Depression, cognitive deficit and factors associated with malnutrition in elderly people with cancer]. Cien Saude Colet 2015;20(3):751–760. [DOI] [PubMed] [Google Scholar]
- 45.Lis CG, Gupta D, Lammersfeld CA, Markman M, Vashi PG. Role of nutritional status in predicting quality of life outcomes in cancer--a systematic review of the epidemiological literature. Nutr J 2012;11:27. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 46.Hazzard E, Walton K, McMahon AT, Milosavljevic M, Tapsell LC. Nutrition-related hospital presentations and admissions among radiotherapy outpatients: a systematic literature review. J Hum Nutr Diet 2018;31(3):357–369. [DOI] [PubMed] [Google Scholar]
- 47.Marshall KM, Loeliger J, Nolte L, Kelaart A, Kiss NK. Prevalence of malnutrition and impact on clinical outcomes in cancer services: A comparison of two time points. Clin Nutr 2019;38(2):644–651. [DOI] [PubMed] [Google Scholar]
- 48.Mohile SG, Velarde C, Hurria A, et al. Geriatric Assessment-Guided Care Processes for Older Adults: A Delphi Consensus of Geriatric Oncology Experts. Journal of the National Comprehensive Cancer Network : JNCCN 2015;13(9):1120–1130. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 49.Kaiser MJ, Bauer JM, Ramsch C, et al. Validation of the Mini Nutritional Assessment short-form (MNA-SF): a practical tool for identification of nutritional status. The journal of nutrition, health & aging 2009;13(9):782–788. [DOI] [PubMed] [Google Scholar]
- 50.Kondrup J, Rasmussen HH, Hamberg O, Stanga Z, Ad Hoc EWG. Nutritional risk screening (NRS 2002): a new method based on an analysis of controlled clinical trials. Clin Nutr 2003;22(3):321–336. [DOI] [PubMed] [Google Scholar]
- 51.Isenring E, Elia M. Which screening method is appropriate for older cancer patients at risk for malnutrition? Nutrition. 2015;31(4):594–597. [DOI] [PubMed] [Google Scholar]