Nutrient Intakes and Gastrointestinal Symptoms Among Esophagogastric Cancer Survivors up to 5 Years Post-Surgery

Abstract

A cross-sectional analysis explored nutritional intakes and gastrointestinal (GI) symptoms among esophagogastric cancer survivors up to 12, 13–36, and 37+ months post-surgery. Participants were identified from the Upper GI Cancer Registry at St James’ Hospital, Ireland. The Short Nutritional Assessment Questionnaire, European Prospective Investigation of Cancer Food Frequency Questionnaire, World Cancer Research Fund/American Institute for Cancer Research (WCRF/AICR) Score, and Gastrointestinal Symptoms Rating Scale assessed malnutrition risk, nutritional intake, adherence to (secondary) cancer prevention recommendations, and GI symptoms, respectively. Most (82.5%, n33) participants (n40) were male. Mean age was 65.5 ± 9.3 years. Time post-surgery ranged from 6-62 months. Half (50.0%, n20) had a BMI in the healthy range. A quarter (27.5%, n11) were at risk of malnutrition. Intakes of meat and meat products exceeded recommendations and intakes of fruits, vegetables, and fiber were below recommendations, with no significant between-group differences. The mean WCRF/AICR score was 3.6 ± 1.1, indicating adherence to 3.6 of 7 cancer prevention recommendations. It was not significantly different between subgroups. Minor to mild GI discomfort was reported, with no significant between-group differences in symptoms. As rates of long-term survivorship continue to increase, survivors must be supported to sustain behaviors that enhance quality of life and reduce secondary cancer risk.

Introduction

Ireland has the second-highest incidence of recorded cancer cases globally, with 326.6 cases per 100,000 of the population compared to the global average of 190.0 cases per 100,000 (1). Gastric and esophageal cancers are the 8th (2) and 14th (3) most common cancers in Ireland, respectively. The 5-year survival rates for all cases of gastric or esophageal cancer are 27% and 23%, respectively, partly due to a significant proportion of cases being diagnosed at advanced stages (2, 4, 5). However, significant improvements in the surveillance, detection, treatment, and management of these diseases in recent decades are evident (4, 6), with, for example, the survival rate for those presenting with locally advanced esophageal cancer now approaching 50% (4, 5).

Despite these improvements in survival, the development and treatment of esophagogastric cancer often results in decrements in function, to include muscle loss (7–9), fatigue (10, 11), social limitations (9, 12), and swallowing and other food-related difficulties (11, 13). Malnutrition is common, ranging from 22% to 62%, depending on the stage of diagnosis, treatment, or recovery (14, 15). Long-term consequences of disease management can affect a significant proportion of survivors, with over a third experiencing symptoms associated with their treatment, more than a year after surgery (16). In the Lasting Symptoms After Esophageal Resection (LASER) Study, for example, approximately three-quarters of participants who were at least 12 months post-surgery reported experiencing ongoing early satiety, reduced energy levels, and/or heartburn (16).

As the number of survivors increases, healthcare services must be coordinated to manage the consequences of treatment and to ensure that survivors are supported to implement behaviors that reduce the risk of new and recurrent cancers (17, 18). The World Cancer Research Fund (WCRF) includes among its recommendations for primary and secondary cancer prevention and cancer survival (19) that persons maintain a healthy weight, be physically active, eat a diet rich in wholegrains, vegetables, and fruits, avoid high-calorie foodstuffs, and limit red and processed meats and sugar-sweetened drinks. However, the capacity of survivors to adhere to recommendations may be impacted by symptoms experienced after treatment, such as difficulty consuming a diet rich in wholegrains, vegetables, and fruits when an individual is prone to early satiety (16), diarrhea (10, 11), or weight loss (14, 20, 21).

Research on the long-term nutritional intakes and GI symptoms of survivors of esophagogastric cancer is limited. To better understand the short- and long- term opportunities to optimize nutritional status and secondary cancer prevention, this study aimed to explore nutritional intakes and GI symptoms among esophagogastric cancer survivors up to 12 months, 13–36 months, and 37+ months post-surgery.

Methods

Participants were identified from the Upper Gastrointestinal (UGI) Cancer Registry at St James’ Hospital, Dublin, Ireland. Persons that had completed treatment with curative intent for esophageal, esophagogastric, or gastric cancer in the 5 years prior, and who were in remission, were eligible to participate. Persons with evidence of metastatic or recurrent disease and/or a lack of medical approval to participate, were ineligible for recruitment. Eligible persons were invited to participate by letter and provided written informed consent in advance of data collection.

Demographic Data

Data were collected from medical records on age, smoking status, relevant medical history (gastroesophageal reflux disease (GERD) and Barrett’s Esophagus), and treatment history (neoadjuvant and adjuvant therapy).

Anthropometric Measures and Activity Levels

Anthropometric measures were taken in the Wellcome Trust-Health Research Board Clinical Research Facility (CRF) at St James’ Hospital.

Weight (kg) was obtained using a calibrated SECA digital medical scale. Height (cm) was measured, without shoes, using a SECA stadiometer. Body mass index (BMI) was calculated as (weight (kg))/(height (m²)). Waist circumference (cm) was measured to the nearest millimeter with a flexible measuring tape at the midpoint between the iliac crest and the 12th rib following gentle expiration. Waist circumference was measured in duplicate and averaged for data entry.

Activity levels were monitored by an Actigraph GT3X+ (Actigraph, Pensacola, Florida), a triaxial accelerometer. Participants wore the monitor during waking hours for one week prior to attending the CRF for anthropometric measurements. Monitor wear and non-wear time was logged in an activity diary.

Nutritional intake, Malnutrition, and Secondary Cancer Prevention

Habitual nutritional intake was assessed using the 131-item European Prospective Investigation of Cancer (EPIC) Food Frequency Questionnaire (FFQ) (22, 23). Data were converted to nutrient intakes using the FETA FFQ EPIC Tool for Analysis (version 6.0). The adequacy of total energy, macronutrient and micronutrient intakes, and the contribution of each macronutrient to total energy intake, was assessed in line with relevant national (24, 25) and international (19, 26, 27) guidelines.

Malnutrition risk was assessed using the 4-item Short Nutritional Assessment Questionnaire (SNAQ) (28). Items are cumulatively tallied to a maximum score of 19 points. Scores <14 points indicate a risk of undernutrition.

The WCRF and American Institute for Cancer Research (AICR) Score (29, 30) is a standardized scoring system used to assess adherence to the WCRF/AICR Cancer Prevention Recommendations. The score is based on adherence to 7 core recommendations and one optional recommendation (related to breastfeeding). Adherence to the 7 core recommendations was examined in this study (31). A recommendation is scored as 1, 0.5, or 0 points for meeting, partially meeting, or not meeting the recommendation, respectively. Two recommendations (have a healthy weight and eat a diet rich in wholegrains, vegetables, fruits, and beans) have two sub-recommendations, with the sub-recommendations each scored as 0.5, 0.25, or 0 points for meeting, partially meeting, or not meeting the sub-recommendation, respectively. The final score ranges from 0-7, with a higher score indicating greater adherence to recommendations. Anthropometric measurements, Actigraph data, and data from the EPIC FFQ were used to determine the score for relevant recommendations.

Two components of the WCRF/AICR score were modified: % calories consumed from ultra-processed foods (aUPFs) and weekly consumption of red and processed meat. The output of the EPIC FFQ did not permit the creation of tertiles using % calories consumed from aUPFs, so the data were categorized into tertiles based on grams (g) of snacks and jams consumed. The same scoring applied, with 1, 0.5, and 0 points assigned to the lowest, middle, and highest tertiles, respectively. The output of the EPIC FFQ also did not permit grams of white, red, and processed meats to be analyzed separately, so meat (chicken, turkey, beef, pork, lamb) and meat products (e.g. bacon, corned beef, sausages, and beef burgers) were analyzed as a composite weight. The WCRF/AICR cutoffs were amended to reflect national recommendations (24) on grams of cooked white (50–75 g per day up to 3 days a week), red (50–75 g per day up to 3 days a week), and processed (limited) meat consumed weekly. Scores of 1, 0.5, and 0 were assigned to daily intakes of ≤43 g (≤150 g red meat + ≤150 g white meat divided by 7 days), 44–64 g (151–225 g red meat + 151–225 g white meat divided by 7 days), and ≥65 g (≥225 g red meat + ≥225 g white meat divided by 7 days), respectively.

Gastrointestinal Symptoms

The 15-item Gastrointestinal Symptoms Rating Scale (GSRS) (32) provided ratings for five gastrointestinal symptom clusters: abdominal pain, diarrhea, constipation, reflux, and indigestion. Each item was rated on a 7-point Likert scale, ranging from no discomfort to very severe discomfort over the past 7 days. The mean score of 3 items determined the score for the overall cluster to which those 3 items belong. The composite scores of items on stomach pain, hunger, and nausea contribute to the overall score for Abdominal Pain. The composite scores of items on diarrhea, loose stools, and the urgent need to have a bowel movement contribute to the overall score for Diarrhea. The composite scores of items on constipation, hard stools, and the sensation of not emptying bowels upon defecating contribute to the overall score for Constipation. The composite scores of items on heartburn and acid reflux contribute to the overall score for Reflux. The composite scores of items on borborygmus, bloating, burping, and flatus contribute to the overall score for Indigestion. Higher scores indicate more severe GI symptoms.

Analysis

Data were entered into SPSS (version 27) and assessed for normality. Data were presented descriptively using counts and percentages. Normally distributed data were presented using the mean and standard deviation and non-normally distributed data were presented using the median and interquartile range (IQR). Participant characteristics, nutritional intakes, and GI symptoms were summarized numerically for the full cohort. Participants were also categorized based on time post-surgery, that is, up to 12 months post-surgery, 13–36 months post-surgery, and 37+ months post-surgery. Comparisons of nutritional intakes, WCRF/AICR scores, and GI symptoms between the three subgroups were made using a one-way between-groups ANOVA with post-hoc tests. Actigraph data were analyzed using Actilife 6 software. Moderate-to-vigorous physical activity (MVPA) levels were assessed using Freedson (1998) cut-points (33). Statistical significance was taken at p < 0.05.

Results

Demographics

Most (82.5%, n33) of the 40 participants were male and almost one in five (17.5%, n7) were female (Table 1). The mean age of the total group was 65.5 ± 9.3 years and mean time post-surgery was 28.8 ± 18.4 months (range 6–62 months). A majority (80.0%, n32) of participants had been diagnosed with esophageal cancer and 20.0% (n8) had been diagnosed with gastric cancer (Table 1).

Table 1. Health and demographic characteristics of 40 esophago-gastric cancer survivors.

	Total group, n40		6–12 m post-op, n12		13–36 m post-op, n14		37+ m post-op, n14
	Mean ± SD		Mean ± SD		Mean ± SD		Mean ± SD
Time post-surgery (months)	28.8 ± 18.5		8.6 ± 1.7		25.3 ± 9.4		49.7 ± 8.5
Age (years)	65.5 ± 9.3		60.8 ± 6.9		67.2 ± 11.1		67.9 ± 7.2
BMI (kg/m^2)	25.8 ± 4.5		25.5 ± 3.1		26.3 ± 5.0		25.5 ± 5.2
Weight (kg)
Male	76.8 ± 14.4		78.6 ± 12.1		78.8 ± 16.9		72.5 ± 13.9
Female	62.4 ± 12.4		60.9 ± 0.0		55.3 ± 3.6		66.3 ± 15.8
Waist circumference (cm)
Male	94.1 ± 13.0		95.5 ± 8.3		94.5 ± 17.2		92.4 ± 12.5
Female	84.0 ± 11.1		80.3 ± 0.0		78.3 ± 8.6		87.8 ± 13.4
	n	%	n	%	n	%	n	%
Gender
Male	33	82.5	11	91.7	12	85.7	10	71.4
Female	7	17.5	1	8.3	2	14.3	4	28.6
Smoking status
Current	2	5.0	1	8.3	1	7.1	0	0
Ex-smoker	33	82.5	10	83.3	10	71.4	13	92.9
Never smoked	5	12.5	1	8.3	3	21.4	1	7.1
Had Barrett’s esophagus	17	42.5	6	50.0	6	42.9	5	35.7
Had GERD	16	40.0	3	25.0	4	28.6	9	64.3
Cancer type
Esophageal	32	80.0	12	100.0	11	78.6	9	64.3
Gastric	8	20.0	0	0	3	21.4	5	35.7
Tumor type
Adenocarcinoma	32	80.0	9	75.0	12	85.7	11	78.6
Squamous cell carcinoma	6	15.0	3	25.0	1	7.1	2	14.3
Associated Barrett’s	2	5.0	0	0	1	7.1	1	7.1
Had neoadjuvant therapy	25	62.5	8	66.7	9	64.3	8	57.1
Had adjuvant therapy	10	25.0	4	33.3	3	21.4	3	21.4
BMI category†
Healthy (18.5–25.0 kg/m^2)	20	50.0	6	50.0	7	50.0	7	50.0
Overweight (25.1–29.9 kg/m^2)	12	30.0	5	41.7	3	21.4	4	28.6
Obese (≥30.0 kg/m^2)	8	20.0	1	8.3	4	28.6	3	21.4
Meeting MVPA guidelines	18	45.0	4	33.3	6	42.9	8	57.1
Male waist circumference‡
Low risk (<94 cm)	14	42.4	4	36.4	6	50.0	4	40.0
High risk (94–102 cm)	10	30.3	4	36.4	1	8.3	5	50.0
Very high risk (>102 cm)	9	27.3	3	27.3	5	41.7	1	10.0
Female waist circumference‡
Low risk (<80 cm)	3	42.9	0	0	1	50.0	2	50.0
High risk (80–88 cm)	2	28.6	1	100.0	1	50.0	0	0
Very high risk (>88 cm)	2	28.6	0	0	0	0	2	50.0

Abbreviations: BMI: body mass index; GERD: gastroesophageal reflux disease; MVPA: moderate-to-vigorous physical activity; SD: standard deviation.

Most (82.5%, n33) participants were ex-smokers, with the highest proportion (39.4%, n13) of ex-smokers being in the 37+ months post-surgery category. Only 12.5% (n5) of the total group had never smoked and 5.0% (n2) were smoking at the time of the study (Table 1).

Anthropometric Measures and Activity Levels

Half (50.0%, n20) of the total group and of each subgroup had a BMI in the healthy range (Table 1), with 30.0% (n12) and 20.0% (n8) of the total group having a BMI in the overweight and obese categories, respectively. The subgroup that was 6–12 months post-surgery had the highest proportion (41.7%, n5) of persons with a BMI in the overweight category. The subgroup that was 13–36 months post-surgery had the highest proportion (28.6%, n4) of persons with a BMI in the obese category. No participant had an underweight BMI.

In terms of waist circumference and associated elevated cardiac risk, 42.4% (n14) of male participants and 42.9% (n3) of female participants had a waist circumference in the low-risk category, while all remaining participants presented with waist circumferences categorized as high or very high risk (Table 1).

MVPA levels were lowest among those who were 6–12 months post-surgery (Table 1) and highest among those who were 37+ months post-surgery, with more than two in five (45.0%, n18) of the total group meeting the activity guidelines.

Nutritional intakes, Malnutrition, and Secondary Cancer Prevention

Participants within 12 months of surgery had statistically significantly higher fat (129 ± 46 g), fiber (21 ± 9 g), folate (385 ± 154 µg), copper (0.8 ± 0.6 mg), and iron (15 ± 4 mg) intakes when compared to participants that were 13–36 months post-surgery (86 ± 28 g, 13 ± 3 g, 264 ± 42 µg, 0.7 ± 0.4 mg, and 10 ± 2 mg respectively) (Table 2). There were no significant differences between the intakes of those who were 13–36 months post-surgery and those who were 37+ months post-surgery.

Table 2. Daily nutrient intakes of 40 esophago-gastric cancer survivors.

	Total group, n40	6–12 m post-op, n12	13–36 m post-op, n14	37+ m post-op, n14	p†
	Mean ± SD	Mean ± SD	Mean ± SD	Mean ± SD
Macronutrients
Energy (kJ)	10079 ± 3486	11899 ± 3652	8776 ± 2400	9822 ± 3803	0.07
Energy (kcal)	2399 ± 831	2833 ± 869	2085 ± 570	2340 ± 909	0.07
Energy (kcal/kg)	33 ± 12	38 ± 14	29 ± 11	33 ± 11	0.19
Protein (g)	105 ± 46	121 ± 41	88 ± 21	109 ± 62	0.18
Total fat (g)	109 ± 45	*129 ± 46	*86 ± 28	114 ± 51	0.05
SFA (g)	45 ± 20	53 ± 20	35 ± 12	47 ± 23	0.06
MUFA (g)	39 ± 16	*47 ± 17	29 ± 10	*41 ± 18	0.02
PUFA (g)	15 ± 8	17 ± 6	13 ± 6	15 ± 9	0.48
Total CHO (g)	260 ± 98	309 ± 112	249 ± 86	229 ± 86	0.10
NSP (g)	17 ± 7	*21 ± 9	*13 ± 3	17 ± 7	0.04
Alcohol^§ (g)	4 ± 7	5 ± 9	3 ± 4	4 ± 9	0.87
Vitamins
Retinol (µg)	1111 ± 1716	1976 ± 2920	752 ± 549	727 ± 574	0.11
Thiamine (mg)	2 ± 1	2 ± 0	2 ± 0	2 ± 1	0.18
Riboflavin (mg)	2 ± 1	3 ± 1	2 ± 1	2 ± 1	0.05
Niacin (mg)	25 ± 11	29 ± 8	29 ± 8	26 ± 15	0.18
Pyridoxine (mg)	3 ± 1	3 ± 1	2 ± 0	3 ± 1	0.24
Folate (µg)	311 ± 115	*385 ± 154	*264 ± 42	296 ± 101	0.02
Cobalamin (µg)	10 ± 9	14 ± 13	8 ± 4	9 ± 6	0.11
Vitamin C (mg)	100 ± 69	137 ± 101	74 ± 41	94 ± 45	0.06
Vitamin D (µg)	4 ± 3	5 ± 3	3 ± 2	5 ± 4	0.22
Vitamin E (mg)	13 ± 6	14 ± 5	12 ± 5	13 ± 8	0.72
Minerals
Calcium (mg)	1056 ± 444	1288 ± 533	940 ± 263	973 ± 457	0.09
Copper (mg)	0.5 ± 1.0	^*‡0.8 ± 1.6	*0.7 ± 0.4	^‡0.5 ± 0.6	0.03
Iodine (µg)	60 ± 99	81 ± 129	60 ± 71	88 ± 88	0.24
Iron (mg)	12 ± 4	*15 ± 4	*10 ± 2	12 ± 5	0.03
Magnesium (mg)	350 ± 117	399 ± 130	318 ± 76	341 ± 133	0.20
Phosphorus (mg)	763 ± 632	1000 ± 677	763 ± 337	869 ± 755	0.12
Potassium (mg)	1919 ± 1214	2962 ± 1358	2095 ± 644	1919 ± 1464	0.26
Selenium (µg)	81 ± 41	95 ± 45	73 ± 29	95 ± 45	0.40
Sodium (mg)	3478 ± 1371	4083 ± 1325	2828 ± 942	4083 ± 1325	0.06
Zinc (mg)	12 ± 5	14 ± 4	10 ± 2	14 ± 4	0.17

Note: p < 0.05.

Abbreviations: SD: standard deviation; SFA: saturated fatty acid; MUFA: monounsaturated fatty acid; PUFA: polyunsaturated fatty acid; CHO: Carbohydrate; NSP: non-starch polysaccharide.

^§One standard drink contains 10 g alcohol (25) under Irish guidelines.

^†One-way between-groups ANOVA with post-hoc tests.

^*Statistically significant difference (p < 0.05) between two variables.

^‡Statistically significant difference (p < 0.05) between two variables.

Among the full cohort, mean protein intake (105 ± 46 g) accounted for 17.5% of total energy intake. Mean total fat (109 ± 45 g) and saturated fat intakes (45 ± 20 g) represented 40.9% and 16.9% of total energy intake, respectively. Mean carbohydrate intake (260 ± 98 g) accounted for 43.4% of total energy intake.

Mean intakes of fiber, Vitamin D, copper, iodine, and potassium were below recommended intakes (34, 35), whereas mean sodium intakes exceeded public health recommendations (36) across all three subgroups (Table 2). The proportions that always or usually added salt during cooking were 41.6% (n5), 50.0% (n7), and 42.8% (n6) of those that were 6–12 months, 13–36 months, and 37+ months post-surgery, respectively. The proportions that always or usually added salt at the table were 16.7% (n2), 57.1% (n8), and 64.2% (n9) of those that were 6-12 months, 13–36 months, and 37+ months post-surgery, respectively.

Vegetables were eaten daily by 50.5% (n6), 35.7% (n5), and 50.0% (n7) of those that were 6–12 months, 13–36 months, and 37+ months post-surgery, respectively. Fruits were eaten daily by 50.5% (n6), 35.7% (n5), and 57.1% (n8) of those that were 6–12 months, 13–36 months, and 37+ months post-surgery, respectively. The total group consumed a median of 287 g (approx. 3.7 portions) fruits and vegetables daily. The median weight of fruits and vegetables consumed were 392 g (approx. 5 portions), 233 g (approx. 3 portions), and 343 g (approx. 4.5 portions) among those who were 6–12 months, 13–36 months, and 37+ months post-surgery, respectively. There were no statistically significant (p = 0.484) between-group differences in fruit and vegetable intakes.

Meat (red and white meat) and meat products were consumed by almost all (97.5%, n39) participants. A median of 120 g (IQR 95) cooked meat and meat products per day was consumed by the total group, with those that were 6–12 months, 13–36 months, and 37+ months post-surgery consuming a median of 136 g (IQR 112), 112 g (IQR 75), and 136 g (IQR 173) per day, respectively. There were no statistically significant (p = 0.313) between-group differences in meat and meat product consumption.

The range for SNAQ scores (Table 3) was widest for those that were 6–12 months post-surgery, ranging from 4 to 18. SNAQ scores for those 13–36 months and 37+ months post-surgery ranged from 11–18 and 10–18, respectively. Of the total group, 27.5% (n11) scored <14 on the SNAQ, indicating a risk of malnutrition. The proportion of each subgroup that scored <14 on the SNAQ was 33.3% (n4), 28.6% (n4), and 21.4% (n3) for 6–12 months, 13–36 months, and 37+ months post-surgery, respectively.

Table 3. Appetite score and gastrointestinal symptoms among 40 esophago-gastric cancer survivors.

	Total group, n40	6–12 m post-op, n12	13–36 m post-op, n14	37+ m post-op, n14	p^†
	Median (IQR)	Median (IQR)	Median (IQR)	Median (IQR)
Malnutrition risk
SNAQ score	14.5 (3.0)	14.5 (3.5)	15.0 (3.3)	14.0 (2.8)	0.77
	Mean ± SD	Mean ± SD	Mean ± SD	Mean ± SD
GSRS
Abdominal pain	1.98 ± 1.05	2.03 ± 1.14	1.97 ± 1.07	1.95 ± 1.06	0.98
Diarrhea	2.04 ± 1.29	2.41 ± 1.49	1.57 ± 0.68	2.19 ± 1.49	0.21
Constipation	1.85 ± 1.17	2.00 ± 1.26	1.45 ± 0.97	2.12 ± 1.24	0.31
Reflux	1.79 ± 1.18	2.13 ± 1.46	1.50 ± 0.98	1.81 ± 1.09	0.38
Indigestion	2.60 ± 1.39	2.84 ± 1.36	2.29 ± 1.29	2.73 ± 1.54	0.58

Note: p < 0.05.

Abbreviations: IQR: interquartile range; SD: standard deviation; SNAQ: simplified nutritional appetite questionnaire; GSRS: gastrointestinal symptoms rating scale.

^†One-way between-groups ANOVA with post-hoc tests.

The mean WCRF/AICR score for the total group was 3.6 ± 1.1 (range 0.75–5.5), indicating adherence to an average of 3.6 of the 7 cancer prevention recommendations included. Mean scores for each subgroup were 3.3, 3.4, and 3.9 for those that were 6–12 months, 13–36 months, and 37+ months post-surgery, respectively. There were no statistically significant between-group differences (p = 0.432).

Gastrointestinal Symptoms

There were no significant between-group differences in gastrointestinal symptoms (Table 3). Average scores indicated that discomfort levels ranged from minor (score on scale = 2) to mild (score on scale = 3) discomfort. Abdominal pain, constipation, and reflux were more commonly reported as minor symptoms, while indigestion and constipation were more commonly reported as mild symptoms (Table 3).

Discussion

It is well-established that as an upper GI cancer, esophagogastric cancer has profound short- and medium- (8, 11, 14, 21, 37, 38) term effects on the nutritional status of those diagnosed. As the 5-year survival rate continues to improve (4), there is greater exploration of the long-term impacts of GI symptoms and nutritional changes on health outcomes (16), and on factors that play a role in secondary cancer prevention. This analysis explored cross-sectional nutrient intakes and GI symptoms at 3 timepoints across a 5-year period after curative treatment for esophagogastric cancer. At all timepoints, a risk of malnutrition was evident, discomfiting GI symptoms were reported, overweight and obesity were present in half of participants, and adherence to nutritional guidance for secondary cancer prevention (19) was limited.

The proportion of participants at risk of malnutrition in the present study ranged from a fifth to a third, with scores highest among those who were 13–36 months post-surgery. Nutritional challenges are common, with findings in the current study reflecting several findings in the LASER study (16), a multicenter European study of over 800 disease-free patients that underwent esophageal cancer resection. The LASER study reported that over 40% of participants struggled to maintain their weight or continued to lose weight, more than one year post completion of treatment. In the current study, caloric intakes were lowest among individuals who were 13–36 months post-surgery. Although their intakes were not statistically significantly lower relative to the intakes of those who were 6–12 and 37+ months post-surgery, this finding may highlight the value of nutrition support from dietitians which was provided throughout the first 12 months post-surgery, and possibly indicate that challenges to nutritional intake persist for several years post-surgery before becoming more stable after 36 months.

The LASER study (16) reported that common long-term GI symptoms associated with treatment included early satiety, heartburn, and bloating/cramping; all of which have the potential to negatively impact on food intake (11, 39) and subsequent nutritional status. There were no significant between-group differences in GI symptoms in this study, with all subgroups experiencing similar levels of minor/mild GI discomfort, regardless of the time since treatment. Somewhat similarly, the presentation of these symptoms in the LASER study was persistent across timepoints (1–2 years, 3–4 years, and >5 years), but at least 15% of participants in the LASER study reported experiencing severe GI symptoms. The development of the ES⁴ (Esophagus and Stomach Surgery Symptom Scale) scale (40) included 344 persons with esophagogastic cancer who were 6 months to 5 years post-surgery, of which 107 persons had undergone surgery for esophageal cancer. Most participants in the ES⁴ study reported no symptoms or mild symptoms in terms of abdominal distension, abdominal hypersensitivity, cervico-thoracic symptoms, and diet-induced systemic symptoms (40). The likely presentation of even mild GI symptoms for a prolonged period post-surgery highlights the need to monitor nutritional status over time (41, 42) and manage survivors’ expectations of their recovery.

Malnutrition is associated with involuntary losses of fat and lean tissue (38) and an increased risk of sarcopenia, a multifactorial syndrome linked with compromised functional performance (8). Although no participant in this study had underweight, half of participants had overweight or obesity, and it is known that excess adiposity can mask lean tissue losses (8, 43). The incidence of sarcopenic obesity in this patient group is potentially as high as 75% (44) and it has been implicated in adverse health outcomes such as Type 2 Diabetes Mellitus and nonalcoholic fatty liver disease (45). Elevated cardiometabolic risk is also typically present, and this was potentially indicated in this study due to most participants having waist circumferences categorized as either high or very high risk. Exercise and nutrition interventions (41, 46, 47) have the potential to improve long-term markers of cardiovascular and metabolic health, with in-person (9, 47) and telehealth (41) approaches deemed acceptable in the literature. Telehealth approaches may be particularly valuable in providing long-term rehabilitative support across a wider geographic area, and their long-term feasibility warrants further exploration.

Nutrition-related recommendations for secondary cancer prevention include adequate amounts of wholegrains, vegetables, and fruits, limited amounts of red and processed meats, and limited amounts of refined and convenience foods (19). International recommendations for fiber range between 25 and 30 g per day (26), and at 17 g/d in this study, intakes were lower than recommendations and the national average of 19 g (48). Relatedly, suboptimal intakes of fruits and vegetables were also evident, with a median of 3.7 portions/d consumed, compared to the national recommendation of 5–7 portions/d (24). That said, average intakes of fruits and vegetables were higher in this study compared to the average national intake of 2.9 portions/d (49). Meat and meat products were consumed regularly by almost all participants. A median of 120 g/d cooked meat and meat products was consumed, exceeding national recommendations (24) and the average national intake of approximately 70 g/d (50). With discomfiting GI symptoms, meeting requirements for fiber, vegetables, and fruits is challenging, and when appetites are poor, displacing these with nutritionally dense alternatives such as meat and dairy is common. However, given the importance of fiber, vegetables, and fruits in reducing the risk of cardiovascular disease and cancer (51), and improving day-to-day function (52), it is important that survivors are supported by qualified professionals, such as dietitians, to adopt health-promoting eating behaviors that optimize their long-term wellbeing.

The strengths and limitations of this work are acknowledged. Participants were identified through a high-volume national center for esophagogastric cancer treatment and include only those with no evidence of disease progression at the time of data collection. The modest sample size reflects the challenges of long-term disease-free follow-up in this cohort and is comparable to other studies in this area (8, 9, 37, 39). The measures of physical function and dietary habits may be confounded by the overall and sub-group sample sizes, and as such, results must be interpreted with caution. Causal inferences cannot be made due to the observational study design. Validated instruments were used to collect data on nutritional intakes (22, 23), malnutrition status (28), and GI symptoms (32), and this is a strength of the study. Obtaining accurate assessments of nutritional intake is challenging, particularly in smaller cohorts where measurement error is more difficult to overcome (53), and this must be considered in interpreting the data. Future research should employ validated instruments to assess dietary intake on a larger cohort at regular intervals to provide more nuanced insights into the trajectory of dietary change post-surgery.

As rates of long-term survivorship continue to increase, it is essential that those recovering from esophagogastric cancer are supported to implement and maintain behaviors that enhance the quality of their survival and reduce secondary cancer risk. This study indicates that many opportunities remain for the development of health-promoting interventions in the rehabilitation of this cohort, and that further research on the long-term health needs of this group is warranted.

Author Contributions

JH, EMG, SLD, LON, JOS, and JVR contributed to the conception and design of the study. AEB, SLD, EMG, and LON contributed to the analysis and interpretation of the data. AEB drafted the manuscript. AEB, SLD, EMG, and LON critically revised the manuscript for intellectual content. All authors were involved in the final approval of the version of the manuscript to be published. All authors agree to be accountable for all aspects of the work.

Ethical Approval

Ethical approval was granted by the St James’ Hospital/Tallaght Hospital Joint Research Ethics Committee.

Acknowledgements

The authors acknowledge the assistance and support of the Wellcome Trust/HRB Clinical Research Facility at St James’ Hospital in providing a dedicated environment for the conduct of high-quality clinical research activities.

Disclosure Statement

No potential conflict of interest was reported by the authors.

Data Availability Statement

The data that support the findings of this study are available from the corresponding author, [AEB], upon reasonable request.

Additional information

Funding

This work was supported by the Health Research Board under grant HRA-POR-2014-535.