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What are the late effects of older gastric cancer survivors? A scoping review

Open AccessPublished:July 04, 2022DOI:https://doi.org/10.1016/j.apjon.2022.100113

      Abstract

      Objective

      Older gastric cancer survivors account for a high proportion of cancer survivors. To improve their quality of life, a cancer survivorship care plan with a consideration of the late effects is required. This study aimed to understand the extent and type of evidence in relation to the late effects in older gastric cancer survivors.

      Methods

      We conducted a scoping review based on the JBI scoping review framework. We explored articles in the Cumulative Index to Nursing and Allied Health Literature (CINAHL), Medical Literature Analysis and Retrieval System Online (MEDLINE), SCOPUS, Web of science, Excerpta Medica dataBASE (EMBASE), Research InformationSharing Service (RISS), Korean Medical dataBASE(KMBase), and National Digital Science Library (NDSL) databases published from January 1, 2012, to December 31, 2021. The keywords used for search are “gastric cancer”, “aged”, “survivors”, and “late effect or long-term effect or late symptom or time factors”. While 439 records were initially identified, 14 articles were eventually selected based on the inclusion criteria.

      Results

      Most studies were conducted in 2019 (4 studies, 28.6%), and more than half (8 studies, 57.1%) were conducted in Asia. In total, six definitions of cancer survivors were found in the studies. The most common age range in the studies was 60–64 years (7 studies, 50.0%). The second primary cancer risk was the most common late effects (5 studies, 20.8%). Among 14 studies, there was only one study of intervention study (7.1%).

      Conclusions

      It is time to shift the focus from survival to care that improve the quality of life after treatment. We suggest future studies to define cancer survivors, set the age criteria and characterize the late effects in older gastric cancer survivors.

      Keywords

      Gastric cancer is one of the most prevalent cancer types. In 2020,
      National Cancer Center Japan
      Cancer Statistics in Japan ’22.
      it ranked fifth in incidence and fourth in mortality, worldwide. Furthermore, East Asian countries such as China, Japan, and Korea have high incidence and mortality rates.
      National Cancer Center Japan
      Cancer Statistics in Japan ’22.
      • Sung H.
      • Ferlay J.
      • Siegel R.L.
      • et al.
      Global cancer statistics 2020: GLOBOCAN estimates of incidence and mortality worldwide for 36 cancers in 185 countries.
      • Zeng H.
      • Chen W.
      • Zheng R.
      • et al.
      Changing cancer survival in China during 2003-15: a pooled analysis of 17 population-based cancer registries.
      In addition, the older population is more vulnerable as the incidence and mortality rates of gastric cancer increase progressively with age.
      National Cancer Center Japan
      Cancer Statistics in Japan ’22.
      ,
      • Lyons K.
      • Le L.C.
      • Pham Y.T.-H.
      • et al.
      Gastric cancer: epidemiology, biology, and prevention: a mini review.
      • Thrift A.P.
      • El-Serag H.B.
      Burden of gastric cancer.
      Meanwhile, due to advances in early detection, surgical techniques, and targeted therapies in the past decade, mortality in gastric cancer has remained low compared to other cancer types.
      • Siegel R.L.
      • Miller K.D.
      • Fuchs H.E.
      • Jemal A.
      Cancer statistics.
      In China, one of the countries with a high incidence of gastric cancer, a significant increase in survival rates for gastric cancer over the last 10 years has been recorded.
      • Zeng H.
      • Chen W.
      • Zheng R.
      • et al.
      Changing cancer survival in China during 2003-15: a pooled analysis of 17 population-based cancer registries.
      Moreover, in Japan, the 5-year relative survival rates for gastric cancer were slightly higher than for other cancers.
      National Cancer Center Japan
      Cancer Statistics in Japan ’22.
      This trend is even more prominent in Korea; among gastric cancer survivors, the proportion of those over 65 is 49.4%.
      Ministry of Health and Welfare, Korea Central Cancer Registry, National Cancer Center
      Annual Report of Cancer Statistics in Korea in 2018.
      Several definitions of a cancer survivor have been proposed; over time, it has evolved to include the entire cancer trajectory, from diagnosis to completion of active treatment and long-term survival.
      • American Cancer Society
      Cancer Treatment & Survivorship Facts & Figures 2019-2021.
      Cancer survivors are defined as patients with cancer who have completed active treatment
      • ASCO
      Long-term side effects of cancer treatment.
      or those who have lived five years after the initial diagnosis and completed active treatment.
      • National Cancer Institute
      Late effects of cancer treatment.
      Institute of Medicine defines a cancer survivor as a patient with cancer who does not require hospice or palliative care after the completion of active treatment and before the diagnosis of new cancer.
      • Institute of Medicine, National Research Council
      From Cancer Patient to Cancer Survivor: Lost in Transition.
      Therefore, it is expected that understanding which criteria were mainly applied when defining gastric cancer survivors will help optimize care.
      Cancer survivors often report distressing symptoms that appear months or years after treatment. Late effects are chronic disorders resulting from cancer treatment that cause physical and psychological problems, including secondary cancer.
      • National Cancer Institute
      Late effects of cancer treatment.
      Late effects have been reported for all cancer types and commonly include the risk of a second primary cancer, anxiety, depression, trauma, cardiovascular disease risk, cognitive dysfunction, employment and return to work, pain, and sexual dysfunction.
      • NCCN
      NCCN Guidelines-General Survivorship.
      One study on symptom burden of cancer survivors reported that they suffered from late effects even more than 10 years after the termination of primary cancer treatment.
      • Harrington C.B.
      • Hansen J.A.
      • Moskowitz M.
      • Todd B.L.
      • Feuerstein M.
      It's not over when it's over: long-term symptoms in cancer survivors—a systematic review.
      Wu reported that about a third of cancer survivors experience symptom burden due to late effects, which has a significant impact on their quality of life (QOL) and is related to disability and health care use. Depending on the diagnosis or time since diagnosis, the most prevalent concerns differ among the physical, social, spiritual, emotional domains, and other symptoms also vary.
      • Sheryl Ness R.
      • Janine Kokal R.
      • Fee-Schroeder K.
      • Novotny P.
      • Satele D.
      • Debra Barton R.
      Concerns across the survivorship trajectory: results from a survey of cancer survivors.
      Therefore, identification and management of the various late and long-term effects is a crucial aspect of cancer survivors’ care plan.
      • ASCO
      Long-term side effects of cancer treatment.
      ,
      • McCabe M.S.
      • Faithfull S.
      • Makin W.
      • Wengstrom Y.
      Survivorship programs and care planning.
      In particular, gastric cancer survivors have reported late effects such as weight loss, diarrhea, chemotherapy-induced neuropathy, fatigue, bone health, indigestion, vitamin B12 deficiency, iron deficiency, postprandial fullness or eating dysfunction, dumping syndrome, and small intestine bacterial overgrowth.
      • NCCN N.C.C.N.
      guidelines-gastric cancer.
      Previous studies have also reported other late effects in gastric cancer survivors including secondary new cancer,
      • Thrift A.P.
      • El-Serag H.B.
      Burden of gastric cancer.
      survival rate,
      • Jin Won L.
      • Ali B.
      • Han Mo Y.
      • et al.
      Conditional survival analysis in Korean patients with gastric cancer undergoing curative gastrectomy.
      • Kadowaki S.
      • Komori A.
      • Narita Y.
      • et al.
      Long-term outcomes and prognostic factors of patients with advanced gastric cancer treated with S-1 plus cisplatin combination chemotherapy as a first-line treatment.
      • Hochwald S.N.
      • Kim S.
      • Klimstra D.S.
      • Brennan M.F.
      • Karpeb M.S.
      Analysis of 154 actual five-year survivors of gastric cancer.
      • Yuri I.
      • Tomio N.
      • Isao M.
      • et al.
      Conditional survival for longer-term survivors from 2000-2004 using population-based cancer registry data in Osaka, Japan.
      vitamin D deficiency,
      • Li Z.
      • Shi J.
      • Wang Z.
      • Chen H.
      • Liu Y.
      Nutrient status of vitamin D among cancer patients.
      and osteopathy
      • Leach J.
      Osteopathic support for a survivor of gastric cancer: a case report.
      associated with gastrectomy. Although many studies have examined the characteristics and burden of late effects,
      • Duijts S.F.
      • Van Egmond M.P.
      • Spelten E.
      • Van Muijen P.
      • Anema J.R.
      • van der Beek A.J.
      Physical and psychosocial problems in cancer survivors beyond return to work: a systematic review.
      • Lee J.A.
      • Kim S.Y.
      • Kim Y.
      • et al.
      Comparison of health-related quality of life between cancer survivors treated in designated cancer centers and the general public in Korea.
      • Seiler A.
      • Klaas V.
      • Tröster G.
      • Fagundes C.P.
      eHealth and mHealth interventions in the treatment of fatigued cancer survivors: a systematic review and meta-analysis.
      studies on late effects specifically experienced by older gastric cancer survivors, who account for a large proportion of cancer survivors, are sparse.
      A scoping review is one of the most recently used methodologies for the preliminary assessment of potential size and scope of available research literature.
      • Daudt H.M.L.
      • van Mossel C.
      • Scott S.J.
      Enhancing the scoping study methodology: a large, inter-professional team's experience with Arksey and O'Malley's framework.
      It involves a mapping of existing literature to identify trends in research conducted in a field of interest.
      • Arksey H.
      • O'Malley L.
      Scoping studies: towards a methodological framework.
      Such mapping can help us establish where we are and could be used to determine the direction we need to go. A scoping review is used as a standalone project or as a preliminary step for a systematic review.
      • Tricco A.C.
      • Lillie E.
      • Zarin W.
      • et al.
      A scoping review on the conduct and reporting of scoping reviews.
      In this study, we designed a scoping review to identify how research on the late effects in older gastric cancer survivors has been conducted to provide fundamental and comprehensive understanding of the current research trends of the same.
      This study aimed to understand the extent and type of evidence related to the late effects in older gastric cancer survivors over the past decade. The research objectives are as follows: (1) identify the recent research trends; (2) describe the characteristics of the study participants; (3) demonstrate the types of confirmed late effects; (4) explore the interventions used in previous studies, if applicable. With this scoping review, we expect to suggest appropriate interventions and research domains to future researchers for the further study of late effects in older gastric cancer survivors and to consequently improve their health-related QOL.

      Methods

      Study design and research questions

      We conducted this scoping review in accordance with the JBI scoping review framework.
      • Peters MDJ G.C.
      • McInerney P.
      • Munn Z.
      • Tricco A.C.
      • Khalil H.
      [Chapter 11]: scoping reviews (2020 version).
      We aimed to answer the following research questions in order to identify the characteristics of late effects in older gastric cancer survivors:
      • (1)
        How have studies on late effects been conducted in older gastric cancer survivors over the past decade?
      • (2)
        What are the characteristics of the study participants?
      • (3)
        What symptoms and variables have been identified as late effects?
      • (4)
        What interventions have been implemented to manage late effects?

      Search strategy

      We searched for relevant studies using the following four search concepts “gastric cancer”, “aged”, “survivors”, and “late effect or long-term effect or late symptom or time factors”, in conjunction with Boolean operators, proximity locators, and MeSH terms in the following databases: Cumulative Index to Nursing and Allied Health Literature (CINAHL), Medical Literature Analysis and Retrieval System Online (MEDLINE), SCOPUS, Web of Science, Excerpta Medica dataBASE (EMBASE), Research information sharing service (RISS), Koreamed, Korean medical database (KMBase), and National digital science library (NDSL). As subject headings varied in the databases, the modification of terms was repeated in each database. Research papers published included those in English and Korean in the last 10 years between January 1, 2012 and December 31, 2021.

      Selection of evidence sources

      We identified 439 studies from our search of the above-mentioned databases. Duplicates were removed, and 194 research papers were extracted. In the primary screening process, two researchers independently reviewed titles and abstracts with keywords. Researchers excluded 59 papers and selected 135 studies. In the second screening process, two researchers independently reviewed the full text and selected the papers based on the pre-established selection criteria. The inclusion criteria were as follows: (1) studies presenting results related to the elderly or with participants aged 60 years or older; (2) participants primarily diagnosed with gastric cancer; (3) participants’ completion of active cancer treatment and being under observation; (4) description of late effects in general cancer survivors as provided by Survivorship version 1, 2021 NCCN guidelines
      • Tevaarwerk A.
      • Denlinger C.S.
      • Sanft T.
      • et al.
      Survivorship, version 1.2021.
      or as stated by the NCCN guidelines-gastric cancer, 2022
      • NCCN N.C.C.N.
      guidelines-gastric cancer.
      ; (5) study types such as systematic review, descriptive study of late effects, experimental study of interventions for late effects, clinical trial studies of late effects, protocol, review, letter, and gray literature. The exclusion criteria were studies that (1) cover only survival rate, mortality, and recurrence rates without exploring the symptoms experienced by the participants; (2) describe the effects of recurrent gastric cancer after treatment according to the type of treatment; (3) include gastric cancer patients undergoing active treatment; (4) do not present the characteristics of gastric cancer survivors over 60 years of age separately; (5) do not have the primary cancer diagnosis as gastric cancer; (6) examined esophagogastric junction cancer and gastrointestinal stromal tumor; (7) do not include the full text; or (8) do not include gastric cancer survivors or are not able to distinguish gastric cancer survivors from other cancer types.
      The differences of opinions were resolved through a consensus process within the research team by a third researcher. Finally, 14 papers were selected (Fig. 1).
      Fig. 1
      Fig. 1PRISMA, flow diagram of study selection process.

      Data-charting process and analysis

      The following data on general information of the selected studies and on the aforementioned four research questions were collated using Microsoft Excel 2020.
      • (1)
        General information: Research author, publication year, title, digital object identifier, research purpose, research design, research country, population, number of the study participants, and age of the population.
      • (2)
        Information related to the study questions: measurement of late effect, outcome, and summary of study results.
      The collected data were encoded and analyzed using descriptive statistics, such as frequency and percentage, on Microsoft Excel 2020.

      Results

      Research trends on older cancer survivors with gastric cancer in the last decade

      Table 1 shows the characteristics of studies targeting older gastric cancer survivors. Since 2018, studies have been published at a steady rate. Most of them were performed in 2019 (4 studies, 28.6%).
      • Choi Y.J.
      • Shin D.W.
      • Jang W.
      • et al.
      Risk of dementia in gastric cancer survivors who underwent gastrectomy: a nationwide study in Korea.
      • Iki M.
      • Fujita Y.
      • Kouda K.
      • et al.
      Increased risk of osteoporotic fracture in community-dwelling elderly men 20 or more years after gastrectomy: the Fujiwara-Kyo Osteoporosis Risk in Men (FORMEN) Cohort Study.
      • Morais S.
      • Castro C.
      • Antunes L.
      • Peleteiro B.
      • Bento M.J.
      • Lunet N.
      Second primary cancers and survival in patients with gastric cancer: association with prediagnosis lifestyles.
      • Morton L.M.
      • Dores G.M.
      • Schonfeld S.J.
      • et al.
      Association of chemotherapy for solid tumors with development of therapy-related myelodysplastic syndrome or acute myeloid leukemia in the modern era.
      After 2019, four studies (28.6%) investigated late effects related to gastrectomy (risk of dementia,
      • Choi Y.J.
      • Shin D.W.
      • Jang W.
      • et al.
      Risk of dementia in gastric cancer survivors who underwent gastrectomy: a nationwide study in Korea.
      osteoporotic fractures,
      • Iki M.
      • Fujita Y.
      • Kouda K.
      • et al.
      Increased risk of osteoporotic fracture in community-dwelling elderly men 20 or more years after gastrectomy: the Fujiwara-Kyo Osteoporosis Risk in Men (FORMEN) Cohort Study.
      nutrition status,
      • Gharagozlian S.
      • Mala T.
      • Brekke H.K.
      • Kolbjørnsen L.C.
      • Ullerud Å.A.
      • Johnson E.
      Nutritional status, sarcopenia, gastrointestinal symptoms and quality of life after gastrectomy for cancer – a cross-sectional pilot study.
      sarcopenia,
      • Gharagozlian S.
      • Mala T.
      • Brekke H.K.
      • Kolbjørnsen L.C.
      • Ullerud Å.A.
      • Johnson E.
      Nutritional status, sarcopenia, gastrointestinal symptoms and quality of life after gastrectomy for cancer – a cross-sectional pilot study.
      gastrointestinal symptoms,
      • Gharagozlian S.
      • Mala T.
      • Brekke H.K.
      • Kolbjørnsen L.C.
      • Ullerud Å.A.
      • Johnson E.
      Nutritional status, sarcopenia, gastrointestinal symptoms and quality of life after gastrectomy for cancer – a cross-sectional pilot study.
      QOL,
      • Gharagozlian S.
      • Mala T.
      • Brekke H.K.
      • Kolbjørnsen L.C.
      • Ullerud Å.A.
      • Johnson E.
      Nutritional status, sarcopenia, gastrointestinal symptoms and quality of life after gastrectomy for cancer – a cross-sectional pilot study.
      presence of Enterobacteriaceae
      • Horvath A.
      • Bausys A.
      • Sabaliauskaite R.
      • et al.
      Distal gastrectomy with Billroth II reconstruction is associated with oralization of gut microbiome and intestinal inflammation: a proof-of-concept study.
      ) and four studies (28.6%) performed secondary cancer studies.
      • Morais S.
      • Castro C.
      • Antunes L.
      • Peleteiro B.
      • Bento M.J.
      • Lunet N.
      Second primary cancers and survival in patients with gastric cancer: association with prediagnosis lifestyles.
      ,
      • Morton L.M.
      • Dores G.M.
      • Schonfeld S.J.
      • et al.
      Association of chemotherapy for solid tumors with development of therapy-related myelodysplastic syndrome or acute myeloid leukemia in the modern era.
      ,
      • Amikura K.
      • Ehara K.
      • Kawashima Y.
      The risk of developing multiple primary cancers among long-term survivors five years or more after stomach carcinoma resection.
      ,
      • Schonfeld S.J.
      • Morton L.M.
      • de González A.B.
      • Curtis R.E.
      • Kitahara C.M.
      Risk of second primary papillary thyroid cancer among adult cancer survivors in the United States, 2000-2015.
      More than half studies (8 studies, 57.1%) were conducted in Asian countries, including Korea
      • Choi Y.J.
      • Shin D.W.
      • Jang W.
      • et al.
      Risk of dementia in gastric cancer survivors who underwent gastrectomy: a nationwide study in Korea.
      ,
      • Jun J.H.
      • Yoo J.E.
      • Lee J.A.
      • et al.
      Anemia after gastrectomy in long-term survivors of gastric cancer: a retrospective cohort study.
      • Hu Y.
      • Kim H.I.
      • Hyung W.J.
      • et al.
      Vitamin B12 deficiency after gastrectomy for gastric cancer: an analysis of clinical patterns and risk factors.
      • Lee S.S.
      • Chung H.Y.
      • Kwon O.K.
      • Yu W.
      Long-term quality of life after distal subtotal and total gastrectomy: symptom- and behavior-oriented consequences.
      • Lee J.E.
      • Shin D.W.
      • Lee H.
      • et al.
      One-year experience managing a cancer survivorship clinic using a shared-care model for gastric cancer survivors in Korea.
      and Japan.
      • Iki M.
      • Fujita Y.
      • Kouda K.
      • et al.
      Increased risk of osteoporotic fracture in community-dwelling elderly men 20 or more years after gastrectomy: the Fujiwara-Kyo Osteoporosis Risk in Men (FORMEN) Cohort Study.
      ,
      • Horvath A.
      • Bausys A.
      • Sabaliauskaite R.
      • et al.
      Distal gastrectomy with Billroth II reconstruction is associated with oralization of gut microbiome and intestinal inflammation: a proof-of-concept study.
      ,
      • Amikura K.
      • Ehara K.
      • Kawashima Y.
      The risk of developing multiple primary cancers among long-term survivors five years or more after stomach carcinoma resection.
      Prospective studies (8 studies, 57.1%) were mainly performed. Among the prospective studies, more than half studies (7 studies, 50.0%)
      • Iki M.
      • Fujita Y.
      • Kouda K.
      • et al.
      Increased risk of osteoporotic fracture in community-dwelling elderly men 20 or more years after gastrectomy: the Fujiwara-Kyo Osteoporosis Risk in Men (FORMEN) Cohort Study.
      ,
      • Morais S.
      • Castro C.
      • Antunes L.
      • Peleteiro B.
      • Bento M.J.
      • Lunet N.
      Second primary cancers and survival in patients with gastric cancer: association with prediagnosis lifestyles.
      ,
      • Gharagozlian S.
      • Mala T.
      • Brekke H.K.
      • Kolbjørnsen L.C.
      • Ullerud Å.A.
      • Johnson E.
      Nutritional status, sarcopenia, gastrointestinal symptoms and quality of life after gastrectomy for cancer – a cross-sectional pilot study.
      ,
      • Horvath A.
      • Bausys A.
      • Sabaliauskaite R.
      • et al.
      Distal gastrectomy with Billroth II reconstruction is associated with oralization of gut microbiome and intestinal inflammation: a proof-of-concept study.
      ,
      • Lee S.S.
      • Chung H.Y.
      • Kwon O.K.
      • Yu W.
      Long-term quality of life after distal subtotal and total gastrectomy: symptom- and behavior-oriented consequences.
      • Lee J.E.
      • Shin D.W.
      • Lee H.
      • et al.
      One-year experience managing a cancer survivorship clinic using a shared-care model for gastric cancer survivors in Korea.
      • Climent M.
      • Pera M.
      • Aymar I.
      • Ramón J.M.
      • Grande L.
      • Nogués X.
      Bone health in long-term gastric cancer survivors: a prospective study of high-dose vitamin D supplementation using an easy administration scheme.
      were prospective observational studies, while one was interventional study (7.1%).
      • Climent M.
      • Pera M.
      • Aymar I.
      • Ramón J.M.
      • Grande L.
      • Nogués X.
      Bone health in long-term gastric cancer survivors: a prospective study of high-dose vitamin D supplementation using an easy administration scheme.
      Retrospective studies were conducted using big data from hospitals or countries. Most studies focused on the risk of second primary cancer (4 studies, 23.5%),
      • Morais S.
      • Castro C.
      • Antunes L.
      • Peleteiro B.
      • Bento M.J.
      • Lunet N.
      Second primary cancers and survival in patients with gastric cancer: association with prediagnosis lifestyles.
      ,
      • Morton L.M.
      • Dores G.M.
      • Schonfeld S.J.
      • et al.
      Association of chemotherapy for solid tumors with development of therapy-related myelodysplastic syndrome or acute myeloid leukemia in the modern era.
      ,
      • Amikura K.
      • Ehara K.
      • Kawashima Y.
      The risk of developing multiple primary cancers among long-term survivors five years or more after stomach carcinoma resection.
      ,
      • Schonfeld S.J.
      • Morton L.M.
      • de González A.B.
      • Curtis R.E.
      • Kitahara C.M.
      Risk of second primary papillary thyroid cancer among adult cancer survivors in the United States, 2000-2015.
      followed by psychosocial symptoms such as QOL (2 studies, 11.8%),
      • Gharagozlian S.
      • Mala T.
      • Brekke H.K.
      • Kolbjørnsen L.C.
      • Ullerud Å.A.
      • Johnson E.
      Nutritional status, sarcopenia, gastrointestinal symptoms and quality of life after gastrectomy for cancer – a cross-sectional pilot study.
      ,
      • Lee S.S.
      • Chung H.Y.
      • Kwon O.K.
      • Yu W.
      Long-term quality of life after distal subtotal and total gastrectomy: symptom- and behavior-oriented consequences.
      and healthy behavior (2 studies, 11.8%).
      • Gharagozlian S.
      • Mala T.
      • Brekke H.K.
      • Kolbjørnsen L.C.
      • Ullerud Å.A.
      • Johnson E.
      Nutritional status, sarcopenia, gastrointestinal symptoms and quality of life after gastrectomy for cancer – a cross-sectional pilot study.
      ,
      • Lee S.S.
      • Chung H.Y.
      • Kwon O.K.
      • Yu W.
      Long-term quality of life after distal subtotal and total gastrectomy: symptom- and behavior-oriented consequences.
      Studies on specific physical symptoms such as anemia,
      • Jun J.H.
      • Yoo J.E.
      • Lee J.A.
      • et al.
      Anemia after gastrectomy in long-term survivors of gastric cancer: a retrospective cohort study.
      bone metabolism,
      • Iki M.
      • Fujita Y.
      • Kouda K.
      • et al.
      Increased risk of osteoporotic fracture in community-dwelling elderly men 20 or more years after gastrectomy: the Fujiwara-Kyo Osteoporosis Risk in Men (FORMEN) Cohort Study.
      ,
      • Lee J.E.
      • Shin D.W.
      • Lee H.
      • et al.
      One-year experience managing a cancer survivorship clinic using a shared-care model for gastric cancer survivors in Korea.
      ,
      • Climent M.
      • Pera M.
      • Aymar I.
      • Ramón J.M.
      • Grande L.
      • Nogués X.
      Bone health in long-term gastric cancer survivors: a prospective study of high-dose vitamin D supplementation using an easy administration scheme.
      gastrointestinal symptoms,
      • Lee S.S.
      • Chung H.Y.
      • Kwon O.K.
      • Yu W.
      Long-term quality of life after distal subtotal and total gastrectomy: symptom- and behavior-oriented consequences.
      intestinal bacterial,
      • Horvath A.
      • Bausys A.
      • Sabaliauskaite R.
      • et al.
      Distal gastrectomy with Billroth II reconstruction is associated with oralization of gut microbiome and intestinal inflammation: a proof-of-concept study.
      vitamin B12 deficiency,
      • Choi Y.J.
      • Shin D.W.
      • Jang W.
      • et al.
      Risk of dementia in gastric cancer survivors who underwent gastrectomy: a nationwide study in Korea.
      ,
      • Hu Y.
      • Kim H.I.
      • Hyung W.J.
      • et al.
      Vitamin B12 deficiency after gastrectomy for gastric cancer: an analysis of clinical patterns and risk factors.
      and nutritional status
      • Gharagozlian S.
      • Mala T.
      • Brekke H.K.
      • Kolbjørnsen L.C.
      • Ullerud Å.A.
      • Johnson E.
      Nutritional status, sarcopenia, gastrointestinal symptoms and quality of life after gastrectomy for cancer – a cross-sectional pilot study.
      in gastric cancer survivors were also performed. Other research aimed at exploring the risk of dementia (1 study, 5.9%)
      • Choi Y.J.
      • Shin D.W.
      • Jang W.
      • et al.
      Risk of dementia in gastric cancer survivors who underwent gastrectomy: a nationwide study in Korea.
      and renal function after radiochemotherapy (1 study, 5.9%).
      • Haneder S.
      • Budjan J.M.
      • Schoenberg S.O.
      • et al.
      Dose-dependent changes in renal (1)H-/(23)Na MRI after adjuvant radiochemotherapy for gastric cancer.
      Table 1Characteristics and summary of studies on late effects in older gastric cancer survivors.
      Reference; first author; date published; countryAim of the studyMethodology: study design, data analysisSample size (total or older/total)Participant characteristicsMean age ± SD (years old) (total or older/total)Outcomes and measuresKey findings related to older gastric cancer survivorsLate effects from key findings based on NCCN guidelines
      Hu Y, 2013
      • Hu Y.
      • Kim H.I.
      • Hyung W.J.
      • et al.
      Vitamin B12 deficiency after gastrectomy for gastric cancer: an analysis of clinical patterns and risk factors.


      Republic of Korea
      Identification of risk factors for vitamin B12 deficiency and changes in vitamin B12 over time post gastrectomyProspective observational study, the Kaplan–Meier method, Cox proportional hazards model184/645Gastric cancer patients who underwent STG or TG61.0 ​± ​11.0/58.5 ​± ​12.2Cumulative vitamin B12 deficiency after surgeryMean time from surgery was 24 months (range: 3–72 months).

      Risk factors for vitamin B12 deficiency in gastric cancer survivors include age during STGa and preoperative vitamin B12 level. Patients with vitamin B12 deficiency had an average age of 60 years or older.
      Vitamin B12 deficiency
      Haneder S, 2015
      • Haneder S.
      • Budjan J.M.
      • Schoenberg S.O.
      • et al.
      Dose-dependent changes in renal (1)H-/(23)Na MRI after adjuvant radiochemotherapy for gastric cancer.


      Germany
      Evaluating renal function in long-term gastric cancer survivors receiving combined radiochemotherapyRetrospective study

      Univariate analysis of variance

      Linear correlations
      1/18Patients after chemoradiotherapy

      105 months passed since last treatment.
      63.0/52.1 (range: 24–69,

      No information of SD)
      3T functional MRIc including DWId,23Na imaging

      Late toxicity: CTCe questionnaire, creatinine values
      Radiation therapy for gastric cancer causes kidney damage.Renal dysfunction
      Lee JE, 2016
      • Lee J.E.
      • Shin D.W.
      • Lee H.
      • et al.
      One-year experience managing a cancer survivorship clinic using a shared-care model for gastric cancer survivors in Korea.


      Republic of Korea
      Describing the health care status of gastric cancer survivors and reporting the experience of using the shared-care model during a one-year experience at the cancer survivorship clinicProspective observational study250Patients with gastric cancer. 3 years post surgery62 (range: 36–85

      No information of SD)
      Health behaviors, comorbid conditions, secondary cancer screenings, survivorship care status (bone density, vaccinations)Among the survivors, 7.2% were current smokers, 8.8% were at-risk drinkers, and 32.4% were physically inactive. Among the patients who did not know their bone density status, the majority were in the osteopenic (37.1%) or osteoporotic range (24.1%). Screening among the eligible population within the recommended time intervals were 76.3% for colorectal cancer, but only 13.6% for lung cancer.Bone health, screening new primary cancer, cardiovascular disease risk, healthy lifestyle, vaccination
      Jun JH, 2016
      • Jun J.H.
      • Yoo J.E.
      • Lee J.A.
      • et al.
      Anemia after gastrectomy in long-term survivors of gastric cancer: a retrospective cohort study.


      Republic of Korea
      Exploring the incidence and risk factors of anemia in long-term gastric cancer survivorsRetrospective cohort study Kaplan–Meier survival analysis

      Cox regression analysis
      106/385Gastric cancer patients who survived more than 5 years after gastrectomyNo information

      /53.21 ​± ​9.77
      The cumulative incidence rate of anemia after surgeryThe incidence of anemia steadily increased in patients who had underwent gastrectomy. The 5-year cumulative incidence of anemia was almost 40%. The risk of anemia was higher in women and in patients with TGb, diabetes, and low body mass index. There was no significant increased risk of anemia with age.Iron deficiency
      Lee SS, 2016
      • Lee S.S.
      • Chung H.Y.
      • Kwon O.K.
      • Yu W.
      Long-term quality of life after distal subtotal and total gastrectomy: symptom- and behavior-oriented consequences.


      Republic of Korea
      Assessment of long-term QOL 5 years after STG and TG by comparing groups matched by a set of patient factors at and beyond postoperative 5 yearsProspective observational study5-year survivors after STG and TG: 53 pairs

      Long-term survivors after STG and TG (> 5 years): 36 pairs
      Gastric cancer survivors of more than 5 years after surgery5-year survivors: STG: 61.0 ​± ​8.3

      TG: 61.0 ​± ​8.3

      Long-term survivors (> 5 ​years)

      STG: 62.3 ​± ​10.7

      TG: 62.3 ​± ​10.2
      QLQf -C30

      QLQf -STO22
      Five-year survivors after TGb showed significantly worse QOLg in social functioning, nausea and vomiting, eating restrictions, and taste. For long-term survivors, QOLg inferiority of the TGb group was observed only in eating restrictions. Among 4 items constituting eating restrictions, the TGb group tended to exhibit worse QOLg in 2 items (enjoyable meals and social meals).Employment and return symptoms, healthy lifestyle, nausea and vomiting, postprandial fullness or eating dysfunction
      Climent M, 2018
      • Climent M.
      • Pera M.
      • Aymar I.
      • Ramón J.M.
      • Grande L.
      • Nogués X.
      Bone health in long-term gastric cancer survivors: a prospective study of high-dose vitamin D supplementation using an easy administration scheme.


      Spain
      Investigating bone health after curative resection of gastric cancer and the consequences of high-dose vitamin D supplementation in patients with low levels of 25-(OH)-vitamin DProspective, non-selected, observational, clinical cohort study40Disease-free patients at least 24 months after gastrectomy68.9 ​± ​11.725-(OH)-vitamin D iPTHMean time from surgery was 48.9 (range: 24–109) months.

      Vitamin D insufficiency, secondary hyperparathyroidism, osteoporosis, and prevalent fractures were observed at baseline. Vitamin D supplementation led to reaching 25-(OH)-vitamin D values above 30 ​ng/mL and helped reduce iPTH levels and markers of bone turnover.
      Bone health
      Morton LM, 2019
      • Morton L.M.
      • Dores G.M.
      • Schonfeld S.J.
      • et al.
      Association of chemotherapy for solid tumors with development of therapy-related myelodysplastic syndrome or acute myeloid leukemia in the modern era.


      US
      Quantification of tMDS/AML risk among adults who were diagnosed with a first primary solid cancer and correlation tMDS/AML risk patterns with chemotherapy treatment practicesRetrospective population-based cohort study

      Poisson-based relative risk estimation
      10,329

      /32,239
      Patients with first primary solid cancer who survived 1 year or more without developing a second cancer73 (range: 66–84, No information of SD)

      /61
      Second primary tMDS/AMLh

      Patterns of chemotherapy use
      The risk of tMDS/AMLh was higher at <5 years after diagnosis compared to >5 years after diagnosis of gastric cancer. SIRis were higher among patients who received initial chemoradiotherapy than those with chemotherapy alone for gastric cancers. The EARj of tMDS/AMLh for gastric cancer was significantly higher in the age group 65 years or older [SPCk SIRi 2.0(95% CIl: 1.2–3.3), EARj 5.8] than in the age group 50–64 years [SPCk SIRi4.1(95% CIl: 20.-7.2), EAR5.2].Screening new primary cancer
      Choi YJ, 2019
      • Choi Y.J.
      • Shin D.W.
      • Jang W.
      • et al.
      Risk of dementia in gastric cancer survivors who underwent gastrectomy: a nationwide study in Korea.


      Republic of Korea
      Comparing the risk of dementia, including AD and VaD, between gastric cancer patients who underwent gastrectomy and the general populationRetrospective study

      Cox regression analysis
      63,998

      /267,274
      Patients with gastric cancer who underwent gastrectomy for more than 2 years and are over 50 years of age63.3 ​± ​8.1

      /63.2 ​± ​8.1
      Incidence of ADs and VaDtGastric cancer patients who underwent gastrectomy had increased risk of ADs [adjusted HRr 1.08, 95% CIl 1.03–1.14]. The risk of ADs was especially marked for those who received a total gastrectomy [adjusted HRr 1.39, 95% CIl 1.25–1.54]. VaDt risk was not high in gastric cancer patients [adjusted HRr 0.85, 95% CIl 0.73–0.98].Vit B12 deficiency, cognitive function
      Iki M, 2019
      • Iki M.
      • Fujita Y.
      • Kouda K.
      • et al.
      Increased risk of osteoporotic fracture in community-dwelling elderly men 20 or more years after gastrectomy: the Fujiwara-Kyo Osteoporosis Risk in Men (FORMEN) Cohort Study.


      Japan
      Clarification about the association of gastrectomy with aBMD, bone metabolism markers, and fracture risk in community-dwelling elderly Japanese men (aged ≥ 65 years)Prospective cohort study A 5-year longitudinal study

      Cox proportional hazards models
      74

      /1985
      Elderly patient with gastric cancer who underwent gastrectomy74.2 ​± ​5.6

      /73.0 ​± ​5.2
      aBMD at the spine and hip,

      serum levels of intact PTHm, intact OCn, TRACP5bo, ucOCp, OPFsq
      Mean time from surgery was 9.75(±8.3) years. The risk of osteoporotic fractures in men who underwent gastrectomy for gastric cancer was not significant [HRr: 1.94, 95% CIl: 0.60–6.32]. Patients who survived 20 years or more after surgery were at risk of osteoporotic fractures [HRr: 5.38, 95% CIl: 1.43–9.60].Bone health
      Morais S, 2019
      • Morais S.
      • Castro C.
      • Antunes L.
      • Peleteiro B.
      • Bento M.J.
      • Lunet N.
      Second primary cancers and survival in patients with gastric cancer: association with prediagnosis lifestyles.


      Portugal
      Quantification of the association between prediagnosis lifestyles with the risk of SPCs and survival of patients with gastric FPCProspective observational study, case–control study.

      Cox proportional hazards regression analysis
      207

      /574
      Gastric cancer survivors who underwent gastrectomyNo information

      /No information
      Smoking, drinking, BMI, dietary exposures, second primary cancers, mortalitySPCks occurred more often in males than in females [HRr 3.67, 95% CIl 1.26–10.65], and in older patients [55–69 and ​≥ ​70: HRr 9.03, 95% CIl 1.16–70.57 vs. <55 16.39, 2.16–124.43]. Significantly higher HRrs (95% CIl) were found for older patients [55–69 and ​≥70: 1.53 (1.17–2.00) vs. <55: 2.09 (1.61–2.71)]. No statistically significant estimates were observed between smoking or alcohol intake and the occurrence of an SPCk and between smoking or dietary exposures and mortality.Screening new primary cancer
      Gharagozlian S, 2020
      • Gharagozlian S.
      • Mala T.
      • Brekke H.K.
      • Kolbjørnsen L.C.
      • Ullerud Å.A.
      • Johnson E.
      Nutritional status, sarcopenia, gastrointestinal symptoms and quality of life after gastrectomy for cancer – a cross-sectional pilot study.


      Norway
      Assessment of nutritional status, GI-symptoms and QOL 2–5 years after gastrectomy for malignancyProspective observational study21No recurrence among patients with gastric cancer who underwent gastrectomy60.0 ​± ​12.6Nutritional status: SGAw.

      Dietary intake: repeated 24-h dietary recalls

      GSRSx, SF-36
      Mean time from surgery was 28.7(±8.3) months.

      A high prevalence of weight loss and pre-sarcopenia was observed. Malnutrition as assessed by SGAw was associated with more GIv-symptoms (abdominal pain syndrome) and reduced QOLg scores (bodily pain and vitality).
      Weight Loss, pain,

      physical activity
      Schonfeld SJ, 2020
      • Schonfeld S.J.
      • Morton L.M.
      • de González A.B.
      • Curtis R.E.
      • Kitahara C.M.
      Risk of second primary papillary thyroid cancer among adult cancer survivors in the United States, 2000-2015.


      US
      Evaluation of second PTC risk among ≥ 1-year adult survivors of non-thyroid malignancies from US population-based cancer registriesRetrospective study

      SIRs Multivariable Poisson regression models
      35,039/3,175,216Cancer survivors one year after diagnosisMean age at diagnosis:

      63.2 (range: 20–84) No information of SD/61.5 (No information of SD)
      Incidence of second PTCySIRis tended to be higher among patients diagnosed with first primary malignancy at ​< ​50 versus ≥50 years (SIRi 1.9, 95% CIl 1.2–2.7, Phet 0.62).Screening new primary cancer
      Amikura K, 2020
      • Amikura K.
      • Ehara K.
      • Kawashima Y.
      The risk of developing multiple primary cancers among long-term survivors five years or more after stomach carcinoma resection.


      Japan
      Evaluation of MPC and delayed stomach carcinoma recurrence in long-term survivors over 5 years after gastrectomyRetrospective cohort study325/4883Long-term gastric cancer survivors of more than 5 years who underwent gastrectomyMean age at diagnosis of MPC: 72.4 (range: 38–95)/No informationIncidence of MPCz, delayed stomach carcinoma recurrenceIn the elderly patients, 80 years or older, the mortality and the survival rate after MPCz diagnosis were significantly worse than those in younger patients. The onset of MPCz 5 years after surgery was significantly higher in patients over 80 years of age than within 5 years after surgery. Those diagnosed with MPCz within 5 years of surgery were younger than those diagnosed 5 years after surgery.Screening new primary cancer
      Horvath A, 2021
      • Horvath A.
      • Bausys A.
      • Sabaliauskaite R.
      • et al.
      Distal gastrectomy with Billroth II reconstruction is associated with oralization of gut microbiome and intestinal inflammation: a proof-of-concept study.


      Japan
      Investigating whether SGB2 is associated with specific changes in gut microbiome composition and intestinal inflammation.Prospective cross-sectional proof-of-concept study14

      /22
      Patients gastric cancer who underwent gastrectomy and treatment for more than 1 year68 (range: 64–74, No information of SD)

      /No information
      Sequencing from stool sample.

      Lithuanian versions of EORTC QLQ-C30, EORTC QLQ-STO22§
      The most documented GIv symptoms after SGB2 were abdominal discomfort (n ​= ​9; 69%), diarrhea (n ​= ​7; 54%), and bloating (n ​= ​6; 46%). Fecal calprotectin was increased in SGB2 group, and calprotectin levels positively correlated with the abundance of Streptococcus. GIv symptoms in SGB2 patients were associated with distinct taxonomic changes of the gut microbiome.Small intestine bacterial overgrowth,

      GIv symptoms
      STG, subtotal gastrectomy; TG, total gastrectomy; MRI, magnetic resonance imaging; DWI, diffusion-weighted imaging; CTC, Common Toxicity Criteria; QLQ, The European Organization for Research and Treatment of Cancer QOL Questionnaire; QOL, quality of life; tMDS/AML, therapy-related myelodysplastic syndrome/acute myeloid leukemia; SIR, standardized incidence ratio; EAR, excess absolute risk; SPC, second primary cancer; CI, confidence Interval; PTH, parathyroid hormone; OC, osteocalcin; TRACP5b, tartrate-resistant acid phosphatase isoenzyme 5b; ucOC, undercarboxylated OC; OPFs, osteoporotic fractures; HR, hazard ratio; AD, Alzheimer's disease; VaD, vascular dementia; FPC, first primary cancer; GI, gastrointestinal; SGA, subjective global assessment; GSRS, GI-Symptom Rating Scale; PTC, primary papillary thyroid cancer; MPC, multiple primary cancers; SGB2, subtotal gastrectomy with Billroth II reconstruction; EORTC QLQ-C30, the European Organization for Research and Treatment Quality of Life Questionnaire Core 30; EORTC QLQ-STO22, gastric cancer-specific module EORTC QLQ.

      Characteristics of older gastric cancer survivors

      In the selected studies, six operational definitions of cancer survivors were noted. We presented the characteristics of participants in Table 1. Undergoing surgery, being diagnosed, and completing active treatment were described as the beginning of survivorship. The most commonly used definitions of gastric cancer survivors included (1) patient who lived for five years or more after gastrectomy (4 studies, 28.6%)
      • Morais S.
      • Castro C.
      • Antunes L.
      • Peleteiro B.
      • Bento M.J.
      • Lunet N.
      Second primary cancers and survival in patients with gastric cancer: association with prediagnosis lifestyles.
      ,
      • Amikura K.
      • Ehara K.
      • Kawashima Y.
      The risk of developing multiple primary cancers among long-term survivors five years or more after stomach carcinoma resection.
      ,
      • Jun J.H.
      • Yoo J.E.
      • Lee J.A.
      • et al.
      Anemia after gastrectomy in long-term survivors of gastric cancer: a retrospective cohort study.
      ,
      • Lee S.S.
      • Chung H.Y.
      • Kwon O.K.
      • Yu W.
      Long-term quality of life after distal subtotal and total gastrectomy: symptom- and behavior-oriented consequences.
      and (2) active treatment completion to cancer recurrence (4 studies, 28.6%).
      • Choi Y.J.
      • Shin D.W.
      • Jang W.
      • et al.
      Risk of dementia in gastric cancer survivors who underwent gastrectomy: a nationwide study in Korea.
      ,
      • Gharagozlian S.
      • Mala T.
      • Brekke H.K.
      • Kolbjørnsen L.C.
      • Ullerud Å.A.
      • Johnson E.
      Nutritional status, sarcopenia, gastrointestinal symptoms and quality of life after gastrectomy for cancer – a cross-sectional pilot study.
      ,
      • Schonfeld S.J.
      • Morton L.M.
      • de González A.B.
      • Curtis R.E.
      • Kitahara C.M.
      Risk of second primary papillary thyroid cancer among adult cancer survivors in the United States, 2000-2015.
      ,
      • Lee J.E.
      • Shin D.W.
      • Lee H.
      • et al.
      One-year experience managing a cancer survivorship clinic using a shared-care model for gastric cancer survivors in Korea.
      The criteria for old age also varied, as shown in the mean age of the participants in Table 1. Seven studies (50%)
      • Iki M.
      • Fujita Y.
      • Kouda K.
      • et al.
      Increased risk of osteoporotic fracture in community-dwelling elderly men 20 or more years after gastrectomy: the Fujiwara-Kyo Osteoporosis Risk in Men (FORMEN) Cohort Study.
      • Morais S.
      • Castro C.
      • Antunes L.
      • Peleteiro B.
      • Bento M.J.
      • Lunet N.
      Second primary cancers and survival in patients with gastric cancer: association with prediagnosis lifestyles.
      • Morton L.M.
      • Dores G.M.
      • Schonfeld S.J.
      • et al.
      Association of chemotherapy for solid tumors with development of therapy-related myelodysplastic syndrome or acute myeloid leukemia in the modern era.
      ,
      • Horvath A.
      • Bausys A.
      • Sabaliauskaite R.
      • et al.
      Distal gastrectomy with Billroth II reconstruction is associated with oralization of gut microbiome and intestinal inflammation: a proof-of-concept study.
      ,
      • Amikura K.
      • Ehara K.
      • Kawashima Y.
      The risk of developing multiple primary cancers among long-term survivors five years or more after stomach carcinoma resection.
      ,
      • Jun J.H.
      • Yoo J.E.
      • Lee J.A.
      • et al.
      Anemia after gastrectomy in long-term survivors of gastric cancer: a retrospective cohort study.
      ,
      • Climent M.
      • Pera M.
      • Aymar I.
      • Ramón J.M.
      • Grande L.
      • Nogués X.
      Bone health in long-term gastric cancer survivors: a prospective study of high-dose vitamin D supplementation using an easy administration scheme.
      were conducted with older gastric cancer survivors over 65 years age. Looking at the mean age of participants, 60–64 years was the most common age range (7 studies, 50.0%),
      • Choi Y.J.
      • Shin D.W.
      • Jang W.
      • et al.
      Risk of dementia in gastric cancer survivors who underwent gastrectomy: a nationwide study in Korea.
      ,
      • Gharagozlian S.
      • Mala T.
      • Brekke H.K.
      • Kolbjørnsen L.C.
      • Ullerud Å.A.
      • Johnson E.
      Nutritional status, sarcopenia, gastrointestinal symptoms and quality of life after gastrectomy for cancer – a cross-sectional pilot study.
      ,
      • Schonfeld S.J.
      • Morton L.M.
      • de González A.B.
      • Curtis R.E.
      • Kitahara C.M.
      Risk of second primary papillary thyroid cancer among adult cancer survivors in the United States, 2000-2015.
      ,
      • Hu Y.
      • Kim H.I.
      • Hyung W.J.
      • et al.
      Vitamin B12 deficiency after gastrectomy for gastric cancer: an analysis of clinical patterns and risk factors.
      • Lee S.S.
      • Chung H.Y.
      • Kwon O.K.
      • Yu W.
      Long-term quality of life after distal subtotal and total gastrectomy: symptom- and behavior-oriented consequences.
      • Lee J.E.
      • Shin D.W.
      • Lee H.
      • et al.
      One-year experience managing a cancer survivorship clinic using a shared-care model for gastric cancer survivors in Korea.
      ,
      • Haneder S.
      • Budjan J.M.
      • Schoenberg S.O.
      • et al.
      Dose-dependent changes in renal (1)H-/(23)Na MRI after adjuvant radiochemotherapy for gastric cancer.
      and in one study, the participants were over 80 years old (7.1%).
      • Amikura K.
      • Ehara K.
      • Kawashima Y.
      The risk of developing multiple primary cancers among long-term survivors five years or more after stomach carcinoma resection.

      Types of late effects in older gastric cancer survivors

      Concerning late effects in older gastric cancer survivors, studies on the risk of second primary cancer were the most common (5 studies, 20.8%),
      • Morais S.
      • Castro C.
      • Antunes L.
      • Peleteiro B.
      • Bento M.J.
      • Lunet N.
      Second primary cancers and survival in patients with gastric cancer: association with prediagnosis lifestyles.
      ,
      • Morton L.M.
      • Dores G.M.
      • Schonfeld S.J.
      • et al.
      Association of chemotherapy for solid tumors with development of therapy-related myelodysplastic syndrome or acute myeloid leukemia in the modern era.
      ,
      • Amikura K.
      • Ehara K.
      • Kawashima Y.
      The risk of developing multiple primary cancers among long-term survivors five years or more after stomach carcinoma resection.
      ,
      • Schonfeld S.J.
      • Morton L.M.
      • de González A.B.
      • Curtis R.E.
      • Kitahara C.M.
      Risk of second primary papillary thyroid cancer among adult cancer survivors in the United States, 2000-2015.
      ,
      • Lee J.E.
      • Shin D.W.
      • Lee H.
      • et al.
      One-year experience managing a cancer survivorship clinic using a shared-care model for gastric cancer survivors in Korea.
      followed by bone health degradation due to vitamin deficiency (3 studies, 12.5%)
      • Iki M.
      • Fujita Y.
      • Kouda K.
      • et al.
      Increased risk of osteoporotic fracture in community-dwelling elderly men 20 or more years after gastrectomy: the Fujiwara-Kyo Osteoporosis Risk in Men (FORMEN) Cohort Study.
      ,
      • Lee J.E.
      • Shin D.W.
      • Lee H.
      • et al.
      One-year experience managing a cancer survivorship clinic using a shared-care model for gastric cancer survivors in Korea.
      ,
      • Climent M.
      • Pera M.
      • Aymar I.
      • Ramón J.M.
      • Grande L.
      • Nogués X.
      Bone health in long-term gastric cancer survivors: a prospective study of high-dose vitamin D supplementation using an easy administration scheme.
      and vitamin deficiency resulting from gastrectomy (2 studies, 8.3%).
      • Choi Y.J.
      • Shin D.W.
      • Jang W.
      • et al.
      Risk of dementia in gastric cancer survivors who underwent gastrectomy: a nationwide study in Korea.
      ,
      • Hu Y.
      • Kim H.I.
      • Hyung W.J.
      • et al.
      Vitamin B12 deficiency after gastrectomy for gastric cancer: an analysis of clinical patterns and risk factors.
      Moreover, iron deficiency (1 study, 4.2%),
      • Jun J.H.
      • Yoo J.E.
      • Lee J.A.
      • et al.
      Anemia after gastrectomy in long-term survivors of gastric cancer: a retrospective cohort study.
      postprandial fullness or eating dysfunction (1 study, 4.2%),
      • Lee S.S.
      • Chung H.Y.
      • Kwon O.K.
      • Yu W.
      Long-term quality of life after distal subtotal and total gastrectomy: symptom- and behavior-oriented consequences.
      bacterial overgrowth in the small intestine (1 study, 4.2%)
      • Horvath A.
      • Bausys A.
      • Sabaliauskaite R.
      • et al.
      Distal gastrectomy with Billroth II reconstruction is associated with oralization of gut microbiome and intestinal inflammation: a proof-of-concept study.
      were also evaluated. Three studies (12.5%) related to the late effects experienced by cancer survivors in general as well as gastric cancer survivors (cardiovascular disease risk,
      • Lee S.S.
      • Chung H.Y.
      • Kwon O.K.
      • Yu W.
      Long-term quality of life after distal subtotal and total gastrectomy: symptom- and behavior-oriented consequences.
      ,
      • Lee J.E.
      • Shin D.W.
      • Lee H.
      • et al.
      One-year experience managing a cancer survivorship clinic using a shared-care model for gastric cancer survivors in Korea.
      employment and return to work,
      • Lee S.S.
      • Chung H.Y.
      • Kwon O.K.
      • Yu W.
      Long-term quality of life after distal subtotal and total gastrectomy: symptom- and behavior-oriented consequences.
      healthy lifestyle,
      • Lee S.S.
      • Chung H.Y.
      • Kwon O.K.
      • Yu W.
      Long-term quality of life after distal subtotal and total gastrectomy: symptom- and behavior-oriented consequences.
      ,
      • Lee J.E.
      • Shin D.W.
      • Lee H.
      • et al.
      One-year experience managing a cancer survivorship clinic using a shared-care model for gastric cancer survivors in Korea.
      pain,
      • Gharagozlian S.
      • Mala T.
      • Brekke H.K.
      • Kolbjørnsen L.C.
      • Ullerud Å.A.
      • Johnson E.
      Nutritional status, sarcopenia, gastrointestinal symptoms and quality of life after gastrectomy for cancer – a cross-sectional pilot study.
      physical activity,
      • Gharagozlian S.
      • Mala T.
      • Brekke H.K.
      • Kolbjørnsen L.C.
      • Ullerud Å.A.
      • Johnson E.
      Nutritional status, sarcopenia, gastrointestinal symptoms and quality of life after gastrectomy for cancer – a cross-sectional pilot study.
      weight loss
      • Gharagozlian S.
      • Mala T.
      • Brekke H.K.
      • Kolbjørnsen L.C.
      • Ullerud Å.A.
      • Johnson E.
      Nutritional status, sarcopenia, gastrointestinal symptoms and quality of life after gastrectomy for cancer – a cross-sectional pilot study.
      ) were also conducted. Three studies (12.5%) examined renal dysfunction,
      • Haneder S.
      • Budjan J.M.
      • Schoenberg S.O.
      • et al.
      Dose-dependent changes in renal (1)H-/(23)Na MRI after adjuvant radiochemotherapy for gastric cancer.
      vaccination,
      • Lee J.E.
      • Shin D.W.
      • Lee H.
      • et al.
      One-year experience managing a cancer survivorship clinic using a shared-care model for gastric cancer survivors in Korea.
      and nausea and vomiting,
      • Lee S.S.
      • Chung H.Y.
      • Kwon O.K.
      • Yu W.
      Long-term quality of life after distal subtotal and total gastrectomy: symptom- and behavior-oriented consequences.
      which have not been previously studied as late effects in cancer survivors. The identified late effects shown in Table 1 highlight the detailed results of late effects in older gastric cancer survivors.

      Types of interventions for managing late effects

      Among the 14 studies, only one study (7.1%)
      • Climent M.
      • Pera M.
      • Aymar I.
      • Ramón J.M.
      • Grande L.
      • Nogués X.
      Bone health in long-term gastric cancer survivors: a prospective study of high-dose vitamin D supplementation using an easy administration scheme.
      included an intervention. This study was a prospective cohort study. To confirm the effect of preventing osteoporosis, patients with 25-(OH)-vitamin D ​≤ ​30 ​ng/mL at baseline received 16,000 IU of vitamin D3 oral supplements every 10 days for three months during the 1-year follow-up.
      • Climent M.
      • Pera M.
      • Aymar I.
      • Ramón J.M.
      • Grande L.
      • Nogués X.
      Bone health in long-term gastric cancer survivors: a prospective study of high-dose vitamin D supplementation using an easy administration scheme.
      They reported that the oral administration of high doses of vitamin D was easily performed and restored 25-(OH)-vitamin D and iPTH values, which were often disturbed after gastrectomy.

      Discussion

      This study demonstrated the research trends on the late effects of older gastric cancer survivors. The varied definitions of gastric cancer survivors have been employed depending on the trajectory of cancer treatment. Furthermore, the baselines for classifying older people based on age were mixed: 60 years old, 65 years old, 70 years old, and 80 years old or more. Most studies focused on the risk of second primary cancer and physical symptoms related to gastrectomy as the late effects. However, contrary to our expectations, interventional studies to manage the late effects were rare.
      Although we found many studies on older gastric cancer survivors, most studies were conducted with respect to survival, mortality, or recurrence rates.
      • Kadowaki S.
      • Komori A.
      • Narita Y.
      • et al.
      Long-term outcomes and prognostic factors of patients with advanced gastric cancer treated with S-1 plus cisplatin combination chemotherapy as a first-line treatment.
      ,
      • Yuri I.
      • Tomio N.
      • Isao M.
      • et al.
      Conditional survival for longer-term survivors from 2000-2004 using population-based cancer registry data in Osaka, Japan.
      ,
      • Lee J.A.
      • Kim S.Y.
      • Kim Y.
      • et al.
      Comparison of health-related quality of life between cancer survivors treated in designated cancer centers and the general public in Korea.
      ,
      • Rutkowski P.
      • Andrzejuk J.
      • Bylina E.
      • et al.
      What are the current outcomes of advanced gastrointestinal stromal tumors: who are the long-term survivors treated initially with imatinib?.
      Therefore, more studies are required to understand the late symptoms, experience, and difficulties of older gastric cancer survivors as patients with cancer have low average QOL,
      • Firkins J.
      • Hansen L.
      • Driessnack M.
      • Dieckmann N.
      Quality of life in "chronic" cancer survivors: a meta-analysis.
      which affects their symptoms.
      • Nayak M.G.
      • George A.
      • Vidyasagar M.S.
      • et al.
      Quality of life among cancer patients.
      Older cancer survivors are more likely to suffer from comorbid chronic conditions, such as late effects, and poor health status.
      • Holmes H.M.
      • Nguyen H.T.
      • Nayak P.
      • Oh J.H.
      • Escalante C.P.
      • Elting L.S.
      Chronic conditions and health status in older cancer survivors.
      Therefore, we need to prioritize research on QOL with a consideration of the late effects in older gastric cancer survivors, given that the proportion of them among cancer survivors is gradually increasing.
      Six late effects in overall cancer survivors, including screening for new primary cancer, healthy lifestyle, cardiovascular disease risk, employment and return to work, pain, and physical activity were identified. We also identified six late effects in gastric cancer survivors such as bone health, vitamin B12 deficiency, iron deficiency, postprandial fullness or eating dysfunction, small intestine bacterial overgrowth, and weight loss. However, there was little research on the symptom burden of late effects such as anxiety, depression, trauma, sexual function, diarrhea, chemotherapy-induced neuropathy, and fatigue.
      • NCCN
      NCCN Guidelines-General Survivorship.
      Moreover, a study reported that one-third of cancer survivors experienced adverse effects that had not been studied before.
      • Wu H.-S.
      • Harden J.K.
      Symptom burden and quality of life in survivorship: a review of the literature.
      This implies that researchers should expand and explore research topics related to cancer survivors. In future studies, it is necessary to describe unexamined late effects in older gastric cancer survivors, the differences in symptom burden among late effects, and the impact of late effects on QOL. Beyond exploring late effect experiences in cancer survivors, further studies should be conducted with specific age groups and characteristics that indicate a higher risk. Factors contributing to late effects should be efficiently assessed as well.
      We found that studies on late effects in older gastric cancer survivors were mainly conducted in Asia. This is because the incidence of gastric cancer is the highest in East Asia and Eastern Europe, while the incidence in North America and Northern Europe is generally low and equal to that in Africa. The age-standardized incidence rates for both regions are higher than the global age-standardized incidence rate(males: 15.8, females: 7.0) per 100,000 population.
      • Sung H.
      • Ferlay J.
      • Siegel R.L.
      • et al.
      Global cancer statistics 2020: GLOBOCAN estimates of incidence and mortality worldwide for 36 cancers in 185 countries.
      This may explain why studies of older gastric cancer survivors have been rare in Western countries such as North America, Central and South America, and Oceania. Nevertheless, gastric cancer remains one of the most common and deadly cancers worldwide, especially among older males.
      • Sung H.
      • Ferlay J.
      • Siegel R.L.
      • et al.
      Global cancer statistics 2020: GLOBOCAN estimates of incidence and mortality worldwide for 36 cancers in 185 countries.
      Therefore, it is necessary to actively research older gastric cancer survivors in countries where gastric cancer is prevalent and share the evidence with the world. These efforts will contribute to the development of effective care plans for gastric cancer survivors.
      The stage in the cancer trajectory at which patients with gastric cancer are viewed as gastric cancer survivors varied in the 14 studies included in this review. Defining cancer survivors may improve communication among patients with cancer and organizations that use and work with cancer survivors.
      • Marzorati C.
      • Riva S.
      • Pravettoni G.
      Who is a cancer survivor? A systematic review of published definitions.
      For patients, self-identifying as a cancer survivor is related to better QOL and mental health.
      • Cheung S.Y.
      • Delfabbro P.
      Are you a cancer survivor? A review on cancer identity.
      Defining cancer survivors also helps us compare the results of many studies and use them to assess how well they adapt to their transitions.
      A unified definition of the elderly is also required. Studies included in this review classified the elderly based on various baselines (eg., 60 or 70 or 80 years old). Currently, many studies on cancer survivors using big data are being conducted.
      • Major A.
      • Cox S.M.
      • Volchenboum S.L.
      Using big data in pediatric oncology: current applications and future directions.
      • Vromans R.D.
      • van Eenbergen M.C.
      • Geleijnse G.
      • Pauws S.
      • van de Poll-Franse L.V.
      • Krahmer E.J.
      Exploring cancer survivor needs and preferences for communicating personalized cancer statistics from registry data: qualitative multimethod study.
      • Warrington L.
      • Absolom K.
      • Velikova G.
      Integrated care pathways for cancer survivors–a role for patient-reported outcome measures and health informatics.
      Without standardization and harmonization processes of rigorous data, leveraging data from electronic health records seems challenging due to the inconsistency in terminology usage.
      • Meehan R.A.
      • Mon D.T.
      • Kelly K.M.
      • et al.
      Increasing EHR system usability through standards: conformance criteria in the HL7 EHR-system functional model.
      Therefore, it is essential to define cancer survivors and classify the elderly.
      Among the 14 studies, only one intervention study was included. Given the increasing number of older gastric cancer survivors, studies on managing late effects seem insufficient. Numerous studies have shown that cancer survivorship care plans improve satisfaction in cancer survivors.
      • Brennan M.E.
      • Gormally J.F.
      • Butow P.
      • Boyle F.M.
      • Spillane A.J.
      Survivorship care plans in cancer: a systematic review of care plan outcomes.
      ,
      • Williams V.A.
      • Brown N.I.
      • Johnson R.
      • et al.
      A web-based lifestyle intervention for cancer survivors: feasibility and acceptability of survivorSHINE.
      Therefore, to develop an appropriate care plan, further research on diverse care models or interventions for older gastric cancer survivors is needed. Moreover, further studies on suitable tools for screening late effects in gastric cancer survivors remain to be conducted.
      This study has several limitations. First, in our research, we searched databases using the keywords “late effects”, “long term effects”, and “late symptoms”. Therefore, studies not using these terms or not specifically classifying symptoms as late effects might not have been included. Second, we included studies published only in English and Korean. Therefore, we could not include the results of domestic studies in Japan or Eastern Europe, where the incidence of gastric cancer is fairly high. Despite these limitations, this study is meaningful, as it highlights the research trends in studies on older gastric cancer survivors and identifies the characteristics of late effects in older gastric cancer survivors.
      After active treatment completion, most patients with cancer go through transition phases and become cancer survivors. They sometimes have physical and psychological problems during transitions, moving forward to new satisfactory lives. Difficulties during transition may include persisting symptoms of disease and treatment, such as late effects. With the identification of the characteristics and factors related to late effects in older gastric cancer survivors, further studies may help understand the basis for caring and providing appropriate management. Hence, identifying the unmet needs of older gastric cancer survivors who experience late effects and conducting research on interventions will contribute to the successful transition of patients with cancer to cancer survivors and achieving improved health-related QOL in older gastric cancer survivors.

      Conclusions

      With advances in medical science and technology, the number of older gastric cancer survivors has increased. Accordingly, many older gastric cancer survivors are likely to suffer from the burden of late effects even after the completion of cancer treatment. This review highlights recent research trends on late effects in older gastric cancer survivors. Although many studies on gastric cancer survivors have been conducted, we found that the definition of cancer survivors in terms of the stage of treatment varied amongst the studies. In addition, late effects were mainly explored for secondary cancer and physical symptoms related to gastrectomy. Thus, further studies need to identify the undiscovered issues associated with older gastric cancer survivors. Also, the interaction mechanisms of late effects and symptom burden need to be investigated, focusing on the older population. Intervention studies of late effects were also limited. Experimental studies are needed to validate the effectiveness of interventions on various late effects, personalized care planning, and their sustainability over time. Although this review on gastric cancer clearly correlates with regional specificity in gastric cancer prevalence, we suggest that these findings have global currency given that older gastric cancer survivors are increasing worldwide.

      Author contributions

      MJ: Conceptualization, Data curation, Project administration, Writing—original draft, review and editing, Formal analysis, Visualization, Final approval of the version to be published. SK: Conceptualization, Data curation, Methodology, Funding acquisition, Project administration, Supervision, Validation, Writing—review and editing, Formal analysis. NY: Data curation, Formal analysis, Writing—review and editing, Formal analysis.

      Declaration of competing interest

      None declared.

      Finding

      This work was supported by the Basic Science Research Program through the National Research Foundation (NRF), funded by the Ministry of Education, Korea (Grant No. 2020R1A6A1A03041989). Misun Jeon received a scholarship from Brain Korea 21 FOUR Project funded by the NRF of Korea, Yonsei University College of Nursing .

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