Published online Jun 07, 2023.
https://doi.org/10.5230/jgc.2023.23.e23
Outcomes of Gastrectomy for Gastric Cancer in Patients Aged >80 Years: A Systematic Literature Review and Meta-Analysis
Abstract
This meta-analysis examined the surgical management of older patients (>80 years) with gastric cancer, who were often excluded from randomized controlled trials. We analyzed 23 retrospective cohort studies involving 18,372 patients and found that older patients had a higher in-hospital mortality rate (relative risk [RR], 3.23; 95% confidence interval [CI], 1.46–7.17; P<0.01) and more post-operative complications (RR, 1.36; 95% CI, 1.19–1.56; P<0.01) than did younger patients. However, the surgical complications were similar between the two groups. Older patients were more likely to undergo less extensive lymph node dissection and longer hospital stays. Although older patients had statistically significant post-operative medical complications, they were not deprived of surgery for gastric cancer. The comorbidities and potential risks of post-operative complications should be carefully evaluated in older patients, highlighting the importance of careful patient selection. Overall, this meta-analysis provides recommendations for the surgical management of older patients with gastric cancer. Careful patient selection and evaluation of comorbidities should be performed to minimize the risk of post-operative complications in older patients, while recognizing that they should not be deprived of surgery for gastric cancer.
INTRODUCTION
Gastric cancer is a global health problem, with more than one million newly diagnosed cases worldwide each year [1]. According to the latest estimates released by GLOBOCAN in 2020, the annual number of gastric cancers globally reached 1,089,000 (corresponding to an age-standardized incidence rate of 11.1 per 100,000), ranking fifth among all malignant tumors. In the same year, 769,000 deaths were caused by gastric cancer (corresponding to an age-standardized mortality rate of 7.7 per 100,000), ranking fourth among all cancer types, after lung, colorectal, and liver cancers [2]. The annual burden of gastric cancer is predicted to surge to about 1.8 million new cases and 1.3 million deaths by 2040 [3]. In all populations, gastric cancer is uniformly rare in adults aged <50 years; however, gastric cancer incidence rates increase with increasing age, reaching a plateau between 55 and 80 years. In addition, the incidence of gastric cancer are two-fold to three-fold higher in men than in women [4, 5].
Globally, the incidence of gastric cancer has a normal distribution curve, with a peak age of incidence between 65 and 75 years in both males and females, whereas the incidence of death peaks between 65 and 80 years in males and between 70 and 85 years in females [6].
At the biological level, aging is characterized by a gradual, lifelong accumulation of molecular and cellular damage that results in a progressive, generalized impairment of many bodily functions, increased vulnerability to environmental challenges, and a growing risk of disease and death [7]. The aging population presents healthcare challenges due to frailty and complex health issues because multimorbidity affects over 60% of the older and can lead to adverse physiological consequences and mortality. Hence, surgery in older patients of advanced age increases morbidity and mortality risk [8, 9, 10]. East Asia and Southeast Asia experienced the strongest impact of population aging, with more than half of the countries in these regions having less than a 1% population growth between 2015 and 2020, indicating that they are becoming aging or aged societies [11].
With a shift in demographics, gastric cancer cases are becoming increasingly common in very older age groups. A study conducted by the Korean Gastric Cancer Association (KGCA) on data from 14,076 cases from 68 institutions in Korea revealed that the proportion of gastric cancer patients who were aged ≥71 years increased from 9.1% in 1995 to 28.8% in 2019 [12]. The aforementioned statistics, together with the fact that East Asian countries, including China, Japan, and Korea, contributed to 60.3% of gastric cancer cases worldwide in 2020 [3], highlight the necessity of formulating suitable recommendations for managing gastric cancer cases in the older population aged 80 years and above, given the ongoing demographic transition.
Older patients with gastric cancer aged 80 years are often not included in randomized controlled trials (RCTs), which can provide guidelines for surgical management. Most studies involving older patients have been retrospective cohort studies. We identified six recent meta-analyses that evaluated the effects of gastrectomy in older patients with gastric cancer. However, five of these studies did not specify a cutoff age for the older population; instead, they analyzed a broad range of ages within this group. Among the identified studies, four focused on patients aged 65–75 years [13, 14, 15, 16], one on patients aged 65–80 years [17], and one study on patients aged 65–85 years [18]. This lack of consistency in defining the “older” population can lead to issues with representativeness, variability within the age range, heterogeneity among the studies, and potential bias. Therefore, generalizing the findings and drawing conclusions from such meta-analyses to a broader older population should be performed with caution. One study [19], conducted in 2019, defined older as patients aged 80 years and above, but employed odds ratios for dichotomous variables in retrospective cohort studies, which can result in a less intuitive measure of association. Five other studies compared surgical approaches, open and laparoscopic, in older patients above the age of 80 [20, 21, 22, 23, 24]. Hence, we conducted a thorough systematic literature review and meta-analysis, stratifying patients by an age cutoff of 80 years and using risk ratios (RRs) for all dichotomous variables to arrive at a stronger recommendation, for the treatment of patients with gastric cancer above 80 years of age.
MATERIALS AND METHODS
Literature search
We published a protocol on PROSPERO on the date 13/02/2023 with the publication ID CRD42023394832 after confirming that no other systematic literature review and meta-analysis on the same topic is ongoing. A systematic literature search was performed using four major databases: PubMed, Embase, Web of Science, and Cochrane Library. For each database, the following terms were combined as “Keywords”: Gastric cancer OR Gastric Ca OR Stomach Cancer OR Cancer of the stomach OR Stomach malignancy OR Gastric Malignancy OR Gastric neoplasm OR Malignant neoplasm of the stomach; Elderly OR Above 80 OR Octogenarians OR Very old OR Very elderly OR aged; Stomach surgery OR Gastrectomy OR Distal Gastrectomy OR Proximal Gastrectomy OR Total Gastrectomy. The present meta-analysis aligned with the Preferred Reporting Items for Systematic Reviews and Meta-Analyses (PRISMA) statement [25]; the PRISMA framework is visually represented in Fig. 1. A thorough systematic literature search was performed using four major databases. We looked for articles that compared the outcome of gastrectomies in older patients (≥80 years) versus younger patients (<80 years) [26–48]. The final search was conducted on February 13, 2023. A detailed search strategy is provided in Appendix 1. Additionally, a manual search of the related articles and reference lists of the identified studies was conducted to identify any additional studies that might have been overlooked. The inclusion criteria for the studies were limited to those published in English and conducted within the past two decades.
Fig. 1
PRISMA frame work.
From: Page MJ, McKenzie JE, Bossuyt PM, Boutron I, Hoffmann TC, Mulrow CD, et al. The PRISMA 2020 statement: an updated guideline for reporting systematic reviews. BMJ 2021;372: n71. DOI: 10.1136/bmj. n71.
Selection criteria
The inclusion criteria were as follows: eligible patients for inclusion in the meta-analysis were those with pathologically confirmed stomach carcinoma, who underwent gastrectomy as a treatment modality and were divided into two age groups: older than 80 years and younger than 80 years. In addition to this, studies that included patients above 80 years old, and a subset of patients above and below 80 years of age were included. Studies that included only patients below 80 years of age, recurrent gastric cancer patients, stage 4 gastric cancer patients who underwent palliative surgery, and patients who did not undergo surgical treatment were excluded. The inclusion criteria for the studies were limited to those published in the past 20 years, including RCTs, and cohort studies that provided a comparative analysis between older and younger patients with gastric cancer. The studies were required to be published in English, and document pre-operative patient status as well as intraoperative and post-operative treatment courses. Excluded studies were those in the form of case reports, case series, case-control studies, reviews, letters and comments, unpublished research, studies that did not provide specific data of interest, or those with fewer than 40 study participants.
Data extraction and quality assessment
Two independent reviewers performed data extraction and quality assessment using a standardized form. Both independently screened the records for inclusion and exclusion, and the researchers were blinded to each other’s decisions until the final decision was made. Any disagreements were resolved through discussion until a consensus was reached. The extracted data included the Study ID (first author’s name and publication year), country, study period, sample size, sex, mean age, mean body-mass index, pre-operative comorbidities, American Society of Anesthesiologists (ASA) Physical Status Classification System, type of surgery, extent of lymph node dissection (D1, D1+, or D2), operation time, intraoperative blood loss, number of harvested lymph nodes, post-operative complications, in-hospital mortality, and length of hospital stay. The fundamental parameters and features of these studies are listed in Table 1. The Newcastle-Ottawa Quality Assessment tool was used to assess the quality of the studies (http://www.ohri.ca/programs/clinical_
Table 1
Fundamental parameters and features of the studies that have been incorporated
Table 2
The Newcastle-Ottawa Quality Assessment Scale
The outcome of interest
The outcomes of interest were in-hospital mortality, number of complications, number of lymph nodes harvested during surgery, curative resection, operation time, intraoperative blood loss, and post-operative hospital stay.
Statistical analysis
Statistical analyses were performed using JL, ZM, and CG software. This meta-analysis used pooled RR with 95% confidence intervals (CIs) for all dichotomous variables, such as in-hospital mortality, the number of lymph nodes harvested during surgery, curative resection, and the number of complications. We used weighted mean differences (WMD) with 95% CIs for continuous variables, such as operation time, intraoperative blood loss, and post-operative hospital stay. We applied the method described by Hozo et al. [49] to convert the medians and interquartile ranges to the mean and standard deviation (SD) for studies that reported the median and interquartile range instead of the mean and SD. Statistical heterogeneity was assessed using the methods described by Higgins et al. [50], using I square with P-values. Values between 0% and 25% indicated low heterogeneity, values between 25% and 50% suggested moderate heterogeneity, and values above 50% indicated high heterogeneity. Pooled effects were calculated using the Inverse Variance for random effects models described by DerSimonian and Laird [51]. We assumed that the studies analyzed did not have similar populations, interventions, and outcomes. In addition, the random-effects model had a more conservative result; hence, we used it for the meta-analysis. The analysis was performed based on age cutoffs, specifically for patients with gastric cancer aged >80 years and <80 years. We utilized appropriate statistical formulae to merge subgroups of patients aged <80 years in 6 studies [21, 29, 31, 32, 38, 41]. Forest plots for the meta-analysis, meta-regression, and funnel plots were constructed using R (version 4.0.2; R Foundation for Statistical Computing, https://www.r-
RESULTS
A systematic literature search initially retrieved 2,408 articles. After screening topics and abstracts, 58 articles were selected for full-text assessment. Studies with age cut points of 65 (n=2), 70 (n=14), and 75 (n=13) were excluded due to inconsistent usage of the definition of “elderly.” Case-control studies (n = 1) and studies comparing laparoscopic and open gastrectomy in older patients aged >80 years (n = 5) were excluded. To avoid confusion, only studies with an age cut point of 80 years were selected for analysis, resulting in 23 papers. These studies were divided into two groups for analysis. The first analysis compared patients aged >80 years and those aged <80 years. The PRISMA flowchart of the literature review is presented in Fig. 1, and Table 1 displays the fundamental parameters and features of the studies. A total of 18,372 patients were included in the meta-analysis, and older and younger patient groups were compared. Of the 23 studies, 13 were conducted in Japan, three in Korea, two in Italy, two in the US, one in Taiwan, one in Canada, and one in China. All studies achieved a minimum of six stars on the Newcastle-Ottawa Quality Assessment Scale (Table 2).
Older patients had higher in-hospital mortality compared to that of the younger group (RR, 3.23; 95% CI, 1.46–7.17, P <0.01; Fig. 2A). There was no difference in the curative R0 resection between the two groups (RR, 0.99; 95% CI, 0.96–1.02; P=0.53; Fig. 2B). Older patients were more likely to have less D2 lymph node dissection than their younger counterparts (RR, 1.85; 95% CI, 1.46–2.33, P<0.01; Fig. 2C). There was a higher number of post-operative complications in the older group than in the younger counterparts (RR, 1.36; 95% CI, 1.19–1.56; P<0.01; Fig. 2D). Operations were significantly faster in the older age group as compared to their younger counterparts (WMD, −0.30; 95% CI, −0.49 to −0.11; P<0.01; Fig. 2E). Intraoperative bleeding was lesser in the older group (WMD, −0.39; 95% CI, −0.69 to −0.09, P=0.01; Fig. 2F). Longer post-operative hospital stays were observed in older patients as compared to that in their younger counterparts (RR, 0.41; 95% CI, 0.11 to 0.70; P<0.01; Fig. 2G). Older patients have higher pre-operative comorbidities and higher ASA scores compared to those of younger patients. Besides, older patients have a higher rate of post-operative medical complications like cardiovascular and pulmonary complications. Surgical complications are similar between the two groups except for anastomotic leakage, which is higher in the older group. The summarized forest plot for the burden of comorbidities and ASA scores are demonstrated in Table 3, and that of post-operative complications are depicted in Table 4.
Fig. 2
Meta-analysis forest plots for the studies: comparison between elderly and non-elderly. (A) In-hospital mortality, (B) Curative R0 resection, (C) Less D2 lymph node dissection, (D) The number of complications, (E) Operation time, (F) Intraoperative bleeding, (G) Post-operative hospital stay, (H) Pre-operative cardiovascular disease, (I) Pre-operative respiratory disease, (J) Pre-operative Diabetes Mellitus, (K) Pre-operative Hypertension, (L) Pre-operative liver disease, (M) Pre-operative renal disease, (N) ASA class 3 and 4, (O) Surgical site infection, (P) Post-operative bleeding, (Q) Anastomotic leakage, (R) Pancreatic fistula, (S) Ileus/ bowel obstruction, (T) Pulmonary complications, (U) Cardiac complications, (V) Delirium.
CI = confidence interval.
Table 3
Summarized meta-analysis of pre-operative comorbidities and ASA class 3 and 4
Table 4
Summarized meta-analysis of post-operative surgical and medical complications
On the meta-regression, out of the seven outcomes of interest, no cause for heterogeneity could be found in any of the four variables in five studies (Fig. 3B-E, and G). The meta-regression for the in-hospital mortality showed higher mortality in the East Asian region compared to that of the rest of the world (r = 1; SE = 1.48; 95% CI, 0.70 to 2.26; P=0.0002; Fig. 3A). Intraoperative bleeding was higher in the East Asian region (r = 0.97; SE = 1.21; 95% CI, 0.92 to 1.50; P=0.0049; Fig. 3E) and in the male gender (r = 0.65; SE = 5.25; 95% CI, 1.59 to 8.90; P=0.0002; Fig. 3E).
Fig. 3
Bubble plot of fitted regression line and Meta-regression with single covariates, τ2: estimated amount of residual heterogeneity. (A) In-hospital mortality, (B) Curative R0 resection, (C) Less D2 lymph node dissection, (D) The number of complications, (E) Operation time, (F) Intraoperative bleeding, (G) Post-operative hospital stay.
SE = standard error; CI = confidence interval.
To assess the possibility of publication bias or other sources of small-study effects, funnel plots were done for each outcome variable which showed evidence of publication bias with an asymmetric distribution in one of the studies (Fig. 4G). We conducted a trim-and-fill analysis to address this bias, which identified 5 missing studies. After filling in these missing studies, the funnel plot became symmetrical, indicating a reduced risk of publication bias (Fig. 4H). The remaining six funnel plot revealed a symmetrical distribution of study results, suggesting an absence of publication bias (Fig. 4A-F).
Fig. 4
Funnel plots, P-value by rank correlation test of funnel plot asymmetry (Begg’s test). (A) In-hospital mortality, (B) Curative R0 resection, (C) Less than D2 dissection, (D) Number of complications, (E) Operation time, (F) Post-operative hospital stay, (G) Intraoperative bleeding before trim and fill method, (H) Intraoperative bleeding after trim and fill method.
DISCUSSION
The results of our meta-analysis indicate that older patients who undergo gastrectomy for gastric cancer are more likely to have higher ASA scores and comorbidities, such as cardiac illness and respiratory disease, than do younger patients. Based on our analysis, older patients have similar surgical complications, except for anastomotic leakage, which is higher in the older patients but has significantly higher post-operative medical complications such as pulmonary and cardiac diseases. Moreover, there is a higher number of post-operative complications in the older group than in the younger counterparts. However, in the older group operations were significantly faster and has lesser intraoperative bleeding compared to those in their younger counterparts, which is an interesting observation that warrants further investigation. One possible explanation is that the extent of lymph node dissection at D2 and above was greater in the younger group than in the older group. However, the reasons underlying these findings remain unclear. The curative ability of the resection was similar in both groups. Despite the higher rates of comorbidities, we found a similar number of surgical complications between the two groups except for anastomotic leakage. Post-operative hospital stay and in-hospital mortality rates were significantly higher in older patients. The fact that a large proportion of older patients present with comorbidities and are more vulnerable to surgical stress, poses the challenge of a potentially higher number of post-operative medical complications and in-hospital mortality, probably because of higher ASA class and pre-operative comorbidities. Hence, older patients with gastric cancer who are candidates for gastrectomy should be carefully evaluated for comorbidities, and a thorough pre-operative preparation is warranted to reduce the potential risk of post-operative complications. However, surgery for gastric cancer should not be denied only because of age.
Subgroup analysis was performed using meta-regression to explore heterogeneity in the outcomes of interest across various covariates. The results showed that in five out of the seven outcomes of interest, no cause for heterogeneity could be found in any of the four covariates considered in the meta-regression analysis. However, for in-hospital mortality, the meta-regression analysis revealed a higher mortality rate in East Asia than in the rest of the world. Similarly, the incidence of intraoperative bleeding was higher in East Asians and the male gender. Overall, these results suggest that there may be important differences in health outcomes related to regional and demographic factors. However, it is important to interpret these findings with caution, as the study investigated only a limited set of covariates and may not be representative of all populations or contexts. Further research is needed to confirm and expand upon these findings and explore the potential mechanisms underlying the observed differences.
It is important to note the limitations of this study. All studies included in our analysis were retrospective, which could introduce bias owing to factors such as patient selection, surgeon techniques, surgical extent, and regional differences. In addition, we were unable to find studies that used RCTs to compare the older and younger groups. Furthermore, some studies reported median and interquartile ranges for continuous variables, which were converted to means and SDs using the method described by Hozo et al. [49]. This conversion may also result in bias. In addition to this. There is a lack of the necessary data for studies using the Kaplan–Meier curve, including the number of individuals at risk at each time point, the number of individuals who experienced the event of interest at each time point, and the corresponding survival probability. Together with the poor quality of the Kaplan–Meier curves in most studies and the lack of hazard ratios and their 95% CIs, we did not analyze the pooled 5-year overall survival rate; hence, were unable to evaluate long-term outcomes in both groups. Moreover, our meta-analysis only included studies published in English, which might have omitted important studies published in other languages. Finally, >50 percent of the included studies were conducted in Japan, which may limit the generalizability of our findings to other populations.
Despite these limitations, the results of this meta-analysis have important implications for clinical practice because the cutoff age was 80 years to define the older population, and all included studies were retrospective cohort studies that provided the advantage of increased precision, reduced heterogeneity, and improved generalizability for the decision-making process to clinicians when dealing with friable patients with gastric cancer. In addition, by including studies with similar age cutoff points, the results were less likely to be influenced by confounding factors and were more representative of the population of interest.
Future studies investigating the factors contributing to faster operation times in the older age group are needed. Additionally, we recommend RCTs to examine the impact of laparoscopic versus open surgery in older patients with gastric cancer.
In conclusion, older patients with gastric cancer who are candidates for gastrectomy should be carefully evaluated for comorbidities and the potential risk of post-operative complications; and should not be denied the surgical management for gastric cancer. These findings highlight the importance of careful patient selection and the evaluation of comorbidities in older patients undergoing surgery for gastric cancer.
Conflict of Interest:No potential conflict of interest relevant to this article was reported.
Author Contributions:
Conceptualization: G.C.S.
Data curation: M.Z.C.
Formal analysis: M.Z.C., L.J.S.
Investigation: M.Z.C.
Methodology: G.C.S., M.Z.C., L.J.S.
Supervision: G.C.S.
Validation: G.C.S.
Visualization: M.Z.C., L.J.S.
Writing - original draft: M.Z.C.
Writing - review & editing: G.C.S.
ACKNOWLEDGMENTS
We express our sincere gratitude to Drs. Birkneh Tilahun Tadesse and Alessandro Parente for their invaluable contributions to our meta-analysis by providing invaluable ideas, insights, and encouragement throughout the analysis, which were instrumental in shaping the direction of our work and ensuring its success. We are fortunate to have had the opportunity to work with such conversant colleagues, and we acknowledge them unreservedly for their assistance.
Appendix 1
Search strategy
PubMed Search strategy, February 4, 2023
((“Gastric Ca*” [tiab] OR “Gastric malignancy” [tiab] OR “Gastric Neoplasm*” [tiab] OR “Gastric tumor” [tiab] OR “Stomach cancer” [tiab] OR “Stomach tumor” [tiab] OR “Cancer of the stomach” [tiab] OR “Stomach neoplasm*” [tiab] OR “Stomach Neoplasms” [MeSH]) AND ( Gastrectomy [tiab] OR “Total Gastrectomy” [tiab] OR “ Subtotal Gastrectomy” [tiab] OR “Partial Gastrectomy” [tiab] OR “Distal gastrectomy” [tiab] OR “Proximal gastrectomy” [tiab] OR Gastrectomy [MeSH])) AND (“Older than 80 years” [tiab] OR Elderly [tiab] OR “ Very elderly” [tiab] OR Aged [tiab] OR Octogenarian [tiab] OR Aged [MeSH])
Embase search strategy, February 6, 2023
(‘Gastric Ca*’ ti,ab,kw OR ‘Gastric malignancy’ ti,ab,kw OR ‘Gastric Neoplasm*’ ti,ab,kw OR ‘Gastric tumor’ ti,ab,kw OR ‘Stomach cancer’ ti,ab,kw OR ‘Stomach tumor’ ti,ab,kw OR ‘Cancer of the stomach’ ti,ab,kw OR ‘Stomach neoplasm*’ ti,ab,kw OR 'stomach cancer' exp) AND (‘Older than 80 years’ ti,ab,kw OR ‘Elderly’ ti,ab,kw OR ‘Very elderly’ ti,ab,kw OR ‘Aged’ ti,ab,kw OR ‘Octogenarian, ti,ab,kw ‘Aged’ exp) AND ( ‘Gastrectomy’ ti,ab,kw OR ‘Total Gastrectomy’ ti,ab,kw OR ‘Subtotal Gastrectomy’ ti,ab,kw OR ‘Partial Gastrectomy’ ti,ab,kw OR ‘Distal gastrectomy’ ti,ab,kw OR ‘Proximal gastrectomy’ ti,ab,kw OR ‘Gastrectomy’ exp)
Cochrane library, February 9, 2023
(“Gastric Ca*” [tiab] OR “Gastric malignancy” [tiab] OR “Gastric Neoplasm*” [tiab] OR “Gastric tumor” [tiab] OR “Stomach cancer” [tiab] OR “Stomach tumor” [tiab] OR “Cancer of the stomach” [tiab] OR “Stomach neoplasm*” [tiab] OR “Stomach Neoplasms” [MeSH]) AND (“Older than 80 years” [tiab] OR Elderly [tiab] OR “ Very elderly” [tiab] OR Aged [tiab] OR Octogenarian [tiab] OR Aged [MeSH]) AND ( Gastrectomy [tiab] OR “Total Gastrectomy” [tiab] OR “ Subtotal Gastrectomy” [tiab] OR “Partial Gastrectomy” [tiab] OR “Distal gastrectomy” [tiab] OR “Proximal gastrectomy” [tiab] OR Gastrectomy [MeSH])
Web of Science Search Strategy, February 13, 2023
(((((((ALL=(“Gastric Ca*” )) OR ALL=(“Gastric malignancy”)) OR ALL=(“Gastric Neoplasm*” )) OR ALL=(“Gastric tumor” )) OR ALL=(“Stomach cancer”)) OR ALL=(“Stomach tumor”)) OR ALL=(“Cancer of the stomach”)) OR ALL=(“Stomach neoplasm*”) AND ((((ALL=(“Older than 80 years”))) OR ALL=(Elderly)) OR ALL=(“Very elderly”)) AND ALL=(Aged) AND (((((ALL=(Gastrectomy)) OR ALL=(“Total Gastrectomy”)) OR ALL=(“Subtotal Gastrectomy” )) AND ALL=(“Partial Gastrectomy”)) OR ALL=(“Distal gastrectomy”)) OR ALL=(“Proximal gastrectomy”)
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