3.6 Publication bias
Because there were only 6 studies included, publication bias was only evaluated by Funnel plots and Begg test. The results demonstrated that there was no publication bias according to Begg test with continuity corrected (P = .707). The funnel plot presented by Begg test is shown in Fig. 4.
Postoperative readmission is a common postoperative adverse event that is closely related with patients’ long-term quality of life. The reported postoperative readmission rate is nearly 20% at 30 days postoperation and can rise to 45% at 1-year postoperation.[7–10,18] Due to the different characteristics of different diseases and surgeries, the incidence rate and risk factors for postoperative readmission are various. Generally, physical condition was closely related to the incidence of postoperative readmission. A previous study reported that Eastern Cooperative Oncology Group performance status score and frailty were useful predictive factors for readmission within 1 year after gastrectomy in older (over 65 years) gastric cancer patients. We performed this study and found that the incidence rate of postoperative 30-day readmission was 11.7% for gastric cancer patients with surgical treatment. This study identified several risk factors for 30-day readmission after gastric cancer surgery. Nonhome discharge, diabetes mellitus, postoperative complications, resection pattern (total gastrectomy), and combined organ resection were independent risk factors for postoperative readmission. We also found that patients with postoperative 30-day readmission had significantly poorer survival outcomes than patients without readmission.
The incidence rate of postoperative readmission for gastric cancer patients was various in a different time frames. The results from the California Cancer Registry database showed that 28.8% patients had postoperative readmission, and the readmission rates were 53.6% in the first 30 days, 30.2% in the second 30 days, and 16.2% in the third 30 days. Readmission in different time periods was caused by different reasons; the postoperative 30-day readmission rate reflected the short-term postoperative recovery process. However, the 90-day readmission rate reflected long-term postoperative complications, adverse events caused by adjuvant chemotherapy or radiotherapy, and some other factors. Therefore, the present study only explores the risk factors of postoperative 30-day readmission.
The incidence rate of postoperative readmission was closely related to the complexity of the operations. In the presented study, the readmission rate at 30 days postgastrectomy was 11.7%. The reported readmission rate was diverse among included studies; the incidence rate was 2.7%, 2.9%, and 7.2% in the 3 studies from East Asia[15–17] but was 14.2%, 14.6%, and 16.5% in the other 3 studies from the United States.[12–14] Reasons for the different readmission rates between these studies are unclear. We believe that the characteristics of patients and postoperative management strategies may be the cause. Different readmission criteria are another important factor that may result in the different readmission rates between the East and the West.
It is clear that the incidence of postoperative complications is closely related with postoperative readmission after discharge.[10,29,30] Additionally, in the present studies, we found that patients in the readmission group have a higher complications rate than those in the nonreadmission group (OR 2.68, 95% CI 1.54–4.65, P < .01), and postoperative complication is an independent risk factor for postoperative readmission after discharge (OR 2.656, 95% 1.331–5.300, P = .006). Although the results suggested that postoperative complication was a significant risk factor for the incidence of postoperative 30-day readmission, we also observed that these results had high heterogeneity in the meta-analysis. The high heterogeneity may be because the classifications of complications may be different among studies. Even so, these results have clinical implications for the postoperative management and follow-up period. On one hand, for those patients who have postoperative complications, extra attention should be given during the duration of the follow-up. On the other hand, for patients without postoperative complications during the hospital stay, attention should be paid to those patients who have high risk factors for either postoperative complications or postoperative readmission.
Nevertheless, different diseases have different reasons for postoperative readmission. The study based on the data of the American College of Surgeons National Surgery Quality Improvement Program reported that wound complications (55%) were the major reason for postoperative readmission after lower extremity bypass surgery. In the present study, we found that the intolerability of oral intake was the most common reason for postoperative readmission (up to 30.8%).[12,13,15–17] Postoperative abdominal pain, eating disorders due to fear, gastrointestinal functional disorders, and incomplete obstruction are likely to result from the intolerability of oral intake, which is specific for operations of the esophagus and stomach. We also observed that the diversity of readmission causes was different among studies.
In addition, the general conditions of patients are another risk factor closely related to postoperative 30-day readmission. Comorbid conditions, such as diabetes, cardiovascular, and chronic pulmonary disease, can increase the risk of postoperative discharge.[32–34] These comorbidities increase the incidence risk of postoperative complications, which can result in the incidence of postoperative discharge. Moreover, acute exacerbation of these comorbidities during the postoperative rehabilitation period can also result in postoperative readmission.
Furthermore, whether laparoscopic surgery will increase the likelihood of postoperative 30-day readmission for gastric cancer surgery is unclear. There were several studies that reported that laparoscopic surgery was equally as safe as open surgery.[35,36] The study by Ammori et al reported that laparoscopic surgery is an independent risk factor for 30-day readmission, and they concluded that pancreatic damage and, correspondingly, pancreatic fistula caused by laparoscopic surgery were the major reasons for readmission. Additionally, we noticed that the readmission rate presented by a Japanese study was higher in the laparoscopic group than in the open surgery group. Therefore, limited evidence explores the relationship between laparoscopic surgery and 30-day readmission; whether laparoscopic surgery increases the risk of postoperative 30-day readmission requires further investigation. Besides, robotic surgery is being employed with increasing frequency in recent years and it can be performed as safely as laparoscopic and open surgery.[38,39] However, there is no analysis about the relationship between robotic surgery and postoperative readmission of those 6 included studies. Asaoka et al mentioned that they excluded the robotic surgery and the other 5 studies did not mention whether included robotic surgery in the analysis.[12–14,16,17] Besides, there is limited studies compared the postoperative readmission after robotic gastric cancer surgery with laparoscopic or open surgery. A Korean retrospective study reported that there is no difference of postoperative 30-day readmission among open, laparoscopic and total gastrectomy. Therefore, further studies are expected to examine whether robotic surgery has specific risk factors of postoperative readmission.
We also observed that nonhome discharge is an independent risk factor for postoperative readmission in the pooled analysis. Discharge to a nonhome facility appeared to nearly double the risk of readmission, even when adjusting for confounding factors. Patients who are older, who have poor health status or who have postoperative complications were more likely have been discharged to such facilities. Additionally, those facilities have a professional background and have a communication channel with hospital, which may increase the likelihood of readmission. However, those patients discharged to the local hospital or nursing facility may have reduced readmission due to some nonserious complications, such as superficial site infection. Therefore, the relationship between nonhome discharge and readmission may be underestimated and requires further exploration.
We also analyzed the survival outcomes between the readmission patients and nonreadmission patients and found poor survival outcomes for readmission patients. Although only 2 studies reported the overall survival outcomes in the present study,[12,13] the results coincided, and the pooled results lacked significant heterogeneity. We also noticed that there was another study, which was not included in the meta-analysis, that found that readmission (postoperative 90-day) was also closely correlated with poor long-term survival outcomes. We hypothesize that poor survival outcomes of readmission patients may be due to the synthetic action of the poor characteristics of these patients and the delay of postoperative adjuvant therapy.
The present study also has some limitations. First, this study only included 6 studies, most of which were retrospective studies. Therefore, selection bias and quality deviation is likely among these studies, which may have an influence on the results of the meta-analysis. Second, the standard of the postoperative complications was different among included studies. Third, who makes the decision of postoperative readmission and the judgment standard of readmission was also different in the studies. Therefore, it is difficult to determine which complication is the major reason for postoperative readmission.
Postoperative readmission is a common postoperative adverse event after discharge and can be influenced by the synthetic action of preparative, intraoperative, and postoperative factors. Although postoperative complications are the major reason for readmission, the comorbidities and operative wounds also affect the incidence of postoperative 30-day readmission. Extra attention should be paid to those patients with high risk factors during the postoperative follow-up and recovery periods.
The authors thank the Chinese Evidence-based Medicine Center West China Hospital, Sichuan University for providing statistics consultation.
Conceptualization: Wei-Wei Wu, Wei-Han Zhang, Xiao-Qian Deng, Tao Zhu.
Data curation: Wei-Wei Wu, Wei-Han Zhang.
Formal analysis: Wei-Wei Wu, Wei-Han Zhang, Wei-Yi Zhang, Lei Yang.
Funding acquisition: Xiao-Qian Deng, Wei-Han Zhang.
Methodology: Wei-Wei Wu, Wei-Han Zhang, Wei-Yi Zhang, Lei Yang, Tao Zhu.
Software: Wei-Wei Wu, Wei-Han Zhang, Wei-Yi Zhang, Lei Yang, Xiao-Qian Deng.
Supervision: Wei-Yi Zhang, Tao Zhu.
Writing – original draft: Wei-Wei Wu, Wei-Han Zhang.
Writing – review &editing: Wei-Yi Zhang, Lei Yang, Xiao-Qian Deng, Tao Zhu.
. Colquhoun A, Arnold M, Ferlay J, et al. Global patterns of cardia and non-cardia gastric cancer
incidence in 2012. Gut 2015;64:1881–8.
. Bray F, Ferlay J, Soerjomataram I, et al. Global cancer statistics 2018: GLOBOCAN estimates of incidence and mortality worldwide for 36 cancers in 185 countries. CA Cancer J Clin 2018;68:394–424.
. Shu Y, Zhang W, Hou Q, et al. Prognostic significance of frequent CLDN18-ARHGAP26/6 fusion in gastric signet-ring cell cancer. Nat Commun 2018;9:2447.
. Chen W, Zheng R, Zuo T, et al. National cancer incidence and mortality in China, 2012. Chin J Cancer Res 2016;28:1.
. Yang L, Zheng R, Wang N, et al. Incidence and mortality of stomach cancer in China, 2014. Chin J Cancer Res 2018;30:291–8.
. Jencks SF, Williams MV, Coleman EA. Rehospitalizations among patients in the Medicare fee-for-service program. N Engl J Med 2009;360:1418–28.
. Sellers MM, Merkow RP, Halverson A, et al. Validation of new readmission
data in the American College of Surgeons National Surgical Quality Improvement Program. J Am Coll Surg 2013;216:420–7.
. Hechenbleikner EM, Makary MA, Samarov DV, et al. Hospital readmission
by method of data collection. J Am Coll Surg 2013;216:1150–8.
. McCormack R, Michels R, Ramos N, et al. Thirty-day readmission
rates as a measure of quality: causes of readmission
after orthopedic surgeries and accuracy of administrative data. J Healthc Manag 2013;58:64–76. discussion 76-7.
. Glance LG, Kellermann AL, Osler TM, et al. Hospital readmission
after noncardiac surgery: the role of major complications. JAMA Surg 2014;149:439–45.
. Sivsammye S, Kailasam K. Comparison of demographic variables related to 30-day readmission
in cancers with similar risk factors
: analysis of 290,270 hospitalizations. J Clin Oncol 2017;35(15 suppl 1):
. Acher AW, Squires MH, Fields RC, et al. Readmission
following gastric cancer
resection: risk factors
and survival. J Gastrointest Surg 2016;20:1284–94.
. Ahmad R, Schmidt BH, Rattner DW, et al. Factors influencing readmission
after curative gastrectomy for gastric cancer
. J Am Coll Surg 2014;218:1215–22.
. Ammori JB, Navale S, Schiltz N, et al. Predictors of 30-day readmissions after gastrectomy for malignancy. J Surg Res 2018;224:176–84.
. Asaoka R, Kawamura T, Makuuchi R, et al. Risk factors
for 30-day hospital readmission
after radical gastrectomy: a single-center retrospective study. Gastric Cancer
2018;1–8. doi: 10.1007/s10120-018-0856-4. [Epub ahead of print].
. Xiao H, Quan H, Pan S, et al. Incidence, causes and risk factors
for 30-day readmission
after radical gastrectomy for gastric cancer
: a retrospective study of 2,023 patients. Sci Rep 2018;8:10582.
. Zhuang CL, Wang SL, Huang DD, et al. Risk factors
for hospital readmission
after radical gastrectomy for gastric cancer
: a prospective study. PLoS One 2015;10:e0125572.
. Chang DC, Noorbakhsh A, Mullen J. Analysis of early and late readmission
after gastrectomy to index and nonindex hospitals. J Am Coll Surg 2015;221:122.
. Kim MC, Kim KH, Jung GJ. A 5 year analysis of readmissions after radical subtotal gastrectomy for early gastric cancer
. Ann Surg Oncol 2012;19:2459–64.
. Fang QG, Shi S, Zhang X, et al. Upper extremity morbidity after radial forearm flap harvest: a prospective study. J Int Med Res 2014;42:231–5.
. Kwaan MR, Vogler SA, Sun MY, et al. Readmission
after colorectal surgery is related to preoperative clinical conditions and major complications. Dis Colon Rectum 2013;56:1087–92.
. Sutton JM, Wima K, Wilson GC, et al. Factors associated with 30-day readmission
after restorative proctocolectomy with IPAA: a national study. Dis Colon Rectum 2014;57:1371–8.
. Kulaylat AN, Dillon PW, Hollenbeak CS, et al. Determinants of 30-d readmission
after colectomy. J Surg Res 2015;193:528–35.
. Stang A. Critical evaluation of the Newcastle-Ottawa scale for the assessment of the quality of nonrandomized studies in meta-analyses. Eur J Epidemiol 2010;25:603–5.
. Higgins JE. Cochrane handbook for systematic reviews of interventions. Naunyn-Schmiedebergs Archiv für experimentelle Pathologie und Pharmakologie 2011;5:S38.
. Hozo SP, Djulbegovic B, Hozo I. Estimating the mean and variance from the median, range, and the size of a sample. BMC Med Res Methodol 2005;5:13.
. Choe YR, Joh JY, Kim YP. Association between frailty and readmission
within one year after gastrectomy in older patients with gastric cancer
. J Geriatr Oncol 2017;8:185–9.
. Merchant SJ, Ituarte PH, Choi A, et al. Hospital readmission
following surgery for gastric cancer
: frequency, timing, etiologies, and survival. J Gastrointest Surg 2015;19:1769–81.
. Lawson EH, Hall BL, Louie R, et al. Association between occurrence of a postoperative complication and readmission
: implications for quality improvement and cost savings. Ann Surg 2013;258:10–8.
. Lawson EH, Hall BL, Louie R, et al. Identification of modifiable factors for reducing readmission
after colectomy: a national analysis. Surgery 2014;155:754–66.
. Zhang JQ, Curran T, McCallum JC, et al. Risk factors
after lower extremity bypass in the American College of Surgeons National Surgery Quality Improvement Program. J Vasc Surg 2014;59:1331–9.
. Damle RN, Alavi K. Risk factors
for 30-d readmission
after colorectal surgery: a systematic review. J Surg Res 2016;200:200–7.
. Park P, Nerenz DR, Aleem IS, et al. Risk factors
associated with 90-day readmissions after degenerative lumbar fusion: an examination of the Michigan Spine Surgery Improvement Collaborative (MSSIC) Registry. Neurosurgery 2018;doi: 10.1093/neuros/nyy358.
. Kelly KN, Iannuzzi JC, Rickles AS, et al. Risk factors
associated with 30-day postoperative readmissions in major gastrointestinal resections. J Gastrointest Surg 2014;18:35–43. discussion 43-34.
. Hu Y, Huang C, Sun Y, et al. Morbidity and mortality of laparoscopic versus open D2 distal gastrectomy for advanced gastric cancer
: a randomized controlled trial. J Clin Oncol 2016;34:1350–7.
. Etoh T, Honda M, Kumamaru H, et al. Morbidity and mortality from a propensity score-matched, prospective cohort study of laparoscopic versus open total gastrectomy for gastric cancer
: data from a nationwide web-based database. Surg Endosc 2018;32:2766–73.
. Kodera Y, Yoshida K, Kumamaru H, et al. Introducing laparoscopic total gastrectomy for gastric cancer
in general practice: a retrospective cohort study based on a nationwide registry database in Japan. Gastric Cancer
. Chen K, Pan Y, Zhang B, et al. Robotic versus laparoscopic Gastrectomy for gastric cancer
: a systematic review and updated meta-analysis. BMC Surg 2017;17:93.
. Guerra F, Giuliani G, Iacobone M, et al. Pancreas-related complications following gastrectomy: systematic review and meta-analysis of open versus minimally invasive surgery. Surg Endosc 2017;31:4346–56.
. Yang SY, Roh KH, Kim YN, et al. Surgical outcomes after open, laparoscopic, and robotic gastrectomy for gastric cancer
. Ann Surg Oncol 2017;24:1770–7.
Keywords:Copyright © 2019 The Authors. Published by Wolters Kluwer Health, Inc. All rights reserved.
gastric cancer; operation; readmission; risk factors