Abstract
Background: Body weight, especially lean body mass, significantly decreases after gastrectomy. Postoperative surgical complications are a major risk factor for changes in body weight and body composition after gastrectomy. However, the influence of postoperative surgical complications after gastrectomy on body weight and body composition changes remains unclear. Patients and Methods: This retrospective study examined patients who underwent curative surgery for gastric cancer between May 2010 and February 2017. Their body weight and composition were evaluated by a bioelectrical impedance analyzer within 1 week before surgery, and at 1 week, 1 month and 3 months after surgery. Patients were classified as those with surgical complications and those without. Results: Eight hundred and eighty-eight patients (156 in the group with complications and 732 in the group without) were entered in the present study. When comparing the two groups, the patients' background and surgical factors significantly differed, while the pathological findings were similar. The body weight losses at 1 week, 1 month, and 3 months after surgery were 3.8%, 7.0%, and 10.4%, respectively, in those with complications, and 3.3%, 5.6%, and 6.8%, respectively, in the group without, with p-values of 0.001, 0.002, and 0.001, respectively. The corresponding lean body mass losses were 3.7%, 6.5%, and 6.8%, and 3.2%, 4.2%, and 3.5%, respectively, with p-values of 0.001, 0.001, and 0.001, respectively. Conclusion: Decreases in body weight and lean body mass after gastrectomy were more serious in the patients with surgical complications than in those without. To maintain body weight and lean body mass in patients with surgical complications, additional care or treatments are needed.
Gastric cancer is the fourth most common human malignant disease and the second-most frequent cause of cancer-related death worldwide (1). Complete resection is essential for the cure of gastric cancer (2, 3). However, the surgical complication rate after gastrectomy with lymph node dissection has been reported to range from 15-30% (4-6). Previous studies have shown that the development of surgical complications increased the risk of poor overall survival and tumor recurrence in gastric cancer (7, 8).
Body composition changes are common problems after gastrectomy for gastric cancer (9, 10). Previous studies have shown that body composition changes reduced the nutritional status, postoperative quality of life, and compliance with adjuvant chemotherapy (11-13). Surgical complications after gastrectomy also affect postoperative body composition changes. Body composition changes after gastrectomy might be much more substantial and last longer in patients with postoperative surgical complications than in those without. If body composition changes after gastrectomy are indeed much more substantial in patients with postoperative surgical complications than in those without such complications, additional care or treatments might be needed. However, few reports have evaluated this issue.
The aim of the present study was to evaluate body composition changes after gastrectomy using a bioelectrical impedance analyzer and to compare the degree and duration of body composition changes between patients with postoperative surgical complications after gastrectomy and those without.
Comparison of patient background characteristics.
Patients and Methods
Patients. This was a retrospective cohort study. Patients' records were retrieved from a prospectively collected database of Kanagawa Cancer Center from May 2010 to February 2017. The inclusion criteria were as follows: curative gastrectomy with lymph node dissection for gastric cancer was performed as the primary treatment, R0 resection was achieved, no weight loss over 15% before surgery was experienced, and a body composition analysis was performed within 1 week before surgery, and at 1 week, 1 month and 3 months after surgery.
Surgical procedure. All patients underwent distal or total gastrectomy with nodal dissection for gastric cancer. In principle, D1 or D1 plus lymphadenectomy is indicated for cT1N0 tumors, and D2 is applied for cN+ or cT2-T4 tumors regardless of the approach. Spleen-preserving D2 total gastrectomy was permitted in this study.
Perioperative care. The patients received the enhanced recovery after surgery (ERAS) protocol after gastrectomy. The details of this protocol have been previously reported (14, 15). In brief, the patients were allowed to eat until midnight on the day before surgery and were required to drink a rehydration solution by 3 hours before surgery. The nasogastric tube was removed immediately after surgery. The oral intake was initiated on postoperative day (POD) 1, beginning with water and an oral nutritional supplement. The patients began to eat solid food on POD 2, starting with rice gruel and soft food on POD 3 and advancing in three steps to regular food intake on POD 7. The patients were discharged when they had achieved adequate pain relief and soft food intake and exhibited normal laboratory data on POD 7. No postoperative medications to increase appetite, bowel movement or nutrition supplement were used for patients in this study. Furthermore, in the present study, although all of the patients received the same aftercare, including a physical examination and laboratory tests, in the first 3 months after surgery at the outpatient clinic, the patients did not receive any oral nutrition supplements to help them avoid lean mass loss.
Body composition analysis. The segmental body composition was analyzed using a Tanita MC-190EM bioelectrical impedance analyzer (Tanita, Tokyo, Japan), which provides relative information regarding the amount of lean and fat tissue in the trunk area and each limb, as well as the overall body composition and hydration status. The body weight and composition were evaluated by a bioelectrical impedance analyzer within 1 week before surgery, and at 1 week, 1 month and 3 months after surgery.
Surgical and pathological outcomes after gastrectomy.
Evaluation of operative morbidity and mortality. Surgical and nonsurgical complications were assessed prospectively and classified according to the Clavien–Dindo classification (16). Operative mortality was defined as postoperative death from any cause within 30 days after surgery or during the same hospital stay.
Data evaluation, statistical analyses, and ethics. The values are expressed as the median and range. The statistical analyses were performed using the chi-square test or Wilcoxon's signed-rank test. A p-value of less than 0.05 was considered to indicate statistical significance. The SPSS software package (v12.0 J Win; SPSS, Chicago, IL, USA) was used for all statistical analyses. The R-category and extent of dissection were determined by the Japanese Classification of Gastric Carcinoma (17), third English edition and the Japanese Gastric Cancer Association guidelines (18). The study was approved by the Institutional Review Board of Kanagawa Cancer Center.
Results
Background characteristics. A total of 888 patients were eligible for the present study. The median age was 68 years (range=27-90 years). Five-hundred and ninety-five patients were male, and 293 were female. Seven hundred and forty-two patients were classified as not having any surgical complications and 156 as having surgical complications. The background characteristics of the patients are summarized in Table I. The median age was significantly higher, the American Society of Anesthesiology score significantly worse, and the incidence of male patients, hypertension, and smoking habit significantly higher in the group with complications than in the group without (p=0.002, p=0.026, p=0.036, and p=0.018, respectively). Furthermore, the preoperative total body weight and lean body mass were significantly higher in the group with complications (p=0.011 and p=0.010, respectively). The operative details and pathological findings are shown in Table II. The incidence of total gastrectomy was higher in the group with complications. The median blood loss and median operative time were also much greater in the group with complications (both p<0.001). The median length of hospital stay (LOS) was 8 days in the group without complications and 12 days in the group with, showing a significant difference (p=0.001).
Postoperative surgical complications. The details of the postoperative surgical complications are shown in Table III. The overall complication rate was 17.6% in the present study. Pancreatic fistula and anatomic leakage were the most frequently diagnosed complications of grade 2 or more severity. Among surgical complications of grade 3 or more, anatomic leakage and ileus were the most frequently diagnosed.
A comparison of changes in body weight after gastrectomy between the patients who had postoperative surgical complications and those who did not. Significantly different from the group without complications at *p<0.001 and #p=0.002.
Details of surgical complications after gastrectomy.
Body composition. The rate of loss of body weight for the whole cohort at 1 week, 1 month, and 3 months was 3.4% (range=14.6-7.2%), 6.1% (range=23.7-5.9%), and 8.3% (range=26.6-7.3%), respectively. Figure 1 shows a comparison of the loss of body weight between the groups with and without complications at 1 week to 3 months. Significant decreases were observed at 1 week to 3 months in the group with complications (p<0.001, p=0.002 and p<0.001, respectively).
A comparison of the changes of lean body mass after gastrectomy between the patients who had postoperative surgical complications and those who did not. *Significantly different from the group without complications at p<0.001.
The rates of loss of lean body mass for the whole cohort at 1 week, 1 month, and 3 months were 3.5% (range=27.0-26.1%), 4.8% (range=20.2-17.3%), and 4.9% (range=23.3-24.9%), respectively. Figure 2 shows a comparison of the loss of lean body mass between NC and C group at 1 week to 3 months. Significant differences were observed at 1 week to 3 months (p<0.001, p=0.001, and p<0.001, respectively).
Discussion
The aim of the present study was to compare the degree and duration of body composition changes between patients with and without surgical complications after gastrectomy. The major finding was that decreases in both the body weight and lean body mass after gastrectomy were significantly more serious in patients with surgical complications than in those without. Our results suggest that additional care or treatment might be needed to maintain lean body mass after gastrectomy in patients with surgical complications.
The drivers of loss of body weight and lean body mass are multifactorial, with systemic inflammation, physical inactivity, and a reduced nutrient intake all contributing. Once stresses due to surgery or surgical complications occur, immune cells produce cytokines that act as mediators of both immune and systemic responses to injury. Cytokines, such as interleukin 6, interleukin 1 and tumor necrosis factor, are synthesized from amino acids supplied by muscle catabolism. In addition, the response of skeletal muscle during critical illness is characterized by a rapid decrease in protein content and accelerated amino acid release (19). Hassen et al. demonstrated that negative associations existed between the skeletal muscles mass and systemic inflammatory response syndrome score after surgery in 33 major vascular surgery patients (20). In addition, Iida et al. reported that postoperative muscle weakness was associated with interleukin-6 production immediately after cardiac surgery in 154 consecutive patients who had undergone coronary artery bypass grafting (21). Therefore, surgical stress due to surgical complications might affect the loss of body weight and lean body mass after surgery. In addition, surgical complications are reported to increase the LOS. A previous study showed that lean body mass loss was associated with an increased LOS. In the present study, the median LOS in patients who had surgical complications after gastrectomy was also significantly longer than in those without such complications. Therefore, a longer LOS due to surgical complications might also affect the loss of body weight and lean body mass.
Many trials evaluated the effects of early nutritional support on postoperative body weight loss and postoperative lean body mass in patients with gastric cancer who underwent gastrectomy (22, 23). However, few have described any positive effects of early nutritional support on postoperative body composition changes after gastrectomy. One possible reason for this failure to show such effects might be that previous trials did not take into consideration the influence of postoperative surgical complications on postoperative body composition changes. For example, Ida et al. conducted a prospective randomized phase III trial that evaluated whether or not the perioperative administration of an eicosapentaenoic acid (EPA)-enriched supplement could prevent body weight loss after total gastrectomy for gastric cancer (22). Unfortunately, a standard diet with EPA-enriched immunonutrition did not help prevent body weight loss after total gastrectomy. In their study, about 15% patients with postoperative surgical complications were included in the analysis. In contrast, Hatao et al. investigated the effects of oral nutritional supplement administration on postoperative body weight loss in patients with gastric cancer who had undergone total or distal gastrectomy (23). They demonstrated that oral nutritional supplementation after total gastrectomy significantly prevented postoperative weight loss. In that study, patients who had postoperative surgical complications were excluded from the analysis. These previous findings suggest that postoperative surgical complications might have had some clinical influence on the outcomes. Therefore, postoperative surgical complications might need to be considered as a factor for stratification in future phase III trials evaluating the effects of nutritional treatment for gastric cancer.
Several limitations associated with the present study warrant mentioning. Firstly, the present study was a retrospective analysis performed at a single institution. The results need to be confirmed in another cohort or in a prospective multicenter study. Secondly, we failed to measure the total calorie intake, physical activity, or serum markers after surgery in the present study. The influence of calorie intake and physical activity on postoperative body composition changes was therefore unclear in the present study.
In conclusion, decreases in body weight and lean body mass after gastrectomy were more serious in the patients with surgical complications than in those without surgical complications. In order to maintain body weight and lean body mass among patients with surgical complications, additional care or treatments are needed
Acknowledgements
This work was supported, in part, by the non-governmental organization Kanagawa Standard Anti-cancer Therapy Support System. The authors express their sincere gratitude to Mrs. Natsumi Sato and Mrs. Rika Takahashi for their excellent data management in this study.
Footnotes
↵* These Authors contributed equally to this study.
Ethics Approval and Consent to Participate
The study was approved by the Institutional Review Board of Kanagawa Cancer Center. The study was conducted in accordance with the Declaration of Helsinki. All subjects signed consent forms.
Consent to Publish
The study does not involve any personal identifiable data.
Availability of Data and Materials
Data and materials are available to any researcher interested upon reasonable request to the corresponding author.
Competing Interests
The Authors declare no competing interests in association with the present study.
Funding
None.
- Received December 19, 2018.
- Revision received January 9, 2019.
- Accepted January 10, 2019.
- Copyright© 2019, International Institute of Anticancer Research (Dr. George J. Delinasios), All rights reserved
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