Published online Oct 10, 2023.
https://doi.org/10.5230/jgc.2023.23.e35
Long-term Functional and Patient-reported Outcomes Between Intra-corporeal Delta-shaped Gastroduodenostomy and Gastrojejunostomy After Laparoscopic Distal Gastrectomy
Abstract
Purpose
This study aimed to compare the long-term functional and patient-reported outcomes between intra-corporeal delta-shaped gastroduodenostomy and gastrojejunostomy after laparoscopic distal gastrectomy for gastric cancer.
Materials and Methods
We retrospectively reviewed clinicopathological data from 616 patients who had undergone laparoscopic distal gastrectomy for stage I gastric cancer between January 2015 and September 2020. Among them, 232 patients who had undergone delta-shaped anastomosis and another 232 who had undergone Billroth II anastomosis were matched using propensity scores. Confounding variables included age, sex, body mass index, physical status classification, tumor location, and T classification. Postoperative complications, nutritional outcomes, endoscopic findings, and quality of life (QoL) were compared between the 2 groups.
Results
No significant differences in postoperative complications or nutritional parameters between the two groups were observed. Annual endoscopic findings revealed more residual food and less bile reflux in the delta group (P<0.001) than in the Billroth II group. Changes of QoL were significantly different regarding emotional function, insomnia, diarrhea, reflux symptoms, and dry mouth (P=0.007, P=0.002, P=0.013, P=0.001, and P=0.03, respectively). Among them, the delta group had worse insomnia, reflux symptoms, and dry mouth within three months postoperatively.
Conclusions
Long-term nutritional outcomes and QoL were comparable between the delta and Billroth II groups. However, more residual food and worse short-term QoL regarding insomnia, reflux symptoms, and dry mouth were observed in the delta group. Longer fasting time before endoscopic evaluation and short-term symptom management would have been helpful for the delta group.
INTRODUCTION
Laparoscopic distal gastrectomy is a well-established procedure for both early and advanced gastric cancer [1, 2, 3]. In Korea, the proportion of laparoscopic approaches for gastric cancer was 64.9% in 2019 and continues to increase [4, 5]. In the early period of laparoscopy, extra-corporeal anastomosis was commonly performed after gastrectomy. However, as surgical techniques have advanced and surgeons have gained more experience, intra-corporeal anastomosis has become popular. In a Korean nationwide survey, the proportion of intra-corporeal anastomosis was 84.9% among all laparoscopic gastrectomy cases in 2019 [5].
Three types of reconstruction after distal gastrectomy are common: Billroth I, Billroth II, and Roux-en-Y anastomoses. Billroth I is a popular method, because it preserves the physiological continuity of the gastrointestinal tract and requires a single anastomosis. For intra-corporeal Billroth I anastomosis, delta-shaped anastomosis was introduced by Kanaya et al. [6] in 2002 and is currently being used more frequently. In contrast to conventional Billroth I anastomosis, which is performed using a circular stapler, linear staplers are used in delta-shaped anastomosis.
Delta-shaped anastomosis has advantages such as the absence of mini-laparotomy, and less blood loss and pain compared to the same events associated with extra-corporeal Billroth I anastomosis [7]. However, it is also associated with several complications, including duodenal traction in the ventrodorsal direction, potential deterioration of the duodenal vascularity to ensure sufficient space around the duodenum, and difficulty in the cooperation between the surgeon and assistants [8]. Moreover, suitably sized remnant stomach and duodenum must be ensured for appropriate anastomotic tension. Numerous studies have reported the safety and feasibility of delta-shaped anastomosis [7, 9]. However, only a few studies have evaluated the long-term nutritional and patient-reported outcomes associated with delta-shaped anastomosis [10, 11].
In this study, we evaluated the long-term outcomes of patients who had undergone delta-shaped anastomosis compared with those of patients who had undergone Billroth II anastomosis, which are the most common anastomotic methods after distal gastrectomy in Korea [5]. Postoperative complications; long-term functional outcomes, including nutritional parameters and endoscopic findings; and patient-reported outcomes were assessed. Additionally, propensity score matching (PSM) was used to minimize selection bias.
MATERIALS AND METHODS
Patients
Medical records from 616 patients who had undergone delta-shaped or Billroth II anastomosis after total laparoscopic distal gastrectomy for pathological stage I gastric cancer at the National Cancer Center, Korea between January 2015 and September 2020 were retrospectively reviewed. Patients diagnosed with pathological stage II or higher gastric cancer were excluded, because adjuvant chemotherapy may affect postoperative nutritional status and quality of life (QoL). The anastomotic method is usually selected according to the surgeon’s preference. However, in case of history of duodenal ulcer, duodenal adhesion, pyloric cancer, or short duodenal bulb, surgeons are highly likely to perform Billroth II anastomosis.
This study was approved by the Institutional Review Board at the National Cancer Center, the Republic of Korea (No. NCC 2022-0023), which waived the requirement for patient informed consents because of the retrospective design of the study.
Delta-shaped anastomosis
After dissection of the infrapyloric and suprapyloric lymph nodes, the duodenal bulb was transected close to the pylorus, using a linear stapler [6]. Two-thirds of the stomach were divided, and small incisions were created along the edges of the remnant stomach and duodenum. The posterior walls of the remnant stomach and duodenum were approximated and stapled with a 45 mm linear stapler. Side-to-side anastomosis was performed, and the entry hole was closed using a 60 mm linear stapler.
Billroth II anastomosis
After two-thirds of the stomach were divided, a small incision was made in the greater curvature of the remnant stomach. The proximal jejunum was identified 20 cm distal of the ligament of Treitz and small incisions were made on the anti-mesenteric side. Stapling was performed with a linear stapler that was inserted into the small incisions of the remnant stomach and jejunum. The stapler entry hole was closed using barbed sutures. Braun anastomosis was not routinely performed after Billroth II anastomosis.
Clinicopathological evaluation
Histological types were classified according to the World Health Organization classification in two categories: differentiated, which includes papillary, well-differentiated, and moderately differentiated tubular adenocarcinoma and undifferentiated, which includes poorly differentiated tubular adenocarcinoma, poorly cohesive carcinoma (signet ring cell carcinoma), and mucinous adenocarcinoma [12, 13]. The tumor stages were classified according to the 8th edition of the American Joint Committee on Cancer and the Union for International Cancer Control guidelines [14]. Postoperative complications were graded using the Clavien–Dindo classification [15].
Postoperative follow-up
Postoperatively, patients visited the outpatient clinic at 3 and 12 months postoperatively and every 6 months thereafter. Body weight, serum hemoglobin, and albumin levels were examined at each visit, while ferritin and vitamin B12 levels were estimated annually.
Annual endoscopic evaluations were performed to assess the presence of bile reflux, residual food, and reflux esophagitis. Bile reflux was defined as the presence or absence of bile in the remnant stomach. The amount of residual food was classified into four grades: no residual food, liquid only, soft diet residue, and nearly normal diet. Reflux esophagitis was evaluated according to the Los Angeles (LA) classification [16]: Normal; LA grade A, one or several erosions limited to the mucosal folds and no larger than 5 mm in size; LA grade B, one or several erosions limited to the mucosal folds and larger than 5 mm in size; LA grade C, erosion extending over the mucosal folds, but less than three-quarters of the circumference; and LA grade D, confluent erosions extending over more than 3-quarters of the circumference. The presence of reflux esophagitis indicated LA grade A or higher lesions.
QoL assessment
The QoL was assessed preoperatively and at 1, 3, 12, 18, 24, 30, and 36 months postoperatively using the European Organization for Research and Treatment of Cancer Quality of Life Questionnaire Core 30 (EORTC QLQ-C30) and STO22 [17, 18]. The EORTC QLQ-C30 comprises of one global health status, five functional scales (physical, role, emotional, cognitive, and social), and nine general symptom scales (fatigue, nausea and vomiting, pain, dyspnea, insomnia, appetite loss, constipation, diarrhea, and financial difficulties). The EORTC QLQ-STO22 comprises of nine stomach-specific symptom scales. Scores were converted to a 0–100 scale, according to the EORTC scoring manual. Higher global health status and functional scale scores indicated better QoL or functions. Conversely, high symptom scale scores on the EORTC QLQ C30 and STO22 represented severe symptoms.
Statistical analysis
Continuous variables were presented as means with standard deviations and categorical variables were presented as numbers with percentages. Statistical differences between the two groups were analyzed using a Student’s t-test for continuous variables and the χ2 test or Fisher’s exact test for categorical variables.
Baseline clinicopathological characteristics were not balanced between patients, who had undergone delta-shaped anastomosis and those who had undergone Billroth II anastomosis. Thus, we conducted PSM analyses to minimize potential selection bias [19]. PSM was estimated using a multivariable logistic regression model. Potential confounding covariates included age, sex, body mass index (BMI), American Society of Anesthesiologists physical status classification, tumor location, and pathological T classification. A 1:1 nearest-neighbor matching was used with a caliper of 0.1 without replacement.
Nutritional and QoL outcomes were analyzed using a linear mixed model for repeated measures to compare changes from baseline over time between the two groups. Least-squares means and standard errors of each subscale were estimated with a first-order autoregressive covariance structure using visit, group, and visit-by-group interactions as fixed effects and adjustment for baseline values.
All data were analyzed using SAS version 9.4 (SAS Institute Inc., Cary, NC) and R version 4.2.1 (R Foundation for Statistical Computing, Vienna, Austria). P-values less than 0.05 were considered statistically significant.
RESULTS
Baseline clinicopathological characteristics
This study included 273 patients who had undergone delta-shaped anastomosis (delta group) and 343 who had undergone Billroth II anastomosis (Billroth II group). Baseline clinicopathological factors, including BMI, tumor location, histological type, and pathological T category were significantly different (Table 1). After PSM of 232 pairs, no significant difference in the clinicopathological characteristics was observed between the 2 groups.
Table 1
Clinicopathological characteristics of patients before and after propensity score matching
Surgical outcomes in PSM patients
The proportion of D2 lymph node dissections was higher in the Billroth II group than in the delta group (24.6 vs. 4.7%, P<0.001) (Table 2). The delta group was characterized by longer operating time (186.8 vs. 161.5 minutes, P<0.001) and less blood loss (32.2 vs. 54. 2 mL, P<0.001). However, the overall incidence of complications, type of complications, or severity grade did not differ significantly between the two groups. Patients who experienced delayed gastric emptying (n=13) and anastomotic ischemia (n=2) were treated with supportive care without additional interventions. One patient who had undergone Billroth II anastomosis died of septic shock due to internal herniation and mesenteric infarction one year postoperatively.
Table 2
Surgical outcomes in propensity score-matched patients
Nutritional outcomes in PSM patients
Nutritional parameters were assessed at baseline and 3, 12, 24, and 36 months postoperatively. Data on body weight, hemoglobin, and albumin were collected from all matched patients. However, baseline ferritin and vitamin B12 levels were assessed in just 194 patients (164 and 88 patients in the delta group and the Billroth II group, respectively). Fig. 1 shows the changes in each nutritional parameter from baseline. Body weight and hemoglobin decreased by approximately 4–5 kg and 1 g/dL, respectively, at three months postoperatively and was maintained for the following 3 years. Serum albumin decreased by approximately 0.2 g/dL and gradually increased until 36 months postoperatively. Serum ferritin and vitamin B12 levels also decreased by approximately 40–60 ng/dL and 40–130 pg/mL, respectively, 24 months postoperatively, and did not recover until 36 months postoperatively. No significant differences in any of the nutritional parameters between the delta and Billroth II groups (P=0.281, P=0.51, P=0.209, P=0.679, and P=0.729 for body weight, hemoglobin, albumin, ferritin, and vitamin B12, respectively) were observed.
Fig. 1
Postoperative nutritional parameters. (A) Change in body weight (kg), (B) Change in serum hemoglobin (g/dL), (C) Change in serum albumin (g/dL), (D) Change in serum ferritin (μg/L), and (E) Change in serum vitamin B12 (pg/mL).
Endoscopic findings in PSM patients
Data on endoscopic findings were collected from 455 (98.0%), 411 (88.6%), and 306 (65.9%) patients at 1, 2, and 3 years postoperatively, respectively. The delta group had a significantly higher incidence of residual food than that of the Billroth II group (P<0.001, P<0.001, and P=0.002 at 1, 2, and 3 years postoperatively, respectively) (Fig. 2A). Residual food was observed in approximately half of the patients in the delta group at 1 year postoperatively and the proportion decreased to 35.5% at 3 years. In contrast, less than 20% of the patients in the Billroth II group had residual food at all time points.
Fig. 2
Endoscopic findings in propensity score-matched patients. Graph showing the proportion of patients with (A) residual food, (B) bile reflux, and (C) presence of reflux esophagitis (LA-A or higher).
The incidence of bile reflux was significantly lower in the delta group than in the Billroth II group (26.9%–44.8%, vs. 11.0%–13.8%, P<0001) (Fig. 2B). The proportion of the patients with reflux esophagitis (LA-A or higher) was not different between the two groups (0.4%–1.4% and 0.6%–3% in the delta and Billroth II groups, respectively) (Fig. 2C).
QoL in PSM patients
The response rates to QoL questionnaire were 100%, 65.3%, 38.3%, 67.5%, 54.1%, 54.3%, 40.3%, and 36.0% at baseline and 1, 3, 12, 18, 24, 30, and 36 months postoperatively, respectively. Among the subscales of the EORTC QLQ-C30, significant differences were observed in emotional function, insomnia, and diarrhea (P = 0.007, 0.022, and 0.013, respectively) (Fig. 3A-C). The delta group had better emotional function at 18 months postoperatively. The insomnia score of the delta group was significantly higher at one month postoperatively, indicating severe symptoms, which subsequently decreased. The diarrhea score in the delta group was also significantly higher at 18 months postoperatively, and subsequently decreased. No significant differences were observed in other subscales (Supplementary Fig. 1).
Fig. 3
Quality of life in propensity score-matched patients. (A) Emotional function, (B) Insomnia, (C) Diarrhea, (D) Reflux symptoms, and (E) Dry mouth.
*P<0.05.
Among the subscales of the EORTC QLQ-STO22, significant differences were observed in reflux symptoms and dry mouth (P=0.001 and P=0.03, respectively) (Fig. 3D and E). The reflux symptoms score in the delta group was higher at one month postoperatively and subsequently comparable to that of the Billroth II group. The dry mouth score in the delta group was also higher at three months postoperatively and subsequently decreased. No significant differences were observed in other subscales (Supplementary Fig. 2).
DISCUSSION
In this study, we evaluated the long-term surgical outcomes, including postoperative complications, nutritional and patient-reported outcomes, in patients who underwent either delta-shaped or Billroth II anastomosis following laparoscopic distal gastrectomy. No significant differences were observed in postoperative complications, long-term nutritional outcomes, or QoL between the two groups. However, the delta group had a higher incidence of residual food during a period of three years postoperatively and worse insomnia, reflux symptoms, and dry mouth in the immediate postoperative period (up to 3 months).
Many studies have evaluated the long-term functional outcomes after distal gastrectomy. In a recent meta-analysis, eight randomized controlled trials comparing outcomes between Billroth I, Billroth II, and Roux-en-Y anastomosis were analyzed [20]. Most studies identified a comparable incidence of overall complications, nutritional outcomes, and QoL between Billroth I and Roux-en-Y anastomoses [21, 22, 23, 24, 25]. However, the Billroth I group had a higher frequency of remnant gastritis and bile reflux in postoperative endoscopic examinations than those observed in the Roux-en-Y group. Several retrospective studies also demonstrated similar results, including comparable complication rates and nutritional outcomes and higher frequency of residual food and bile reflux in the Billroth I or II groups compared to those associated with the Roux-en-Y group [26, 27]. In these studies, Billroth I anastomosis was performed via open or laparoscopy-assisted approaches using hand-sewing sutures or circular staplers. However, linear staplers are used in delta-shaped anastomosis, and studies that examine the long-term outcomes of delta-shaped anastomosis are lacking.
Studies on delta-shaped anastomoses have focused on short-term outcomes [9]. In these studies, the delta group had better short-term outcomes in terms of operating time, blood loss, time to oral intake, hospital stay, and postoperative complications than the same parameters associated with extra-corporeal Billroth I anastomosis. Only a few studies analyzed long-term functional outcomes with postoperative endoscopic findings and showed that the delta group had a higher incidence of bile reflux or reflux esophagitis than those observed in the Roux-en-Y group [8, 28]. Regarding long-term patient-reported outcomes, very few studies have compared outcomes between delta-shaped and extra-corporeal anastomoses, and no study has compared the long-term QoL between delta and other anastomoses [11]. This is the first study that compares long-term functional and patient-reported outcomes between patients who underwent delta-shaped and Billroth II anastomoses.
The most notable finding of this study was the higher grade of residual food in the delta group. On postoperative endoscopic evaluation, the proportion of patients having residual food was significantly higher in the delta group compared to that in the Billroth II group. Regarding this delayed passage, Kanaya et al. [29] mentioned that stasis may have been the consequence of duodenal twisting at the site of the delta-shaped anastomosis. Anastomotic twisted alignment interrupts food passage, which results in high grade of residual food. Another study group reported some cases of re-hospitalization after delta-shaped anastomosis due to obstructive symptoms [28]. These patients had edema and panniculitis at the anastomosis site, similarly to our experience of patients with obstruction after delta-shaped anastomosis. Transient edematous narrowing at the anastomosis site is associated with impaired circulation and excessive dissection of the duodenal tissue. Additionally, high food intake may affect food stasis. One study showed a significantly higher amount of food intake in the delta anastomosis group than in the conventional Billroth I group [10]. In delta-shaped anastomosis, the remaining part should be as large as possible to reduce traction tension. Larger remnant stomach and greater food intake may result in more food stasis [30].
Another important finding of this study was the worse QoL of the delta group observed at the initial postoperative period (no longer than three months). Many studies assessed QoL at six months postoperatively or later, without any significant difference between the Billroth I and Roux-en-Y groups [11, 22, 24, 31]. However, in this study, QoL questionnaires were administered at one and three months postoperatively, and significant differences were identified between the two groups. Higher reflux symptoms and insomnia in the delta group may be related to food stasis, and patients with anastomotic edema and food stasis are more likely to experience reflux symptoms. Worse diarrhea symptoms in the delta group were also reported in a previous study [32]. In that study, the Post Gastrectomy Syndrome Assessment Scale (PGSAS)-45 was assessed one month after surgery, and high frequency of diarrhea was observed in the delta group. A wide anastomotic lumen and straightforward alignment from the esophagus to the duodenum could be associated with diarrhea.
Recently, some assessment tools for evaluating postgastrectomy symptoms and QoL have been developed and used in several clinical studies. PGSAS-45 is a questionnaire for the assessment of living status and QoL in postgastrectomy patients, developed by the Japanese Postgastrectomy Syndrome Working Party [33]. KOQUSS-40 is also a symptom-focused QoL questionnaire, developed by the KOrean QUality of life in Stomach cancer patients Study group (KOQUSS) [34]. The validity and reliability of KOQUSS-40 were proven in a validation study. These questionnaires are expected to better evaluate postgastrectomy symptoms and QoL, because they were developed for patients who underwent gastrectomy. Further studies are required to determine whether these questionnaires can more sensitively evaluate postgastrectomy symptoms and QoL compared to the sensitivity of the EORTC QLQ.
No significant differences in nutritional outcomes were observed between the two groups in this study. Consistent with that, many studies reported no significant differences in nutritional outcomes among Billroth I, Billroth II, and Roux-en-Y anastomoses [21, 22, 23, 26]. Only a few studies reported less weight loss after Billroth I compared to those associated with other types of anastomoses [24, 27]. Therefore, the anastomosis method probably has little effect on nutritional outcomes.
The present study had several limitations. First, this study was retrospectively performed using a single-center database, and anastomoses were based on the surgeons’ preferences. Therefore, the proportion of surgeons that performed each type of anastomosis was not equal between the two groups, which might have affected the surgical outcomes. However, no significant difference in postoperative complications were observed between the two groups, and the differences of long-term functional outcomes might have been due to differences in anastomosis methods rather than differences in the surgeons’ skills. Second, a considerable amount of data on nutritional parameters, endoscopic findings, and QoL at each time point was missing. In particular, ferritin and vitamin B12 levels were assessed in just 42% of all matched patients, and QoL data were collected from 35.6%–67.9% of all matched patients. Therefore, the results of ferritin, vitamin B12, and QoL should be carefully interpreted considering the limited data. Third, residual food is highly affected by fasting time. In general, the longer the fasting time, the lesser the residual food. We have no data on patients’ fasting times before endoscopic evaluation, and residual food is not an absolute indicator for gastrointestinal motility function.
In conclusion, delta-shaped gastroduodenostomy and gastrojejunostomy had comparable postoperative complications, long-term nutritional status, and patient-reported outcomes. However, patients with delta-shaped anastomosis had more residual food with limited endoscopic evaluation and worse QoL in some subscales in the immediate postoperative period. For patients undergoing delta-shaped anastomosis, longer fasting time before endoscopic evaluation and symptom management during the initial postoperative period may be helpful.
SUPPLEMENTARY MATERIALS
European Organization for Research and Treatment of Cancer Quality of Life Questionnaire Core 30.Supplementary Fig. 1
European Organization for Research and Treatment of Cancer Quality of Life Questionnaire-STO22.Supplementary Fig. 2
Funding:This study was supported by the National Cancer Center, Republic of Korea, Grant No. 2310270.
Conflict of Interest:No potential conflict of interest relevant to this article was reported.
Author Contributions:
Data curation: P.S.H., Y.H.M., R.K.W., K.Y.W., E.B.W.
Formal analysis: Y.H.M., R.K.W., K.Y.W., H.M.
Funding acquisition: E.B.W.
Investigation: Y.H.M., R.K.W., K.Y.W.
Writing - original draft: P.S.H.
Writing - review & editing: E.B.W.
References
-
Information Committee of the Korean Gastric Cancer Association. Korean Gastric Cancer Association-led nationwide survey on surgically treated gastric cancers in 2019. J Gastric Cancer 2021;21:221–235.
-
-
Watanabe Y, Watanabe M, Suehara N, Saimura M, Mizuuchi Y, Nishihara K, et al. Billroth-I reconstruction using an overlap method in totally laparoscopic distal gastrectomy: propensity score matched cohort study of short- and long-term outcomes compared with Roux-en-Y reconstruction. Surg Endosc 2019;33:3990–4002.
-
-
Bosman FT, Carneiro F, Hruban RH, Theise ND. In: WHO Classification of Tumours of the Digestive System. WHO Classification of Tumours, 4th Edition. Volume 3. Geneva: World Health Organization; 2010.
-
-
Japanese Gastric Cancer Association. Japanese gastric cancer treatment guidelines 2018 (5th edition). Gastric Cancer 2021;24:1–21.
-
-
Brierley JD, Gospodarowicz MK, Wittekind C. In: TNM classification of Malignant Tumours. Hoboken (NJ): John Wiley & Sons; 2017.
-
-
D’Agostino RB Jr. Propensity score methods for bias reduction in the comparison of a treatment to a non-randomized control group. Stat Med 1998;17:2265–2281.
-
-
Nakada K, Ikeda M, Takahashi M, Kinami S, Yoshida M, Uenosono Y, et al. Characteristics and clinical relevance of Postgastrectomy Syndrome Assessment Scale (PGSAS)-45: newly developed integrated questionnaires for assessment of living status and quality of life in postgastrectomy patients. Gastric Cancer 2015;18:147–158.
-
