From January 2012 to December 2015, 720 patients underwent LADG with Billroth II anastosmosis or LAPPG for cT1N0 gastric cancer in the National Cancer Center, Korea. Among these patients, the following were excluded in the analysis; 309 patients whose primary tumor was located less than 5 cm from the pylorus, 9 patients who had multiple gastric cancers, 92 patients who received adjuvant chemotherapy because their postoperative pathological stages were stage II or III; 13 patients who had some other history of cancer before and after the gastrectomy; and 1 patient due to follow-up loss.

LAPPG was performed by four surgeons that were experienced in LADG (EBW, YHM, RKW, and KYW). Infrapyloric vessels were routinely preserved to maintain blood supply to the pyloric cuff, and the right gastric artery with lymph node station No. 5 was also preserved and dissected distally to the first branch of the right gastric artery. The hepatic and pyloric branches of the vagus nerves were preserved, while the celiac branch was generally not preserved. The extent of lymph node dissection was D1+ or more according to the treatment guidelines of the Japanese Gastric Cancer Association[15]. D1+ in the context of PPG indicates the lymph node station numbers 1, 3, 4sb, 4d, 6, 7, 8a, and 9.

After resection was completed, a short 4- to 5-cm midline incision was made, and the tumor location was checked by palpation of the proximal and distal clips. A 3- to 5-cm pyloric cuff remained after the resection of the distal portion, and the gastrogastrostomy was performed by a hand-sewn suture. In LADG, the laparoscopic procedures were performed the same as those used in LAPPG, except for the dissection of the No. 5 and 6 lymph nodes and the vagus nerve. After the procedures, a gastrojejunal anastomosis (Billroth II) was performed extracorporeally through the same incision that was used for LAPPG.

Comorbidity was evaluated using the American Society of Anesthesiologists (ASA) physical status classification system[16]. Histological types were classified according to the 2010 World Health Organization classification[17]. When a tumor consisted of components of two or more histological types, the quantitative predominance was recorded as the histological type. The pathological stage was categorized according to the 8^th American Joint Committee on Tumor-Node-Metastasis classification system[18]. Postoperative symptom complications were evaluated using the Clavien-Dindo classification system within 1 month after surgery[19].

After surgery, the patients visited the outpatient clinic every 6 mo. Body weight, serum hemoglobin, protein, and albumin were checked during this visit and analyzed as nutritional outcomes. Patients with anemia were provided with iron supplementation at the outpatient clinic depending on patient symptoms, hemoglobin levels, and the discretion of the physician. In general, oral iron was administered by 80 mg of ferrous sulfate once or twice per day for a period of 3 or 6 mo. Intravenous iron was typically administered as a single dose of ferric carboxymaltose (500 mg). An esophagogastroduodenoscopy was performed annually, and the patient was evaluated for the presence of bile reflux and the grade of residual food according to the following criteria; no food residue, liquid only, soft diet residue, and nearly normal diet residue.

Postoperative QOL was estimated using the European Organization for Research and Treatment of Cancer (EORTC) QOL Questionnaire (QLQ) -C30 and the gastric cancer-specific module, STO22[20]. The EORTC QLQ-C30 is composed of a global health status/QOL scale, 5 functional scales and 9 symptom scales. The EORTC QLQ-STO22 is composed of 9 symptom scales. Each scale is represented by a score ranging from 0 to 100. A higher score indicates a better QOL as defined by the global health status and functional scales of the EORTC QLQ-C30, while a higher score indicates a poorer QOL on the symptom scale of the EORTC QLQ-C30 and STO22[21].

The QOL survey was performed between October 2016 and December 2018 for patients who underwent surgeries at least 2 years prior and visited the outpatient clinic. The period between surgery and the day that the questionnaire was administered varied, ranging from 2 to 5 years postoperatively.

The continuous variables are shown as the means ± standard deviations or the medians with interquartile ranges, and the categorical variables are presented as proportions. Differences between these groups were tested using a t-test or the Wilcoxon rank-sum test for continuous variables and the chi –square test or Fisher’s exact test for categorical variables. A mixed effect model was performed to analyze changes of the nutritional outcomes between the two groups. In the QOL analysis, each subscale or item is presented as the median and the interquartile range. The distribution of QOL scores did not follow a normal distribution. Therefore, nonparametric statistics (i.e., the Willcoxon rank-sum test) were used to evaluate their statistical significance. Data analyses were conducted using SAS version 9.4 (SAS Institute Inc., Cary, NC, United States). P values less than 0.05 were considered significant.

Among the 720 patients, 195 patients with LADG and 101 patients with LAPPG were ultimately included in this study (Supplementary Figures 1 ). There were no significant differences in baseline demographics, including age, sex, body mass index, and ASA classification (Table 1). The pathological results showed that the distal margin was shorter, and there were less harvested lymph nodes in the LAPPG group when compared to the LADG groups (P < 0.001 and P = 0.046, respectively). The operative time was longer in the LAPPG group (median, 150 min vs 210 min, P < 0.001), while the estimated blood loss and the length of hospital stay were not significantly different between the two groups.

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Figure 1 Postoperative nutritional outcomes. A: Change in hemoglobin; B: Change in serum protein levels; C: Change in serum albumin levels; D: Change in body weight. LADG: Laparoscopy-assisted distal gastrectomy; LAPPG: Laparoscopy-assisted pylorus-preserving gastrectomy. ^aP < 0.05.

The incidence of overall early complications was not significantly different between the LADG and LAPPG groups (Table 2). There were also no significant differences in any of the severity grades of the Clavien-Dindo classification. However, the incidence of delayed gastric emptying was higher in the LAPPG group (P = 0.001). Four patients with grade III delayed gastric emptying were treated with endoscopic Botox injections, after which they improved[22].

Figure 1 shows the comparison of long-term nutritional outcomes between the LADG and LAPPG groups. In the LAPPG group, hemoglobin levels gradually increased and had almost recovered by postoperative year 5. However, decreased hemoglobin levels persisted in the LADG group. Hemoglobin levels were significantly higher in the LAPPG group than in the LADG group (P < 0.001). Iron supplementation in the outpatient clinic was also evaluated; the proportions of patients who were administered any iron supplement were similar between the two groups (22.1% vs 19.8%, P = 0.765) (Table S1).

Serum protein decreased after surgery but increased after 1-2 years postoperatively in both groups. Serum albumin continuously decreased after surgery. There were no significant differences in the changes of serum protein and albumin level between the two groups (P = 0.083 and 0.304, respectively). After surgery, a loss of body weight of approximately 5-6 kg was observed in both groups, and the decreased body weight persisted in the follow-up period. There were no significant differences in the changes in body weight between the two groups (P = 0.092).

Figure 2 shows the proportions of the presence of bile reflux and residual food. After surgery, bile reflux was observed in 30%-60% of the LADG group, and in less than 10% of the LAPPG group (P < 0.001 at every time point). In the LAPPG group, 65% of patients had a nearly normal diet residue at 1 year postoperatively, and the proportion decreased slightly to 45% at 5 years postoperatively. In contrast, less than 10% of the LADG group had a nearly normal diet residue postoperatively. The proportions of residual food were significantly different between the two groups at every time point (P < 0.001).

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Figure 2 Postoperative endoscopic findings. A: Proportions of the presence of bile reflux; B: Proportions of the grade of residual food. ^aP < 0.05.

A total of 108 (55.3%) and 61 (60.4%) patients in the LADG and LAPPG groups answered the QOL questionnaire, respectively, and the time points for the responses to the QOL questionnaire ranged from 2 years to 5 years (Table S2). For the EORTC QLQ-C30, the LAPPG group had better physical function when compared to the LADG group (86.7 vs 90.0, P = 0.032) (Table 3). For the EORTC QLQ-STO22, the pain and reflux score were significantly higher in the LAPPG group than in the LADG group (8.3 vs 16.7 in pain, 11.1 (interquartile range, 0, 22.2) vs 11.1 (interquartile range, 11.1, 33.3) in reflux, P = 0.034 and 0.001, respectively). Other functional and symptom scales/items did not show any differences.

Laparoscopy-assisted pylorus-preserving gastrectomy (LAPPG) was known to have benefits of function-preserving surgery compared to laparoscopy-assisted distal gastrectomy (LADG). However, in clinical settings, delayed gastric emptying and esophageal reflux following LAPPG can be serious issues, making surgeons reluctant to perform LAPPG.

It is unclear that LAPPG had better long-term functional outcomes and quality of life compared to LADG.

To evaluate the long-term functional outcomes and patient-reported quality of life of LAPPG compared to those of LADG with Billroth II anastomosis.

We reviewed the clinicopathological data of 195 patients who underwent LADG with Billroth II anastomosis and 101 patients who underwent LAPPG for cT1N0 gastric cancer in the middle third of the stomach between 2012 and 2015. Postoperative complications, nutritional parameters, and survey results of the EORTC QLQ C30 and STO22 questionnaire were compared between the two groups.

The serum hemoglobin level was significantly higher in the LAPPG group than in the LADG group (P < 0.001). In the endoscopic findings, incidence of bile reflux was lower (P < 0.001); however, the incidence of residual food was higher in the LAPPG group than in the LADG group (P < 0.001). Regarding the quality of life score, the LAPPG group had a better physical functioning score (86.7 vs 90.0, P = 0.032) but also greater pain and reflux when compared to the LADG group (8.3 vs 16.7 in pain, 11.1 (interquartile range, 0, 22.2) vs 11.1 (interquartile range, 11.1, 33.3) in reflux, P = 0.034 and 0.001, respectively).

LAPPG is beneficial to recovery of anemia and to bile reflux, however, it might be unfavorable in terms of pain and reflux symptoms compared to LADG with Billroth II anastomosis.

LAPPG has both advantages and disadvantages in reference to long-term functional outcomes. When a physician informs all possible advantages and disadvantages to a patient, and the patient wants to undergo LAPPG, LAPPG could be a treatment option for middle third early gastric cancer. Additional large-scale study is needed to determine the functional superiority of LAPPG and patient-reported QOL.