Proximal Gastrectomy Is Associated with Lower Incidence of Anemia and Vitamin B12 Deficiency Compared to Total Gastrectomy in Patients with Upper Gastric Cancer

Article information

Cancer Res Treat. 2025;57(1):174-185
Publication date (electronic) : 2024 July 3
doi : https://doi.org/10.4143/crt.2024.319
1Department of Surgery, Yonsei University College of Medicine, Seoul, Korea
2Department of Surgery, Ajou University School of Medicine, Suwon, Korea
Correspondence: Hyoung Il Kim, Department of Surgery, Yonsei University College of Medicine, 50-1 Yonsei-ro, Seodaemun-gu, Seoul 03722, Korea Tel: 82-2-2228-2100 Fax: 82-2-313-8289 E-mail: cairus@yuhs.ac
Received 2024 March 29; Accepted 2024 July 2.

Abstract

Purpose

Proximal gastrectomy is an alternative to total gastrectomy (TG) for early gastric cancer (EGC) treatment in the upper stomach. However, its benefits in terms of perioperative and long-term outcomes remain controversial. The aim of this study was to compare the perioperative, body compositional, nutritional, and survival outcomes of patients undergoing proximal gastrectomy with double-tract reconstruction (PG-DTR) and TG for pathological stage I gastric cancer in upper stomach.

Materials and Methods

The study included 506 patients who underwent gastrectomy for pathological stage I gastric cancer in the upper stomach between 2015 and 2019. Clinicopathological, perioperative, body compositional, nutritional, and survival outcomes were compared between the PG-DTR and TG groups.

Results

The PG-DTR and TG groups included 197 (38.9%) and 309 (61.1%) patients, respectively. The PG-DTR group had a lower rate of early complications (p=0.041), lower diagnosis rate of anemia and vitamin B12 deficiency (all p < 0.001), and lower replacement rate of iron and vitamin B12 compared to TG group (all p < 0.001). The PG-DTR group showed reduced incidence of sarcopenia at 6-months postoperatively, preserved higher amount of visceral fat after surgery (p=0.032 and p=0.040, respectively), and showed a higher hemoglobin level (p=0.007). Oncologic outcomes were comparable between the groups.

Conclusion

The PG-DTR for EGC located in the upper stomach offered advantages of fewer complications, lower incidence of anemia and vitamin B12 deficiency, less decrease in visceral fat volume, and similar survival compared to TG. Consequently, PG-DTR may be considered a superior alternative treatment option to TG.

Introduction

The global incidence of gastric cancer, specifically in the upper stomach, is on an upward trend, including in Asia [1]. Total gastrectomy (TG) is considered the standard surgical procedure for treating upper gastric cancer. However, in recent times, proximal gastrectomy has been considered an alternative, albeit weakly recommended, according to the gastric cancer treatment guidelines in Korea and Japan [1,2].

Patients who underwent proximal gastrectomy with double-tract reconstruction (PG-DTR) have been reported to exhibit comparable long-term oncologic and short-term postoperative outcomes, along with superior nutritional parameters, relative to those who underwent TG [3,4]. Recently, a multicenter randomized controlled study comparing PG-DTR with TG has also confirmed similar results [5]. However, there is a dearth of studies on the differences between PG-DTR and TG, such as a body composition analysis and risk factor analysis for anemia and vitamin B12 deficiency; furthermore, studies with long follow-up periods of > 3 years are lacking.

Therefore, in the present study, we aimed to explore the short-term, long-term, and nutritional impacts, including body compositional analysis, after PG-DTR as compared to TG, for early gastric cancer located in the upper body of the stomach.

Materials and Methods

1. Patients

A retrospective review was conducted on a prospective gastric cancer database, comprising patients who underwent curative gastrectomy from January 2015 to December 2019. This study included patients who underwent radical PG-DTR or TG for pathological stage I gastric cancer. Patients who underwent combined organ resection or lacked computed tomography (CT) scan data required for body composition analysis were excluded.

Clinicopathological characteristics and perioperative outcomes of patients were collated. Pathologic tumor stage was determined according to the 8th edition of the American Joint Committee on Cancer Staging [6]. Complications were defined as any deviation from the normal postoperative course and graded according to the Clavien-Dindo classification [7]. Major complications were defined as Clavien-Dindo grade III or higher complication. Complications occurring within 30 days after surgery were classified as early complication, while surgical complications developing after postoperative 30 days were classified as long-term surgical complications.

2. Surgery

Surgical procedures were conducted using open, laparoscopic, or robotic methods. In the open method, esophagojejunostomy of PG-DTR or TG involved anastomosis between the esophageal stump and the proximal jejunum using a circular stapler. For laparoscopic and robotic methods, detailed procedures for PG-DTR or TG, as previously described [4,8], were followed. Duodenal transection, esophageal transection, esophagojejunostomy, and jejunojejunostomy were performed in the same manner in both methods. After transection of the esophagus, the proximal jejunum was anastomosed to the esophageal stump with a linear stapler. The only difference between PG-DTR and TG was the extent of gastrectomy. For PG-DTR, the stomach was transected above the gastric angle and jejuno-gastrostomy was performed. All laparoscopic or robotic surgical procedures were performed intracorporeally in PG-DTR and TG.

3. Follow-up

Patients visited the outpatient clinic at every 3 months during the first year after surgery, and at every 6 months for the following 2 years, followed by annual visits thereafter. At each visit, body weight was measured, and blood tests were conducted to assess anemia and vitamin B12 deficiency. Additionally, patients underwent abdominopelvic CT scans every 6 months and esophagogastroduodenoscopy every year.

Recurrence was confirmed through various means, including endoscopic biopsy, surgery, or imaging studies, such as abdominopelvic CT, positron emission tomography, or whole-body bone scan.

4. Definitions of anemia and vitamin B12 deficiency and their respective replacement therapies

Anemia was defined as a hemoglobin level of < 13 g/dL in men and < 12 g/dL in women [9]. Patients that were diagnosed with or impending anemia were administered iron, if their serum ferritin levels were < 30 ng/mL [10]. Data on all iron supplements including hemonia, venoferrum, ferinject, feroba, bolgre, and monofer were collected regardless of the dose or duration. Vitamin B12 deficiency was defined as a serum vitamin B12 levels of < 200 pg/mL [11]. Upon confirmation of the diagnosis or impending vitamin B12 deficiency, either oral administration or intramuscular injection of vitamin B12 was carried out [12].

5. Body composition in abdominopelvic CT scan

Body compositional parameters, including visceral fat, subcutaneous fat, muscle volume, and abdominal circumference, were measured at the level of the 3rd lumbar vertebra (L3) on a CT image using commercially available imaging software (Aquarius Intuition version 4.4.12, TeraRecon Inc., San Mateo, CA). A radiologist measured total cross-sectional areas by applying Hounsfield unit thresholds of −29 to +150 for skeletal muscle, −190 to −30 for subcutaneous fat, and −50 to −150 for visceral fat [13]. Skeletal muscle index (SMI) was calculated by normalizing the measured muscle area (cm2) by height in meters squared (m2). Sarcopenia was defined as an SMI of < 43.2 for men and < 34.6 for women [14].

6. Statistical analysis

The Student t test was employed for continuous variables, and the χ2 or Fisher exact tests, as appropriate, were used for categorical variables to compare differences between the groups. Univariable and multivariable analyses using a binary logistic regression analysis were conducted to identify risk factors associated with complications, major complications, anemia, and vitamin B12 deficiency. Variables with a significance level of p < 0.05 in univariable analyses were included in the multivariable model. Variance inflation factors (VIF) were used to assess collinearity among variables, using a threshold of a VIF greater than 10 to identify multicollinearity [15]. In the multivariable analysis, backward stepwise methods were used which led to the removal of insignificant variables (p > 0.05).

The number of patients diagnosed with anemia and/or vitamin B12 deficiency at the outpatient clinic was recorded. The duration from surgery to the first diagnosis of anemia, vitamin B12 deficiency, death, and cancer recurrence was calculated. The Kaplan-Meier method was employed to calculate the cumulative incidence of anemia and vitamin B12 deficiency, as well as overall and recurrence-free survival. Differences between the groups were assessed using the log-rank test.

To compare the longitudinal outcomes of body composition and nutritional laboratory changes, a linear mixed model analysis was applied. A p-value of < 0.05 was considered statistically significant. All statistical analyses were performed using the SPSS ver. 25.0 for Windows (IBM Corp., Armonk, NY).

Results

1. Patient characteristics

A retrospective review of the prospective gastric cancer database identified 506 patients who underwent curative PG-DTR or TG for pathologic stage I disease without combined organ resection and with available CT scan data. Clinicopathological characteristics of the patients are summarized in Table 1. Among the 506 patients, 197 were included in the PG-DTR group and 306 in the TG group. The mean survival follow-up period for was 38.9±15.7 months (range, 3 to 72 months), and the mean anemia follow-up period was 33.5±30.2 (range, 0 to 100). The mean age of patients in the PG-DTG group (57.2±11.8 years) was less than that of patients in the TG group (60.0±10.5 years, p=0.006). Other clinical characteristics, including sex, American Society of Anesthesiology (ASA) scores, weight, height, and body mass index (BMI) did not show statistically significant differences between the two groups (p > 0.05). Tumor size in the PG-DTR group (24.1±15.6 mm) was smaller than that in the TG group (31.6±23.1 mm, p < 0.001). The PG-DTR group had a less advanced T category and overall stage than TG group (p=0.039 and p=0.002, respectively). Other pathological characteristics were comparable between the groups.

Clinicopathological characteristics of patients in the two groups

2. Surgical outcomes

Perioperative outcomes between the PG-DTR and TG groups are summarized in Table 2. The PG-DTR group exhibited a higher frequency of minimally-invasive surgery (laparoscopic and robotic), partial omentectomy, limited lymphadenectomy, and a lower number of retrieved lymph nodes compared to the TG group (all p < 0.001). Operation time and the rate of intraoperative transfusion showed no significant differences between the groups. The PG-DTR group had a lower rate of early complications (p=0.041), however, major complications and long-term surgical complications were marginally different compared to the TG group (p=0.073 and p=0.062, respectively). In comparison with the TG group, the PG-DTR group had a lower diagnosis rate of anemia and vitamin B12 deficiency, leading to lower frequencies of iron and vitamin B12 replacement therapies (all p < 0.001). The number of patients that met the diagnostic criteria for sarcopenia was similar in both groups, however, at 6 months postoperatively, it was significantly lower in the PG-DTR group compared to the TG group (p=0.032).

Perioperative outcomes of patients in the two groups

Univariable and multivariable analyses for complications and major complications are demonstrated in S1 and S2 Tables. Results of the multivariable analyses for complications and for major complications are presented in Table 3. The only identified risk factor for complications was visceral fat area on preoperative CT scan (Exp(B)=1.008, p < 0.001). Multivariable analyses for major complications identified old age, open surgery, and visceral fat as independent risk factors, while subcutaneous fat area on preoperative CT scan was independent protective factor. In multivariable linear regression analysis, visceral fat area on preoperative CT scan positively correlated with the operation time, intraoperative blood loss, and hospital stay (p < 0.001, p=0.006, and p < 0.001, respectively) (S3 Table). Muscle area on preoperative CT scan also correlated with hospital stay (p < 0.001).

Multivariable analyses for complications and for major complications

3. Hematologic outcomes

The cumulative incidences of anemia and iron replacement in the PG-DTR and TG groups are illustrated in Fig. 1. The 5-year cumulative incidence rate of anemia in the PGDTG group was 52.5%, which was significantly lower than that in the TG group (69.3%, p < 0.001) (Fig. 1A). The 5-year cumulative incidence rate of anemia or iron replacement in the PG-DTG group was 54.6%, significantly lower than that in the TG group (71.9%, p < 0.001) (Fig. 1B). The number of iron replacements in the PG-DTR group was significantly lower than that in the TG group (p=0.002) (Fig. 1C).

Fig. 1.

The 5-year cumulative incidences of anemia and vitamin B12 deficiency and their respective replacements in the two study groups. (A) 5-Year cumulative incidence of anemia. (B) 5-Year cumulative incidence of iron replacement. (C) Frequency of iron replacement. (D) 5-Year cumulative incidence of vitamin B12-deficiency. (E) 5-Year cumulative incidence of vitamin B12 replacement. (F) Frequency of vitamin B12 replacement. PG-DTR, proximal gastrectomy with double-tract reconstruction; TG, total gastrectomy.

The 5-year cumulative incidence rate of vitamin B12 deficiency in the PG-DTG group was 15.7%, significantly lower than that in the TG group (32.3%, p < 0.001) (Fig. 1D). The 5-year cumulative incidence rate of vitamin B12 deficiency or replacement in the PG-DTG group was 47.0%, significantly lower than that in the TG group (91.1%, p < 0.001) (Fig. 1E). The frequency of vitamin B12 replacement therapies in the PG-DTR group was significantly lower than that in the TG group (p < 0.001) (Fig. 1F).

Univariable and multivariable analyses for anemia and vitamin B12 deficiency are demonstrated in S4 and S5 Tables. Multivariate analysis regarding risk factors for anemia and vitamin B12 deficiency is presented in Table 4. In addition to the old age and a high ASA score of patients, a low preoperative hemoglobin level was a risk factor (odds ratio [OR], 0.541; 95% confidence interval [CI], 0.463 to 0.632; p < 0.001), and PG was a protective factor for anemia (OR, 0.447; 95% CI, 0.298 to 0.670; p < 0.001). Regarding vitamin B12 deficiency, female sex, high BMI, and low preoperative vitamin B12 level were risk factors, but PG was a protective factor (OR, 0.494; 95% CI, 0.303 to 0.806; p=0.005).

Multivariable analyses for anemia and vitamin B12 deficiency

4. Body compositional changes and changes in laboratory values

Body compositional changes and changes in laboratory values between the PG-DTR and TG groups are illustrated in Fig. 2. All body compositions, including visceral fat, subcutaneous fat, muscle, and abdominal circumference, did not show significant differences at each time period between the groups. Linear mixed model analysis demonstrated similar volumes of subcutaneous fat and muscle and abdominal circumference in both groups, but a higher preserved visceral fat volume in the PG-DTR group (Fig. 2A-D). The difference in body weight between both groups was not significant through the study period (Fig. 2E). The PG-DTR group exhibited higher levels of hemoglobin, albumin, and prognostic nutritional index than the TG group throughout the study period, with hemoglobin being the only parameter that was significantly different in both groups in linear mixed model analysis (p=0.007) (Fig. 2F-H).

Fig. 2.

Changes in body composition and nutritional laboratory values in the two study groups. (A) Visceral fat volume. (B) Subcutaneous fat volume. (C) Muscle volume. (D) Abdominal circumference. (E) Body weight. (F) Hemoglobin. (G) Albumin. (H) Prognostic nutritional index. *p < 0.05.

5. Long-term survival

During the follow-up period, 12 patients (2.4%) died, of which five (2.5%) were from the PG-DTR group and seven (2.3%) were from the TG group. The hazard ratio (HR) for death in the PG-DTR group, as compared to the TG group, was 1.124 (95% CI, 0.352 to 3.590; p=0.844). The 5-year overall survival rate of the PG-DTR group was 96.6%, and that of the TG group was 96.4% (log-rank p=0.790) (Fig. 3A).

Fig. 3.

Overall and recurrence-free survivals of the patients between the two study groups. (A) Overall survivals. (B) Recurrence-free survivals. PG-DTR, proximal gastrectomy with double-tract reconstruction; TG, total gastrectomy.

Six patients (1.2%) experienced recurrence, of which one (0.5%) was from the PG-DTR group and five (1.6%) were from the TG group. The HR for recurrence in the PG-DTR group, as compared to the TG group, was 0.310 (95% CI, 0.036 to 2.675; p=0.260). The 5-year recurrence-free survival rate of the PG-DTR group was 98.8%, and that of the TG group was 97.9% (log-rank p=0.280) (Fig. 3B).

Discussion

In this study, which included patients with pathological stage I gastric cancer located in proximal stomach, surgical outcomes of PG-DTR were compared with TG. Regarding perioperative outcomes, PG-DTR demonstrated a lower frequency of early complications. The incidence of anemia and vitamin B12 deficiency and the frequencies of iron and vitamin B12 replacements were significantly less in the PG-DTR group compared to the TG group. Regarding body composition, PG-DTR was associated with a reduced incidence of sarcopenia at 6 months post-surgery. Multivariable analysis showed that compared with the TG group, the PG-DTR group was associated with a decreased incidence of anemia and vitamin B12 deficiency, shorter operation time, reduced bleeding, and shorter hospital stays. Visceral fat area on CT scan was a risk factor for all cause complications and major complications, and increased operation time, blood loss, and hospital stays. Subcutaneous fat area was a protective factor for major complications, and large muscle area on preoperative CT scan shortened hospital stays.

In this study, certain discrepancies in clinicopathological and surgical characteristics were noted between the PG-DTR and TG groups. The TG group had a larger tumor size; furthermore, total omentectomy as well as D2 lymph node dissection under open surgery were more frequently performed in the TG group than in the PG-DTR group. This limited extent of resection in PG-DTR likely contributed to a lower overall early complication rate compared to TG, despite the additional gastrojejunostomy performed in PG-DTR. Importantly, neither PG-DTR nor TG itself emerged as a risk factor for complications or major complications in the study. For matching the background characteristics of the two groups, measures such as propensity score matching, could be considered. However, matching was not performed because unequal variables in this study, including surgical approach and extent of lymphadenectomy, did not affect long-term nutritional outcomes and survival in patients with early gastric cancer [16,17].

To evaluate nutritional outcomes between the PG-DTR and TG groups, incidence of anemia and vitamin B12 deficiency, as well as frequency of replacement of iron and vitamin B12, were compared. A prior retrospective study on patients who underwent surgery at our institution between 2014 and 2015, in addition to the prospective KLASS-05 study, reported no difference in the incidence of anemia [4,5]. However, in the present study, which has an extended observation period and a higher volume of cases, the incidence of anemia and the frequency of iron supplementation were significantly lower than that in the PG-DTR group. This aligns with recently published results from a meta-analysis [3]. Factors such as the duodenal passage of ingested food and the relative preservation of chief cells in the remnant stomach after PG-DTR have been reported to contribute to enhanced iron absorption [18,19].

The volume of the remaining stomach is recognized as a crucial factor for absorption of nutrients. At our institution, the surgical method for PG-DTR has evolved over time since its initiation in 2014, with modifications aimed at increasing the volume of the remaining stomach. This progressive refinement may have contributed to the favorable outcomes pertaining to anemia and vitamin B12 deficiency in the PG-DTR group as observed in the present study (study duration: from 2015-2019) compared to our previous reports (study duration: from 2014-2015) [4]. The low incidences of vitamin B12 deficiency and the reduced need for replacement after PG-DTR in this study align with the results of the KLASS-05 randomized controlled trial (RCT) and meta-analysis [3,5]. Because intrinsic factor secreted in the stomach is crucial to vitamin B12 metabolism, the absence of intrinsic factor in patients who have undergone TG direct develop to vitamin B12 deficiency [20,21]. Ideally, the incidence of vitamin B12 deficiency approaches 100% in 3-5 years [11]. However, the incidence of vitamin B12 deficiency or frequency of replacement of vitamin B12 in the TG group approached 90%, and not 100%. As this was a retrospective study, we were unable to control the medications administered to the patients outside of our institution. This limitation also applies to the PG group. These factors should be considered when translating our study results into patient care.

To the best of our knowledge, this study is the first to analyze the body compositional data on CT scans between PG-DTR and TG groups. Among the various definitions of sarcopenia, this study utilized the SMI criteria validated in Asians [14]. The volumes of subcutaneous fat and muscle, as well as abdominal circumference, between the groups were not remarkably different. However, visceral fat volume was relatively preserved after PG-DTR compared to that after TG. At 6 months after surgery, sarcopenia occurred less frequently in the PG-DTR group than that in the TG group. The exact reasons for this difference could not be elucidated in this retrospective study. One hypothesis is that the duodenal passage of ingested food after PG-DTR, specifically glucose, stimulates gastric inhibitory polypeptide secretion, which may affect the insulin sensitivity of adipocytes [22]. Our results are supported by an RCT demonstrating that visceral fat loss after distal gastrectomy was greater with Roux-en-Y anastomosis than with gastroduodenostomy [23]. Meanwhile, the prevalence of sarcopenia in the PG-DTR group appeared to increase over time compared to the TG group. However, the sarcopenia rate was not statistically different between the two groups, as determined by repeated-measures analysis of variance (ANOVA) (p=0.083). Although this difference was not significant, further research is needed, including follow-up studies over a longer period.

In contrast to visceral fat volume, laboratory nutritional markers such as albumin and prognostic nutritional index did not show significant differences between the PG-DTR and TG groups. Throughout the follow-up period of the study, the nutritional values of the PG-DTR group were consistently higher than those of the TG group. However, the preoperative values were also high, which might have contributed to the lack of significance in the linear mixed model analysis. A meta-analysis comparing laparoscopic PG versus TG reported similar findings in laboratory nutritional markers, thereby supporting our results [24].

This study included patients with pathological stage I gastric cancer, with a low incidence of gastric cancer-related deaths or recurrence. The long-term survival outcomes between the PG-DTR and TG groups were comparable, aligning with the findings of previous studies [5]. Notably, the present study demonstrated that visceral fat volume was relatively more preserved after PG-DTR than that after TG, and this may have potentially influenced the long-term prognosis after gastrectomy. The loss of visceral fat after gastrectomy has been associated with poor survival in patients with gastric cancer, while higher visceral fat volumes are linked to improved survivals [25,26]. Recently, PG for advanced gastric cancer located in the upper stomach or gastroesophageal junction has been actively investigated [27], and some studies have reported similar or superior survival after PG for advanced gastric cancer compared to that after TG [28-31]. The relationship between limited loss of visceral fat volume after gastrectomy and long-term prognosis warrants further investigation in future research.

Despite its strengths, this study had some limitations. First, this was a retrospective investigation conducted at a single institution, which may limit the generalizability of the findings. In addition, as previously mentioned, several clinicopathological features between the groups differed, although not significantly. Consequently, a multicenter prospective study is warranted to validate and strengthen the reliability of our findings. Second, lifestyle habits such as diet and exercise, which could potentially influence body composition, were not included in the analysis. The inability to control over every patient’s daily lifestyle habits over an extended period, even in randomized clinical trials, poses a challenge in addressing this aspect. Finally, the patient benefits of limited surgery might be considered in the decision-making process. Our data lacks an assessment of quality of life, specifically focusing on reflux symptoms and dumping syndromes, which are important aspects to evaluate the holistic impact of the surgical approach on patients’ well-being.

In conclusion, PG-DTR for early gastric cancer located in the upper stomach offers advantages in reducing the incidences of anemia and vitamin B12 deficiency, along with a lower need for supplementation of both elements when compared to TG. Additionally, compared to TG, PG-DTR demonstrated a lower complication rate, less decrease in visceral fat volume, and similar long-term survival outcomes. These findings suggest that PG-DTR may serve as a viable alternative to TG for the treatment of early gastric cancer located in the upper stomach.

Electronic Supplementary Material

Notes

Ethical Statement

This study included patients who underwent radical PG-DTR or TG for pathological stage I gastric cancer. Patients who underwent combined organ resection or lacked computed tomography (CT) scan data required for body composition analysis were excluded. This study received approval from the Institutional Review Board of Severance Hospital, Yonsei University Health System (4-2024-0081). The informed consent was waived as this was a retrospective study.

Author Contributions

Conceived and designed the analysis: Song JH, Kim HI.

Collected the data: Cho M, Kim YM, Hyung WJ, Kim HI.

Contributed data or analysis tools: Park SH, Kim HI.

Performed the analysis: Song JH, Kim HI.

Wrote the paper: Song JH, Kim HI.

Administrative, technical, or material support: Cho M, Hyung WJ.

Supervision: Kim HI.

Conflict of Interest

Conflict of interest relevant to this article was not reported.

Acknowledgements

We would like to thank Editage (www.editage.co.kr) for English language editing. This study was supported by research grant from the Korean Surgical Society.

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Article information Continued

Fig. 1.

The 5-year cumulative incidences of anemia and vitamin B12 deficiency and their respective replacements in the two study groups. (A) 5-Year cumulative incidence of anemia. (B) 5-Year cumulative incidence of iron replacement. (C) Frequency of iron replacement. (D) 5-Year cumulative incidence of vitamin B12-deficiency. (E) 5-Year cumulative incidence of vitamin B12 replacement. (F) Frequency of vitamin B12 replacement. PG-DTR, proximal gastrectomy with double-tract reconstruction; TG, total gastrectomy.

Fig. 2.

Changes in body composition and nutritional laboratory values in the two study groups. (A) Visceral fat volume. (B) Subcutaneous fat volume. (C) Muscle volume. (D) Abdominal circumference. (E) Body weight. (F) Hemoglobin. (G) Albumin. (H) Prognostic nutritional index. *p < 0.05.

Fig. 3.

Overall and recurrence-free survivals of the patients between the two study groups. (A) Overall survivals. (B) Recurrence-free survivals. PG-DTR, proximal gastrectomy with double-tract reconstruction; TG, total gastrectomy.

Table 1.

Clinicopathological characteristics of patients in the two groups

PG-DTR (n=197) TG (n=309) p-value
Age (yr) 57.2±11.8 60.0±10.5 0.006
Sex
 Male 122 (61.9) 217 (70.2) 0.053
 Female 75 (38.1) 92 (29.8)
ASA
 1 44 (22.3) 48 (15.5) 0.066
 2 117 (59.4) 184 (59.5)
 3 36 (18.3) 77 (24.9)
Weight (kg) 64.3±10.3 64.9±10.4 0.538
Height (cm) 164.5±8.7 164.9±7.6 0.571
BMI 23.7±2.9 23.8±3.1 0.687
Tumor size (mm) 24.1±15.6 31.6±23.1 < 0.001
Histology
 Differentiated 81 (41.1) 121 (39.2) 0.661
 Undifferentiated 116 (58.9) 288 (60.8)
Lymphovascular invasion
 No 175 (88.8) 264 (85.4) 0.272
 Yes 22 (11.2) 45 (14.6)
Perineural invasion
 No 192 (97.5) 293 (94.8) 0.147
 Yes 5 (2.5) 16 (5.2)
T category
 T1a 82 (41.6) 121 (39.2) 0.039
 T1b 98 (49.7) 137 (44.3)
 T2 17 (8.6) 51 (16.5)
N category
 N0 187 (94.9) 282 (91.3) 0.123
 N1 10 (5.1) 27 (8.7)
Stage
 Ia 170 (86.3) 231 (74.8) 0.002
 Ib 27 (13.7) 78 (25.2)

Values are presented as mean±standard deviation or number (%). p-value of < 0.05 is considered significant. ASA, American Society of Anesthesiology scores; BMI, body mass index; PG-DTR, proximal gastrectomy with double-tract reconstruction; TG, total gastrectomy.

Table 2.

Perioperative outcomes of patients in the two groups

PG-DTR (n=197) TG (n=309) p-value
Operation method
 Open 1 (0.5) 113 (36.6) < 0.001
 Laparoscopic 114 (57.9) 149 (48.2)
 Robotic 82 (41.6) 47 (15.2)
Omentectomy
 Partial 189 (95.9) 179 (57.9) < 0.001
 Total 8 (4.1) 130 (42.1)
Lymph node dissection
 D1+ 196 (99.5) 183 (59.2) < 0.001
 D2 1 (0.5) 126 (40.8)
Retrieved lymph nodes 41.1±15.6 56.1±21.5 < 0.001
Operation time 210.0±47.2 214.0±55.9 0.391
Blood loss 76.6±70.2 157.3±151.7 < 0.001
Transfusion 0 3 (1.0) 0.085
Hospital stay 6.3±3.0 8.1±4.1 < 0.001
Early complication 113 (57.4) 205 (66.3) 0.041
Clavien-Dindo grade
 I 59 (29.9) 87 (28.2) 0.089
 II 46 (23.4) 93 (30.1)
 IIIa 8 (4.1) 19 (6.1)
 IIIb 0 3 (1.0)
 IVa 0 3 (1.0)
 V 0 0
Early major complication 8 (4.1) 25 (8.1) 0.073
Long-term surgical complication 5 (2.5) 19 (6.1) 0.062
Clavien-Dindo grade
 I 1 (0.5) 5 (1.6) 0.439
 II 3 (1.5) 6 (1.9)
 IIIa 1 (0.5) 6 (1.9)
 IIIb 0 2 (0.6)
Long-term major surgical complication 1 (0.5) 8 (2.6) 0.084
Anemia 100 (50.8) 211 (68.3) < 0.001
Iron replacement 50 (25.4) 131 (42.4) < 0.001
Vitamin B12 deficiency 31 (15.7) 99 (32.0) < 0.001
Vitamin B12 replacement 91 (46.2) 278 (90.0) < 0.001
Sarcopenia
 Preoperative 35/196 (17.9) 78/308 (25.3) 0.050
 At 6 months postoperatively 44/192 (22.9) 97/305 (31.8) 0.032
 At 12 months postoperatively 55/189 (29.1) 96/294 (32.7) 0.411
 At 60 months postoperatively 75/180 (41.7) 96/245 (39.2) 0.606

Values are presented as number (%) or mean±standard deviation. p-value of < 0.05 is considered significant. PG-DTR, proximal gastrectomy with double-tract reconstruction; TG, total gastrectomy.

Table 3.

Multivariable analyses for complications and for major complications

Complications
Major complications
Odds ratio 95% CI p-value Odds ratio 95% CI p-value
Age 1.043 1.003-1.085 0.035
Operation method
 Open 1 0.006
 MIS 0.344 0.162-0.733
VF 1.008 1.005-1.011 < 0.001 1.009 1.003-1.015 0.003
SF 0.988 0.978-0.997 0.013

p-value of < 0.05 is considered significant. CI, confidence interval; MIS, minimally-invasive surgery; SF, subcutaneous fat; VF, visceral fat.

Table 4.

Multivariable analyses for anemia and vitamin B12 deficiency

Anemia
Vitamin B12 deficiency
Odds ratio 95% CI p-value Odds ratio 95% CI p-value
Sex
 Male 1 0.024
 Female 1.824 1.081-3.076
ASA
 1 1
 2 1.294 0.768-2.181 0.333
 3 2.158 1.139-4.091 0.018
BMI 1.137 1.055-1.226 0.001
Preoperative hemoglobin 0.541 0.463-0.632 < 0.001
Preoperative vitamin B12 0.998 0.998-0.999 < 0.001
Resection extent
 PG-DTR 0.447 0.298-0.670 < 0.001 0.494 0.303-0.806 0.005
 TG 1 1

p-value of < 0.05 is considered significant. ASA, American Society of Anesthesiology scores; BMI, body mass index; CI, confidence interval; PG-DTR, proximal gastrectomy with double-tract reconstruction; TG, total gastrectomy.