Advertisement

Gastric Cancer

, Volume 18, Issue 2, pp 397–406 | Cite as

Factors that minimize postgastrectomy symptoms following pylorus-preserving gastrectomy: assessment using a newly developed scale (PGSAS-45)

  • Tsutomu Namikawa
  • Naoki Hiki
  • Shinichi Kinami
  • Hiroshi Okabe
  • Takashi Urushihara
  • Hiroshi Kawahira
  • Norimasa Fukushima
  • Yasuhiro Kodera
  • Takeyoshi Yumiba
  • Atsushi Oshio
  • Koji Nakada
Original Article

Abstract

Background

Pylorus-preserving gastrectomy (PPG) is sometimes performed as a function-preserving surgery for the treatment of early gastric cancer. The aim of this study was to use an integrated assessment scale for postgastrectomy syndrome to determine the appropriate indicators and optimal methods for PPG.

Methods

The Postgastrectomy Syndrome Assessment Study (PGSAS) is a multicenter survey based on an integrated questionnaire (PGSAS-45) consisting of 45 items. Questionnaire responses were retrieved from a total of 2,520 patients, each of whom had undergone one of six different types of gastrectomy procedures; 313 responses from patients who had received PPG were analyzed here.

Results

The size of the proximal gastric remnant (less than one-quarter, about one-third, or more than one-half of the original size) significantly influenced the change in body weight, the scores for dissatisfaction at the meal, and dissatisfaction for daily life subscale (P = 0.030, P = 0.005, P = 0.034, respectively). The nausea score in patients who underwent hand-sewn anastomosis was significantly lower than in those who underwent anastomosis with a linear stapler (P = 0.006). The scores for diarrhea subscale, increased passage of stools, and sense of foods sticking differed significantly depending on the length of the preserved pyloric cuff (P = 0.047, P = 0.021, P = 0.046, respectively).

Conclusions

The results suggest that preservation of a sufficient proximal gastric remnant is recommended when utilizing PPG as function-preserving surgery.

Keywords

Pylorus-preserving gastrectomy Quality of life Early gastric cancer Function-preserving surgery Postgastrectomy syndrome 

Introduction

Pylorus-preserving gastrectomy (PPG) is a form of function-preserving surgery that preserves the quality of life (QOL) of patients requiring radical gastrectomy [1, 2]. PPG was initially reported by Maki et al. [3] as an effective modification of distal gastrectomy for the treatment of benign gastric diseases. Preserving pyloric function has several advantages, such as the prevention of dumping syndrome, protection against bile mucosal injury of the remnant stomach, and reduction in postoperative body weight loss. The low probability of lymph node metastasis in early gastric cancer (EGC) has allowed the increasing use of limited resection as a treatment option, and PPG has been demonstrated to be a viable option for patients with EGC located in the middle third of the stomach [1, 4, 5]. Moreover, it has been reported that PPG may result in a long-term survival benefit for patients diagnosed with cT1 gastric cancer (mucosal or submucosal), or cN0 gastric cancer in the middle of the body of the stomach [1]. Previous investigators have reported that the overall 5-year survival rate for patients who have undergone PPG is 95–98 % [1, 5, 6].

Evaluation of the various ways of preserving function, such as reducing the extent of gastrectomy, or conducting nerve or sphincter preservation, is very important; however, scientific assessment is not easy because there is no gold standard scale for measuring gastrointestinal function and the QOL of patients. So far, there have been few reports of long-term symptom evaluation following PPG with large numbers of cases [7, 8]. The Postgastrectomy Syndrome Assessment Study (PGSAS) is a multicenter questionnaire survey conducted from July 2009 to December 2010 by the Japan Postgastrectomy Syndrome Working Party to clarify the actual life status of patients after gastrectomy and the relationship between type of gastrectomy and postgastrectomy syndrome (PGS). Although PPG has many benefits compared with conventional distal gastrectomy with Billroth I reconstruction, debate continues regarding the clinical benefits of PPG, the effects of preserving either the celiac or the pyloric branch of the vagal nerve, the relationship between the length of the pyloric cuff and postoperative symptoms, and the indications for PPG. Here, we analyzed responses to the survey questionnaire to determine the appropriate indicators and optimal methods for PPG and which methods of PPG reserve sufficient function to maintain a good QOL for patients with gastric cancer.

Materials and methods

The Japan Postgastrectomy Syndrome Working Party conducted a questionnaire survey by using a newly developed integrated questionnaire that is composed of 45 items (Postgastrectomy Syndrome Assessment Scale-45, PGSAS-45) to assess the effects of gastrectomy on daily life. PGSAS-45 includes the following components: (1) 8 items comprising a generic QOL questionnaire called Short Form-8 (SF-8), an instrument commonly used for measuring health-related QOL that is based on extensive previous work with the SF-36 [9]; (2) 15 items comprising the Gastrointestinal Symptom Rating Scale (GSRS), a symptom-specific instrument used to evaluate common symptoms of gastrointestinal disorders [10]; (3) 8 items regarding important postgastrectomy symptoms; (4) 2 items regarding number and type of early or late dumping symptoms; (5) 8 items regarding meal intake; (6) 1 item regarding working status; and (7) 3 items regarding degree of dissatisfaction with symptoms, meal intake, and ability to work, respectively (Table 1). For the 23 symptom items, a seven-grade (1–7) Likert scale was used, and a five-grade (1–5) Likert scale was used for all the other items except items 1, 4, 29, 32, and 34–37. Based on data from the retrieved PGSAS-45 questionnaires, outcome measures were refined through consolidation and selection [11, 12]. The main outcome measures in PGSAS are listed in Table 2, and the other outcome measures in this study are symptoms of PGSAS-45. The clinical data collected included age, sex, height, body weight, elapsed time since gastrectomy, and details of the surgical methods.
Table 1

Structure of Postgastrectomy Syndrome Assessment Study (PGSAS)-45 (domains/subdomains/items/subscales)

Domains

Subdomains

Items

Subscales

Quality of life

SF-8 (quality of life)

1

Physical functioning*

Physical component summary*

2

Role–physical*

Mental component summary*

3

Bodily pain*

 

4

General health*

 

5

Vitality*

 

6

Social functioning*

 

7

Role–emotional*

 

8

Mental health*

 

Symptoms

GSRS (symptoms)

9

Abdominal pains

Esophageal reflux subscale (items 10, 11, 13, 24)

10

Heartburn

Abdominal pain subscale (items 9, 12, 28)

11

Acid regurgitation

Meal-related distress subscale (items 25–27)

12

Sucking sensations in the epigastrium

Indigestion subscale (items 14–17)

13

Nausea and vomiting

Diarrhea subscale (items 19, 20, 22)

14

Borborygmus

Constipation subscale (items 18, 21, 23)

15

Abdominal distension

Dumping subscale (items 30, 31, 33)

16

Eructation

 

17

Increased flatus

Total symptom scale (more than seven subscales)

18

Decreased passage of stools

 

19

Increased passage of stools

 

20

Loose stools

 

21

Hard stools

 

22

Urgent need for defecation

 

23

Feeling of incomplete evacuation

 

Symptoms

24

Bile regurgitation

 

25

Sense of foods sticking

 

26

Postprandial fullness

 

27

Early satiation

 

28

Lower abdominal pains

 

29

Number and type of early dumping symptoms

 

30

Early dumping, general symptoms

 

31

Early dumping, abdominal symptoms

 

32

Number and type of late dumping symptoms

 

33

Late dumping symptoms

 

Living status

Meals (amount) 1

34

Ingested amount of food per meal*

 

35

Ingested amount of food per day*

 

36

Frequency of main meals

 

37

Frequency of additional meals

 

Meals (quality)

38

Appetite*

Quality of ingestion subscale* (items 38–40)

39

Hunger feeling*

 

40

Satiety feeling*

 

Meals (amount) 2

41

Necessity for additional meals

 

Social activity

42

Ability for working

 

Quality of life

Dissatisfaction (Quality of life)

43

Dissatisfaction with symptoms

Dissatisfaction with daily life subscale (items 43–45)

44

Dissatisfaction at the meal

 

45

Dissatisfaction with working

 

PGSAS-45 Postgastrectomy Syndrome Assessment Scale-45, SF-8 Short Form-8, QOL quality of life, GSRS Gastrointestinal Symptom Rating Scale

In items or subscales with *, higher scores indicate better conditions. In items or subscales without *, higher scores indicate worse conditions. Each subscale is calculated as the mean of its composite items or subscales, except the physical and mental component summaries of SF-8. Items 29 and 32 do not have scores; these items were analyzed separately

Table 2

Main outcome measures in PGSAS

Domains

Main outcome measures

Symptoms

 

 Subscales

Esophageal reflux subscale

Abdominal pain subscale

Meal-related distress subscale

Indigestion subscale

Diarrhea subscale

Constipation subscale

Dumping subscale

 Total

Total symptom score

Living status

 

 Body weight

Change in body weight (%)*

 Meals (amount)

Amount of food ingested per meal*

Necessity for additional meals

 Meals (quality)

Quality of ingestion subscale*

 Work

Ability for working

Quality of life

 

 Dissatisfaction

Dissatisfaction with symptoms

Dissatisfaction at the meal

Dissatisfaction at working

Dissatisfaction withdaily life subscale

 Short Form-8

Physical component summary*

Mental component summary*

PGSAS Postgastrectomy Syndrome Assessment Study

In items or subscales with *, higher scores indicates better conditions; in items or subscales without *, higher scores indicates worse conditions

All patients enrolled in this trial fulfilled the following eligibility criteria: (1) diagnosis of pathologically confirmed stage IA or IB gastric cancer; (2) first-time gastrectomy status; (3) age >20 and ≤75 years; (4) no history of chemotherapy; (5) no recurrence or distant metastasis indicated; (6) gastrectomy conducted 1 or more years before enrollment date; (7) performance status (PS) ≤1 on the Eastern Cooperative Oncology Group (ECOG) scale; (8) full capacity to understand and respond to the questionnaire; (9) no history of other diseases or surgeries that might influence responses to the questionnaire; (10) no presence of organ failure or mental illness; and (11) written informed consent. Patients with dual malignancy or concomitant resection of other organs (with co-resection equivalent to cholecystectomy being the exception) were excluded.

Fifty-two institutions participated in this study. The study utilized continuous sampling from a central registration system for participant enrollment. From July 2009 to December 2010, the questionnaire was distributed to all eligible patients as they presented to participating institutions. After completing the questionnaire, patients were instructed to return forms to the data center. All QOL data from questionnaires were matched with individual patient data collected via case report forms. The study was approved by the institutional review board of the participating institutions [University Hospital Medical Information Network’s Clinical Trials Registry (UMIN-CTR) registration number, 000002116]. Written informed consent was obtained from all enrolled patients, conforming to institutional guidelines.

Survey analysis

During the enrollment period, the PGSAS-45 questionnaire was handed to 2,922 eligible patients. A total of 2,520 questionnaires (86 %) were retrieved, of which 2,368 (81 %) were eligible. Respondents were 393 patients who underwent total gastrectomy, 475 patients who underwent distal gastrectomy with Roux-en-Y reconstruction, 909 patients who underwent distal gastrectomy with Billroth I reconstruction, 313 patients who underwent PPG, 193 patients who underwent proximal gastrectomy, and 85 patients who underwent local resection of the stomach. Here, we investigated the 313 patients who underwent PPG to assess the relationship between their QOL status and the size of the proximal gastric remnant, method of anastomosis, length of the pyloric cuff, and preservation of the pyloric branch of the vagal nerve.

Patients who underwent PPG were divided into three groups according to the size of the proximal gastric remnant (those with more than one-half, about one-third, or less than one-quarter of the stomach remaining) and three groups according to the length of the preserved pyloric cuff (those with less than 2.5 cm, 3.0–5.0 cm, or more than 5.5 cm of the pyloric cuff preserved).

Statistical analysis

The significance of differences between the mean values of two groups was assessed by the unpaired t test and that among three groups was assessed by one-way analysis of variance (ANOVA). In the latter, Bonferroni/Dunn multiple comparisons were performed when the P value of ANOVA was less than 0.1. All data are presented as the mean ± standard deviation. Generally, P values less than 0.05 in t tests or ANOVA were considered to be statistically significant. In a Bonferroni/Dunn multiple comparison, a P value less than 0.05/number of hypothesis was considered to be statistically significant. When P values were less than double the significant level, we calculated Cohen’s d as the effect size. StatView software for Windows version 5.0 (SAS Institute) was used for all statistical analyses.

Results

Patient characteristics

Table 3 summarizes the clinical characteristics of the 313 patients who underwent PPG. One hundred and eighty-three patients (58.5 %) were men and 126 (40.3 %) were women, with a mean age of 61.5 ± 8.7 years. At the time of surgery, 136 patients (43.5 %) underwent laparoscopic PPG and 173 (55.3 %) underwent conventional open PPG. Regarding the size of the proximal gastric remnant compared with the preoperative stomach, 73 patients (23.3 %) retained more than half of the stomach, 222 patients (70.9 %) retained about one-third of the stomach, and 12 patients (3.8 %) retained less than one-quarter of the stomach. Thirty-eight patients (12.1 %) underwent mechanical anastomosis using a linear stapler, and 270 patients (86.3 %) underwent hand-sewn anastomosis. The celiac branch of the vagal nerve was preserved in 213 patients (68.1 %), and the pyloric branch of the vagal nerve was preserved in 254 patients (81.2 %).
Table 3

Clinical characteristics of the 313 patients who underwent pylorus-preserving gastrectomy

Number

313

Period after gastrectomy (months)

38.4 ± 27.7

Body mass index (before gastrectomy)

22.7 ± 3.0

Body mass index (at the time of study)

21.1 ± 2.6

Age (years)

61.5 ± 8.7

Gender

 

 Male

183 (58.5 %)

 Female

126 (40.3 %)

Operation method

 

 Laparoscopic

136 (43.5 %)

 Open

173 (55.3 %)

Size of the proximal gastric remnant

 

 More than half

73 (23.3 %)

 Around one-third

222 (70.9 %)

 Less than one quarter

12 (3.8 %)

Method of anastomosis

 

 Use of linear stapler

38 (12.1 %)

 Hand sewn

270 (86.3 %)

Length of the pyloric cuff (cm)

 

 ≤2.5

34 (10.9 %)

 3.0–5.0

212 (67.7 %)

 ≥5.5

41 (13.1 %)

Preservation of celiac branch of vagal nerve

 

 Yes

213 (68.1 %)

 No

96 (30.7 %)

Preservation of pyloric branch of vagal nerve

 

 Yes

254 (81.2 %)

 No

40 (12.8 %)

Effect of size of the proximal gastric remnant

PGSAS scores in patients grouped according to the size of the proximal gastric remnant (more than half, about one-third, and less than one-quarter) are listed in Table 4. There were significant differences among the three groups with regard to body weight change (%) compared to preoperative weight and the scores for dissatisfaction at the meal and dissatisfaction with daily life subscale (P = 0.030, P = 0.005, and P = 0.034; ANOVA), respectively. When Bonferroni/Dunn comparisons between individual groups were made, the changes in body weight of patients in the “less than one-quarter” group (mean ± SD; −11.9 ± 4.8 %) were significantly greater than those of patients in the “more than one-half” (−6.1 ± 7.1 %; P = 0.008, Cohen’s d = 0.94) ,or “about one-third” groups (−6.8 ± 6.9 %; P = 0.014, Cohen’s d = 0.84), respectively. Similarly, the dissatisfaction at the meal scores in patients in the “less than one-quarter” group (3.1 ± 1.0) were significantly higher than those in the “more than half” (2.0 ± 1.0; P = 0.002, Cohen’s d = 1.04), or “about one-third” groups (2.3 ± 1.1; P = 0.013, Cohen’s d = 0.76), respectively. The scores for dissatisfaction for daily life subscale for patients in the “less than one-quarter” group (2.5 ± 0.8) were significantly higher than those for patients in the “more than half” group (1.8 ± 0.9; P = 0.009, Cohen’s d = 0.82), but not those for patients in the “about one-third” group (1.9 ± 0.8). There were no significant differences among the three groups in other scales examined (Table 4).
Table 4

Outcome measures in patients grouped according to the size of the proximal gastric remnant

 

Size of the proximal gastric remnant

P value (ANOVA)

P value (B/D)

Cohen’s d

More than half (n = 73)

Around one-third (n = 222)

Less than one-quarter (n = 12)

Main outcome measures

Change in body weight (%)

−6.1 ± 7.1 %

−6.8 ± 6.9 %

−11.9 ± 4.8 %

0.030

0.008a

0.94

0.014b

0.85

Physical component summary

51.5 ± 4.8

50.9 ± 5.5

51.2 ± 3.8

≥0.1

  

Mental component summary

50.2 ± 7.0

50.0 ± 5.9

49.2 ± 4.1

≥0.1

  

Esophageal reflux subscale

1.7 ± 0.7

1.7 ± 0.9

1.7 ± 0.6

≥0.1

  

Abdominal pain subscale

1.7 ± 0.9

1.6 ± 0.7

1.7 ± 0.6

≥0.1

  

Meal-related distress subscale

2.0 ± 0.9

2.1 ± 0.9

2.2 ± 0.9

≥0.1

  

Indigestion subscale

2.0 ± 1.0

2.0 ± 0.9

2.1 ± 0.9

≥0.1

  

Diarrhea subscale

1.9 ± 0.9

1.8 ± 1.0

2.2 ± 1.1

≥0.1

  

Constipation subscale

2.2 ± 1.0

2.2 ± 1.1

2.3 ± 1.1

≥0.1

  

Dumping subscale

1.7 ± 0.9

1.8 ± 1.0

1.9 ± 0.6

≥0.1

  

PGSAS total score

1.8 ± 0.7

1.9 ± 0.7

2.0 ± 0.6

≥0.1

  

Amount of food ingested per meal

7.3 ± 2.0

7.0 ± 1.9

6.8 ± 1.6

≥0.1

  

Necessity for additional meals

1.6 ± 0.6

1.8 ± 0.8

1.9 ± 0.6

≥0.1

  

Quality of ingestion subscale

3.5 ± 1.0

3.8 ± 0.9

3.7 ± 0.8

0.064

0.021c

0.31

Ability for working

1.7 ± 0.9

1.8 ± 1.0

2.0 ± 0.6

≥0.1

  

Dissatisfaction with symptoms

1.8 ± 1.0

1.8 ± 0.9

2.3 ± 1.1

≥0.1

  

Dissatisfaction at the meal

2.0 ± 1.0

2.3 ± 1.1

3.1 ± 1.0

0.005

0.002a

1.04

0.013b

0.76

Dissatisfaction at working

1.6 ± 1.0

1.7 ± 0.9

2.1 ± 1.0

≥0.1

  

Dissatisfaction for daily life subscale

1.8 ± 0.9

1.9 ± 0.8

2.5 ± 0.8

0.034

0.009a

0.82

In ANOVA, a P value less than 0.05 was considered as statistically significant

In Bonferroni/Dunn multiple comparisons, a P value less than 0.0167 was considered as statistically significant

Interpretation of effect size in Cohen’s d: ≥0.20 as small, ≥0.50 as medium, ≥0.80 as large

ANOVA one-way analysis of variance, B/D Bonferroni/Dunn multiple comparisons

aMore than half vs. less than one-quarter

bApproximately one-third vs. less than one-quarter

cMore than half vs. approximately one-third

Effect of method of anastomosis

The nausea scores in patients who underwent hand-sewn anastomosis (1.4 ± 0.9) were significantly lower than those in patients who underwent mechanical anastomosis using a linear stapler (1.9 ± 1.2; P = 0.006, Cohen’s d = 0.44; unpaired t test). There were no significant differences between the two groups in other scales examined (Table 5).
Table 5

Outcome measures in patients grouped according to method of anastomosis

 

Method of anastomosis

P value

Cohen’s d

Linear stapler (n = 38)

Hand sewing (n = 270)

Main outcome measures

 

 Change in body weight (%)

−5.7 ± 6.9

−7.0 ± 6.9

≥0.1

 

 Physical component summary

50.7 ± 5.0

51.1 ± 5.3

≥0.1

 

 Mental component summary

49.8 ± 5.9

50.0 ± 6.1

≥0.1

 

 Esophageal reflux subscale

1.8 ± 0.9

1.7 ± 0.8

≥0.1

 

 Abdominal pain subscale

1.7 ± 0.8

1.6 ± 0.7

≥0.1

 

 Meal-related distress subscale

2.2 ± 0.8

2.1 ± 0.9

≥0.1

 

 Indigestion subscale

2.1 ± 0.9

2.0 ± 0.9

≥0.1

 

 Diarrhea subscale

2.0 ± 0.9

1.8 ± 1.0

≥0.1

 

 Constipation subscale

2.1 ± 0.9

2.3 ± 1.1

≥0.1

 

 Dumping subscale

1.7 ± 0.9

1.8 ± 0.9

≥0.1

 

 PGSAS total score

1.9 ± 0.7

1.9 ± 0.7

≥0.1

 

 Amount of food ingested per meal

6.9 ± 2.0

7.0 ± 1.9

≥0.1

 

 Necessity for additional meals

1.7 ± 0.6

1.8 ± 0.8

≥0.1

 

 Quality of ingestion subscale

3.7 ± 0.9

3.8 ± 0.9

≥0.1

 

 Ability for working

1.9 ± 1.0

1.8 ± 0.9

≥0.1

 

 Dissatisfaction with symptoms

1.8 ± 0.9

1.8 ± 0.9

≥0.1

 

 Dissatisfaction at the meal

2.3 ± 1.2

2.2 ± 1.1

≥0.1

 

 Dissatisfaction at working

1.8 ± 1.0

1.6 ± 0.9

≥0.1

 

 Dissatisfaction for daily life subscale

2.0 ± 0.9

1.9 ± 0.8

≥0.1

 

Other outcome measures (symptoms)

 Nausea and vomiting

1.9 ± 1.2

1.4 ± 0.9

0.006

0.44

In the unpaired t test, a P value less than 0.05 was considered as statistically significant

Interpretation of effect size in Cohen’s d: ≥0.20 as small, ≥0.50 as medium, ≥0.80 as large

Effect of the length of the pyloric cuff

Values for various PGSAS outcome measures in patients subgrouped according to the length of the remnant pyloric cuff (≤2.5 cm, 3.0–5 cm, or ≥5.5 cm) are listed in Table 6. There were significant differences among the three groups in terms of the scores for diarrhea subscale, increased passage of stools, and sense of foods sticking (P = 0.047, P = 0.021, and P = 0.046, respectively; ANOVA). Although the group with a remnant pyloric cuff of 3.0–5.0 cm showed the lowest scores for the foregoing outcome measures, no significant differences were found between individual groups by Bonferroni/Dunn multiple comparisons tests.
Table 6

Outcome measures according to the length of the preserved pyloric cuff

 

Length of the pyloric cuff

P value (ANOVA)

P value (B/D)

Cohen’s d

≤2.5 cm (n = 34)

3.0–5.0 cm (n = 212)

≥5.5 cm (n = 41)

Main outcome measures

 Change in body weight (%)

−7.0 ± 4.8

−6.6 ± 6.9

−7.1 ± 8.9 %

≥0.1

  

 Physical component summary

51.4 ± 4.9

51.2 ± 5.1

50.3 ± 6.6

≥0.1

  

 Mental component summary

50.0 ± 6.3

50.0 ± 6.3

49.9 ± 5.4

≥0.1

  

 Esophageal reflux subscale

1.9 ± 1.1

1.6 ± 0.7

1.7 ± 1.0

≥0.1

  

 Abdominal pain subscale

1.6 ± 0.6

1.6 ± 0.7

1.7 ± 0.9

≥0.1

  

 Meal-related distress subscale

2.3 ± 0.9

2.0 ± 0.8

2.3 ± 1.1

0.052

0.038a

0.32

 Indigestion subscale

2.0 ± 0.8

1.9 ± 0.9

2.2 ± 1.0

≥0.1

  

 Diarrhea subscale

2.1 ± 1.0

1.7 ± 0.9

2.0 ± 1.1

0.047

0.046b

0.37

 Constipation subscale

2.5 ± 1.0

2.2 ± 1.1

2.4 ± 1.2

≥0.1

  

 Dumping subscale

1.8 ± 0.8

1.7 ± 0.9

1.9 ± 1.2

≥0.1

  

 PGSAS total score

2.0 ± 0.7

1.8 ± 0.7

2.0 ± 0.8

≥0.1

  

 Amount of food ingested per meal

6.8 ± 1.8

7.0 ± 1.8

7.3 ± 2.3

≥0.1

  

 Necessity for additional meals

1.7 ± 0.8

1.7 ± 0.7

2.0 ± 0.9

≥0.1

  

 Quality of ingestion subscale

3.5 ± 0.8

3.8 ± 1.0

3.7 ± 0.7

≥0.1

  

 Ability for working

1.8 ± 1.1

1.8 ± 0.9

1.8 ± 1.0

≥0.1

  

 Dissatisfaction with symptoms

1.8 ± 0.7

1.7 ± 0.9

2.0 ± 1.1

≥0.1

  

 Dissatisfaction at the meal

2.4 ± 1.1

2.1 ± 1.1

2.6 ± 1.2

0.072

0.029a

0.37

 Dissatisfaction at working

1.9 ± 1.1

1.6 ± 0.8

1.9 ± 1.1

0.072

0.060a

0.31

 Dissatisfaction with daily life subscale

2.0 ± 0.8

1.8 ± 0.8

2.1 ± 1.0

0.062

0.026a

0.36

Other outcome measures (symptoms)

 Increased flatus

2.3 ± 1.3

2.2 ± 1.3

2.7 ± 1.5

0.091

0.029a

0.36

 Increased passage of stools

2.1 ± 1.3

1.7 ± 1.1

2.2 ± 1.5

0.021

0.022a

0.35

 Sense of foods sticking

1.8 ± 0.9

1.5 ± 0.8

1.8 ± 1.2

0.046

0.031a

0.33

In ANOVA, a P value less than 0.05 was considered as statistically significant

In Bonferroni/Dunn multiple comparisons, a P value less than 0.0167 was considered as statistically significant

Interpretation of effect size in Cohen’s d: ≥0.20 as small, ≥0.50 as medium, ≥0.80 as large

ANOVA one-way analysis of variance, B/D Bonferroni/Dunn multiple comparisons

a3.0–5.0 cm vs. ≥5.5 cm

b≤2.5 cm vs. 3.0–5.0 cm

Pyloric branch of the vagal nerve preservation

Patients who underwent PPG with preservation of the pyloric branch of the vagal nerve tended to complain of additional food intake necessity and nausea, whereas those without preservation of the pyloric branch of the vagal nerve tended to complain of late dumping symptoms (Table 7); however, these differences were not statistically significant by Student’s unpaired t test. The other PGSAS scales also showed no significant differences between patients with or without preservation of the vagal nerve pyloric branch.
Table 7

Outcome measures depending on the pyloric branch of the vagal nerve preservation

 

Pyloric branch of the vagal nerve preservation

P value

Cohen’s d

Yes (n = 254)

No (n = 40)

Main outcome measures

 Change in body weight (%)

−6.8 ± 7.1

−6.4 ± 5.6

≥0.1

 

 Physical component summary

50.9 ± 5.5

51.7 ± 4.5

≥0.1

 

 Mental component summary

49.8 ± 6.3

50.1 ± 5.1

≥0.1

 

 Esophageal reflux subscale

1.7 ± 0.8

1.6 ± 0.7

≥0.1

 

 Abdominal pain subscale

1.7 ± 0.7

1.6 ± 0.8

≥0.1

 

 Meal-related distress subscale

2.1 ± 0.9

2.1 ± 0.8

≥0.1

 

 Indigestion subscale

2.0 ± 0.9

1.9 ± 0.7

≥0.1

 

 Diarrhea subscale

1.9 ± 1.0

1.7 ± 0.9

≥0.1

 

 Constipation subscale

2.3 ± 1.1

2.1 ± 0.7

≥0.1

 

 Dumping subscale

1.8 ± 0.9

1.8 ± 1.0

≥0.1

 

 PGSAS total score

1.9 ± 0.7

1.8 ± 0.6

≥0.1

 

 Amount of food ingested per meal

7.0 ± 1.9

7.1 ± 1.5

≥0.1

 

 Necessity for additional meals

1.8 ± 0.8

1.5 ± 0.7

0.056

0.35

 Quality of ingestion subscale

3.8 ± 0.9

3.7 ± 1.0

≥0.1

 

 Ability for working

1.8 ± 1.0

1.6 ± 0.7

≥0.1

 

 Dissatisfaction with symptoms

1.8 ± 0.9

1.9 ± 1.0

≥0.1

 

 Dissatisfaction at the meal

2.2 ± 1.1

2.3 ± 1.1

≥0.1

 

 Dissatisfaction at working

1.7 ± 0.9

1.6 ± 0.9

≥0.1

 

 Dissatisfaction for daily life subscale

1.9 ± 0.8

1.9 ± 0.8

≥0.1

 

Other outcome measures (symptoms)

 Nausea and vomiting

1.5 ± 1.0

1.2 ± 0.6

0.058

0.39

 Late dumping symptoms

1.5 ± 1.0

1.9 ± 1.3

0.083

0.29

In unpaired t tests, a P value less than 0.05 was considered as statistically significant

Interpretation of effect size in Cohen’s d: ≥0.20 as small, ≥0.50 as medium, ≥0.80 as large

Discussion

Patients who undergo gastrectomy often suffer from PGS, resulting in a decrease in their QOL [13]. Therefore, function-preserving operations including PPG have been introduced to prevent this syndrome [1, 5, 7]. Here we examined the appropriate indicators and optimal methods for PPG and the effect of various factors on QOL.

We demonstrated that there were significant differences in terms of body weight change, dissatisfaction at the meal, and dissatisfaction with daily life subscales depending on the size of the proximal gastric remnant after PPG. It has been suggested that PGS is primarily caused by impaired function of the remnant stomach. Nomura et al. [14] reported that patients who undergo half resection rather than the more typical two-thirds resection in distal gastrectomy benefit in terms of functional outcomes such as preservation of body weight, food intake volume, and the incidence of esophagitis and gastritis; they speculated that the reservoir function of the remnant stomach is preserved in the half resection group, leading to improved postoperative nutritional status and body composition. Also, better functional outcomes have been reported in patients with a large remnant stomach than in those with a small remnant stomach following proximal gastrectomy for gastric cancer [15]. Our finding, that several symptoms after PPG are worse when the proximal gastric remnant is a quarter the size of the preoperative stomach compared with when it is around a third or more than half the original size, indicates that the preservation of a proximal gastric remnant of sufficient size is recommended, and that careful consideration is needed before applying PPG in cases of a small-sized remnant stomach. In contrast, in patients with weakened peristalsis, an excessively large remnant stomach may render gastric emptying difficult because of the descending position below the anastomosis when it is filled with food.

A recent questionnaire survey of the status of PPG in 148 Japanese institutions reported that layer-to-layer anastomosis (defined as “two-layer anastomosis with mucosal and seromuscular sutures”) is the most representative technique for gastrogastrostomy [16]. Here, we investigated whether the method of anastomosis (hand-sewn anastomosis or mechanical anastomosis using a linear stapler) affected symptoms after PPG. The results indicated that the nausea score was significantly lower in patients who underwent hand-sewn anastomosis than in those that underwent mechanical anastomosis with small effect size (Cohen’s d = 0.43). This finding suggests that the delicate manipulations of hand-sewn anastomosis might avoid deformity of the proximal gastric remnant, and that insufficient flexibility in the anastomotic site caused by the use of staples might contribute to nausea. Although PPG preserves gastric function, patients occasionally have a feeling of gastric fullness after food intake, and some experience long-term retention of food in the residual stomach [16, 17, 18]. Delayed gastric emptying is the most common complaint after PPG, and it manifests as various symptoms including nausea, epigastric fullness, and poor oral intake [7, 17, 19].

Lee et al. [20] performed intracorporeal gastro-gastric anastomosis with mechanical suture devices in laparoscopic PPG (LAPPG) operations on 12 patients, and advocated that this technique has the potential to provide a better QOL following gastric cancer surgery because of the low incidence of morbidity and no stasis; however, the sample size was small. With advances in devices for anastomosis, mechanical anastomosis using a linear stapler, including totally intracorporeal procedures, is likely to become more popular.

According to Japanese gastric cancer treatment guidelines, modification of gastric resection to PPG is recommended for cT1cN0 tumors in the middle portion of the stomach when the distal tumor border is at least 4 cm proximal to the pylorus [21]. The clinical benefits of PPG are considered to be based on the function of the preserved pylorus [22], and it has been proposed that retention of a longer pyloric cuff may be favorable to decrease postoperative symptoms such as delayed gastric emptying. Nakane et al. [23] reported that PPG with the point of transection 2.5 cm rather than 1.5 cm proximal to the pylorus was superior in terms of some postoperative symptoms and weight recovery, indicating that the length of the pyloric cuff has an important role in the motility of the pylorus following PPG. In contrast, Morita et al. [24] reported that there were no significant differences in symptoms, such as dumping syndrome or emptying disturbances, between patients with pyloric cuff lengths 3.0 cm or less and those with lengths more than 3.0 cm. Shibata et al. [17] concluded that it is uncertain what length of pyloric cuff is reasonable for PPG in terms of gastric emptying. Our results showed that there were significant differences in terms of the score for diarrhea subscale, diarrhea, and sense of foods sticking between patients grouped according to the length of pyloric cuff (<2.5, 3.0–5.0, or >5.5 cm) analyzed by ANOVA. Scores for the afore-listed symptoms were lowest in the group with a remnant pyloric cuff length of 3.0–5.0 cm, indicating that patents with cuff lengths outside this range might have increased symptoms after PPG, although the differences between groups by Bonferroni/Dunn testing were of borderline significance. Thus, although the length of the pyloric cuff might be an important factor for PGS, its contribution is still under discussion.

It is widely accepted that the pyloric branch of the vagal nerve is important for normal pyloric function, and that preservation of the vagal nerve prevents gastric retention after PPG. One of the pitfalls of PPG for gastric cancer is considered to be the lack of suprapyloric lymph node dissection with intention to preserve the right gastric artery and the pyloric branch of the vagal nerve. Here, we compared the patients who underwent PPG with or without preservation of the pyloric branch of the vagal nerve. Although there were some differences in a few symptoms between groups with borderline significance, the effect of either preservation or division of the pyloric branch or vagal nerve was small as to effect size.

We recognize the following limitations of the present study. First, there were uneven numbers of patients among the groups because of the retrospective nature of the study, and the groups with inferior outcomes were small. Second, the cross-sectional design of the study did not allow for the inference of cause and effect; further longitudinal studies with a greater number of subjects are required. Additional prospective randomized control studies of PPG operations should be undertaken to further evaluate the factors that minimize PGS.

In conclusion, the size of the remnant stomach following PPG is closely related to the patient’s dissatisfaction with daily life and body weight change. We therefore need to consider the size of the proximal gastric remnant to obtain the optimal function-preserving benefit of PPG. In addition, having a medium length of remnant pyloric cuff may reduce some symptoms after PPG. However, further investigations, including a multicenter prospective randomized controlled trial and larger samples with longer follow-up periods, are needed to verify these conclusions.

Notes

Acknowledgments

This study was supported by a grant from The Jikei University and The Japanese Society for Gastro-surgical Pathophysiology. The authors thank all physicians who participated in this study and the patients whose cooperation made this study possible.

Conflict of interest

The authors declare no conflicts of interest.

References

  1. 1.
    Hiki N, Sano T, Fukunaga T, Ohyama S, Tokunaga M, Yamaguchi T. Survival benefit of pylorus-preserving gastrectomy in early gastric cancer. J Am Coll Surg. 2009;209:297–301.CrossRefPubMedGoogle Scholar
  2. 2.
    Katai H. Function-preserving surgery for gastric cancer. Int J Clin Oncol. 2006;11:357–66.CrossRefPubMedGoogle Scholar
  3. 3.
    Maki T, Shiratori T, Hatafuku T, Sugawara K. Pylorus-preserving gastrectomy as an improved operation for gastric ulcer. Surgery (St. Louis). 1967;61:838–45.Google Scholar
  4. 4.
    Hiki N, Kaminishi M. Pylorus-preserving gastrectomy in gastric cancer surgery: open and laparoscopic approaches. Langenbecks Arch Surg. 2005;390:442–7.CrossRefPubMedGoogle Scholar
  5. 5.
    Morita S, Katai H, Saka M, Fukagawa T, Sano T, Sasako M. Outcome of pylorus-preserving gastrectomy for early gastric cancer. Br J Surg. 2008;95:1131–5.CrossRefPubMedGoogle Scholar
  6. 6.
    Ikeguchi M, Hatada T, Yamamoto M, Miyake T, Matsunaga T, Fukuda K, et al. Evaluation of a pylorus-preserving gastrectomy for patients preoperatively diagnosed with early gastric cancer located in the middle third of the stomach. Surg Today. 2010;40:228–33.CrossRefPubMedGoogle Scholar
  7. 7.
    Nunobe S, Sasako M, Saka M, Fukagawa T, Katai H, Sano T. Symptom evaluation of long-term postoperative outcomes after pylorus-preserving gastrectomy for early gastric cancer. Gastric Cancer. 2007;10:167–72.CrossRefPubMedGoogle Scholar
  8. 8.
    Jiang X, Hiki N, Nunobe S, Fukunaga T, Kumagai K, Nohara K, et al. Long-term outcome and survival with laparoscopy-assisted pylorus-preserving gastrectomy for early gastric cancer. Surg Endosc. 2011;25:1182–6.CrossRefPubMedGoogle Scholar
  9. 9.
    Tokuda Y, Okubo T, Ohde S, Jacobs J, Takahashi O, Omata F, et al. Assessing items on the SF-8 Japanese version for health-related quality of life: a psychometric analysis based on the nominal categories model of item response theory. Value Health. 2009;12:568–73.CrossRefPubMedGoogle Scholar
  10. 10.
    Svedlund J, Sjödin I, Dotevall G. GSRS: a clinical rating scale for gastrointestinal symptoms in patients with irritable bowel syndrome and peptic ulcer disease. Dig Dis Sci. 1988;33:129–34.CrossRefPubMedGoogle Scholar
  11. 11.
    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 post-gastrectomy patients. Gastric Cancer 2014 (in press). doi: 10.1007/s10120-014-0344-4.
  12. 12.
    Nakada K, Ikeda M, Takahashi M, Kinami S, Yoshida M, Uenosono Y, et al. Development and validation of PGSAS-45, an integrated questionnaire to assess postgastrectomy syndrome. Gastroenterology. 2013;144:S1111.Google Scholar
  13. 13.
    Kumagai K, Shimizu K, Yokoyama N, Aida S, Arima S, Aikou T. Japanese Society for the Study of Postoperative Morbidity after Gastrectomy. Questionnaire survey regarding the current status and controversial issues concerning reconstruction after gastrectomy in Japan. Surg Today. 2012;42:411–8.CrossRefPubMedGoogle Scholar
  14. 14.
    Nomura E, Lee SW, Bouras G, Tokuhara T, Hayashi M, Hiramatsu M, et al. Functional outcomes according to the size of the gastric remnant and type of reconstruction following laparoscopic distal gastrectomy for gastric cancer. Gastric Cancer. 2011;14:279–84.CrossRefPubMedGoogle Scholar
  15. 15.
    Nomura E, Lee SW, Tokuhara T, Kawai M, Uchiyama K. Functional outcomes according to the size of the gastric remnant and type of reconstruction following open and laparoscopic proximal gastrectomy for gastric cancer. Hepatogastroenterology. 2012;59:1677–81.PubMedGoogle Scholar
  16. 16.
    Shibata C, Saijo F, Kakyo M, Kinouchi M, Tanaka N, Sasaki I, et al. Current status of pylorus-preserving gastrectomy for the treatment of gastric cancer: a questionnaire survey and review of literatures. World J Surg. 2012;36:858–63.CrossRefPubMedGoogle Scholar
  17. 17.
    Hiki N, Shimoyama S, Yamaguchi H, Kubota K, Kaminishi M. Laparoscopy-assisted pylorus-preserving gastrectomy with quality controlled lymph node dissection in gastric cancer operation. J Am Coll Surg. 2006;203:162–9.CrossRefPubMedGoogle Scholar
  18. 18.
    Park do J, Lee HJ, Jung HC, Kim WH, Lee KU, Yang HK. Clinical outcome of pylorus-preserving gastrectomy in gastric cancer in comparison with conventional distal gastrectomy with Billroth I anastomosis. World J Surg. 2008;32:1029–1036.Google Scholar
  19. 19.
    Isozaki H, Okajima K, Momura E, Ichinona T, Fujii K, Izumi N, et al. Postoperative evaluation of pylorus-preserving gastrectomy for early gastric cancer. Br J Surg. 1996;83:266–9.CrossRefPubMedGoogle Scholar
  20. 20.
    Lee SW, Bouras G, Nomura E, Yoshinaka R, Tokuhara T, Nitta T, et al. Intracorporeal stapled anastomosis following laparoscopic segmental gastrectomy for gastric cancer: technical report and surgical outcomes. Surg Endosc. 2010;24:1774–80.CrossRefPubMedGoogle Scholar
  21. 21.
    Japanese Gastric Cancer Association. Japanese gastric cancer treatment guidelines 2010, ver. 3. Gastric Cancer. 2011;14:113–23.CrossRefGoogle Scholar
  22. 22.
    Nishikawa K, Kawahara H, Yumiba T, Nishida T, Inoue Y, Ito T, et al. Functional characteristics of the pylorus in patients undergoing pylorus-preserving gastrectomy for early gastric cancer. Surgery (St. Louis). 2002;131:613–24.CrossRefGoogle Scholar
  23. 23.
    Nakane Y, Michiura T, Inoue K, Sato M, Nakai K, Yamamichi K. Length of the antral segment in pylorus-preserving gastrectomy. Br J Surg. 2002;89:220–4.CrossRefPubMedGoogle Scholar
  24. 24.
    Morita S, Sasako M, Saka M, Fukagawa T, Sano T, Katai H. Correlation between the length of the pyloric cuff and postoperative evaluation after pylorus-preserving gastrectomy. Gastric Cancer. 2010;13:109–16.CrossRefPubMedGoogle Scholar

Copyright information

© The International Gastric Cancer Association and The Japanese Gastric Cancer Association 2014

Authors and Affiliations

  • Tsutomu Namikawa
    • 1
  • Naoki Hiki
    • 2
  • Shinichi Kinami
    • 3
  • Hiroshi Okabe
    • 4
  • Takashi Urushihara
    • 5
  • Hiroshi Kawahira
    • 6
  • Norimasa Fukushima
    • 7
  • Yasuhiro Kodera
    • 8
  • Takeyoshi Yumiba
    • 9
  • Atsushi Oshio
    • 10
  • Koji Nakada
    • 11
  1. 1.Department of SurgeryKochi Medical SchoolKochiJapan
  2. 2.Department of Gastroenterological Surgery, Gastroenterological Center, Cancer Institute HospitalJapanese Foundation for Cancer ResearchTokyoJapan
  3. 3.Department of Surgical OncologyKanazawa Medical UniversityIshikawaJapan
  4. 4.Department of SurgeryKyoto University Graduate School of MedicineKyotoJapan
  5. 5.Department of Gastroenterological, Breast and Transplant SurgeryHiroshima Prefectural HospitalHiroshimaJapan
  6. 6.Department of Frontier Surgery, Graduate School of MedicineChiba UniversityChibaJapan
  7. 7.Department of SurgeryYamagata Prefectural Central HospitalYamagataJapan
  8. 8.Department of Gastroenterological SurgeryNagoya University Graduate School of MedicineAichiJapan
  9. 9.Department of SurgeryOsaka Kosei-Nenkin HospitalOsakaJapan
  10. 10.Faculty of Letters, Arts and SciencesWaseda UniversityTokyoJapan
  11. 11.Department of SurgeryThe Jikei University School of MedicineTokyoJapan

Personalised recommendations