Predictive factors for Roux stasis syndrome after distal gastrectomy with Roux-en-Y reconstruction in gastric cancer patients: A retrospective comparative cohort study

doi:10.21203/rs.3.rs-1981675/v1

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Predictive factors for Roux stasis syndrome after distal gastrectomy with Roux-en-Y reconstruction in gastric cancer patients: A retrospective comparative cohort study

https://doi.org/10.21203/rs.3.rs-1981675/v1

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Background: Roux-en-Y (R-Y) reconstruction after distal gastrectomy in gastric cancer patients can cause Roux stasis syndrome (RSS), the pathogenic mechanism of which is unclear. This study retrospectively evaluated the risk factors for RSS.

Material and methods: Patients who were pathologically diagnosed with gastric cancer and underwent distal gastrectomy with R-Y reconstruction between March 2014 and March 2021 were retrospectively analyzed. RSS occurrence was evaluated and examined for correlations with demographic and clinicopathological data. A nomogram was built using “R” package.

Results: RSS was observed in 20/220 patients (9.1%), and there was a significant difference between males and females (11.9% vs. 3.9%, p = 0.049). The incidence of RSS tended to be higher in underweight (body mass index (BMI) < 18.5 kg/m2) and obese (BMI ≥ 28.0 kg/m2) patients (p = 0.043). The rates of smoking and nerve invasion were higher in patients with RSS, but statistical significance was not reached. There were no significant differences in other factors. A nomogram was built in which sex, BMI group, nerve invasion and smoking were incorporated to predict RSS (AUC = 0.71).

Conclusions: Both male sex and a polarized BMI are independent risk factors for RSS after distal gastrectomy with R-Y reconstruction in gastric cancer patients. A nomogram including sex, BMI group, nerve invasion and smoking can predict RSS occurrence.

Trial registration number:

NCT04919577 (ClinicalTrials.gov)

stasis syndrome

distal gastrectomy

anastomosis

Roux-en-Y

gastric cancer

Globally, gastric cancer has been reported to be the fifth most common and fatal cancer, with a 2-fold higher risk in men and the highest incidence in East Asia[1]. In addition to Billroth I and Billroth II operations, Roux-en-Y (R-Y) reconstruction is a common reconstruction approach in distal gastrectomy for gastric cancer[2]. It has the advantage of diminishing gastrointestinal reflux compared to other operating methods[3]. In addition, R-Y anastomosis is not limited by the size of the residual stomach. Nevertheless, some patients who undergo R-Y reconstruction reportedly develop Roux stasis syndrome (RSS)[2, 4].

RSS is one form of gastrointestinal dysfunction with symptoms including abdominal pain, vomiting and post-prandial nausea without mechanical obstruction[5]. The incidence of RSS ranges from 10–30%, while the pathogenic mechanism of this syndrome is still unclear[2, 6, 7]. At present, the disruption of intestinal integrity and enteric neural continuity resulting from transection of the jejunum in R-Y reconstruction, which has been verified via high-resolution manometry, is considered to be the main cause of RSS[8]. The proximal duodenum acts as a pacemaker and promotes peristalsis of the small intestine. The jejunal crosscut separates the distal small intestine from the natural pacemaker located in the duodenum, which may lead to the presence of ectopic pacemakers elsewhere in the small intestine, causing antiperistalsis of the output loop[9]. In addition, after R-Y reconstruction, food does not pass through the duodenum, which affects the mixing of food with bile and pancreatic juice, causing slow transport in the output loop.

However, the risk factors for RSS remain largely unknown[10]. In this study, the risk factors for RSS based on a single-center clinical database were evaluated to obtain further insight into RSS.

This work has been reported in line with the STROCSS criteria[11].

2.1. Patient Selection

Consecutive patients who were pathologically diagnosed with gastric cancer and underwent distal gastrectomy with R-Y reconstruction between March 2014 and March 2021 were retrospectively selected (the detailed screening process is shown in Fig. 1). We followed up each patient for at least 3 months after surgery.

The exclusion criteria for this study were as follows: (1) patients with distant metastasis, (2) patients with gastroparesis pre-operatively; (3) patients who underwent palliative surgery, (4) patients who died within 14 days after the operation, and (5) patients with primary malignant disease in organs other than the stomach.

2.2. Surgical Procedure

All patients underwent mechanical bowel preparation one day before surgery and were deprived of water and fasting 8 hours before surgery. R-Y reconstruction was performed after standard distal gastrectomy and D2 lymph node dissection. About 3/4 stomach was removed. The R-Y reconstruction process proceeded as follows. First, the jejunum was dissected 20 cm (average value) distal to Treitz’s ligament. Second, a side-to-side antecolic gastrojejunostomy was created using a linear stapler between the gastric stump and the distal segment of the jejunum. Finally, an end-to-side or side-to-side jejunostomy was performed in the output limb at approximately 37 cm (average value) distal to the gastrojejunostomy (Fig. 2). Cholecystectomy was performed if the patient had gallbladder-related disease. There were 130 cases of open surgery and 90 cases of laparoscopic surgery. The operations were all performed by experienced surgeons with the same training in our center.

2.3. Data Collection

We divided these patients into two groups depending on whether RSS occurred and retrospectively analysed the following items: sex, age, body mass index (BMI), smoking, diabetes, carcinoembryonic antigen (CEA) level, hypoproteinaemia, hyperlipidaemia, operation approach, operation time, cholecystectomy, length of the input and output loops, intestinal anastomosis approach, pathological T (pT) stage, lymph node metastasis, pathological stage, lymphovascular invasion, nerve invasion and postoperative hospital stay. According to the standard classification of BMI in China[12], we divided patients into three groups: the underweight group (BMI < 18.5 kg/m2), obesity group (BMI ≥ 28.0 kg/m2) and normal group (18.5 kg/m2 ≥ BMI < 28.0 kg/m2). Tumour stage was defined according to the American Joint Committee on Cancer staging system (8th edition).

2.4. Identification of RSS

We defined RSS as (1) the presence of symptoms such as nausea, vomiting, or abdominal fullness, (2) refasting after a liquid or semi-liquid diet, and (3) imaging methods (X-ray, CT, upper gastroenterography) confirmed the absence of mechanical obstruction. All three conditions were required to be met at the same time.

Two gastroenterologists screened each patient one by one according to the RSS definition. A third gastroenterologist discussed the patients with inconsistent results and jointly confirmed whether the patient had RSS.

2.5. Statistical Analysis

Statistical analysis was performed using the SPSS Statistics version 26.0 software program (IBM Corp., Armonk, NY, USA). Qualitative data were compared using the chi-square test or Fisher’s exact test. Quantitative data were compared using a nonparametric test (the Mann-Whitney U test). Variables with p < 0.1 in the univariate analysis and those that may be clinically related to RSS were included in the multivariate binary logistic regression analysis (forward conditional). The Box-Tidwell method was used to verify that the continuous independent variable and the dependent variable logit transform value had a linear relationship (p > 0.05). Linear regression was used to verify that there was no multicollinearity between each independent variable (tolerance > 0.1, variance inflation factor (VIF) < 10). Based on the logistic regression results, a nomogram for predicting RSS occurrence after radical gastrectomy for distal gastrectomy with R-Y anastomosis was established, and the performance of the nomogram was quantified to determine its discrimination and calibration abilities. The model was internally validated using the 1,000 bootstrapping method to obtain relatively unbiased estimates. The nomogram was built using the "rms" package in R software (version 3.1.2.; The R Foundation for Statistical Computing, Vienna, Austria). All tests were bilateral, and P < 0.05 was considered statistically significant.

All patients underwent open or laparoscopic radical distal gastrectomy with D2 lymph node dissection and R-Y reconstruction. A total of 220 patients were enrolled in this study (143 males and 77 females), and RSS was observed in 20 of 220 patients (9.1%).

3.1. Univariate analysis of risk factors

The risk factors were analysed between the RSS group and the non-RSS group. A significant difference in sex was observed between the two groups, with 17 males and 3 females developing RSS (p = 0.049). The differences in age, BMI, smoking, diabetes, CEA level, hypoproteinaemia, hyperlipidaemia, operation time, approach, cholecystectomy, length of the input loops, length of the output loops, intestinal anastomosis approach, pT stage, lymph node metastases, pathological stage and lymphovascular invasion were not significant. The rates of smoking and nerve invasion were higher in the RSS group, but statistical significance was not reached. Interestingly, when we divided patients into three groups according to BMI, a significant difference was observed, with more underweight and obese patients developing RSS (p = 0.047) (Table 1).

Table 1

Univariate analysis of risk factors for RSS after distal gastrectomy with Roux-en-Y anastomosis.

Variable	RSS (+) (n = 20)			RSS (-) (n = 200)		p-value
Sex						0.049
Male	17 (85.0%)			126 (63.0%)
Female	3 (15.0%)			74 (37.0%)
Age (years)	66.0 ± 15.0			63.7 ± 12.0		0.297
BMI (kg/m²)	22.8 ± 3.2			23.1 ± 2.9		0.623
BMI group (Kg/m²)						0.047^a
＜18.5	3 (15.0%)			12 (6.0%)
≥28.0	2 (10.0%)			5 (2.5%)
18.5-27.9	15 (75.0%)			183 (91.5%)
Smoking						0.082
Yes	9 (45.0%)			53 (26.6%)
No	11 (55.0%)			146 (73.4%)
Diabetes						1.000^a
Yes	3 (15.0%)			37 (18.6%)
No	17 (85.0%)			162 (81.4%)
High CEA					0.308
Yes	9 (50.0%)			74 (37.8%)
No	9 (50.0%)			122 (62.2%)
Hypoproteinemia						0.972
Yes	8 (40.0%)			78 (39.6%)
No	12 (60.0%)			119 (60.4%)
Hyperlipidemia						0.599
Yes	10 (52.6%)			88 (46.3%)
No	9 (47.4%)			102 (53.7%)
Operation time (min)	266.9 ± 63.2			275.1 ± 76.9		0.702
Approach						0.573
Open	13 (65.0%)			117 (58.5%)
Laparoscopic	7 (35.0%)			83 (41.5%)
Cholecystectomy						0.285^a
Yes	2 (10.5%)			10 (5.1%)
No	17 (89.5%)			187 (94.9%)
Length of Input loops (cm)			19.8 ± 3.0	20.2 ± 3.3		0.641
Length of Output loops (cm)		35.5 ± 4.8		37.4 ± 6.3		0.130
Intestinal anastomosis						0.480^a
Side-to-side	18 (94.7%)			169 (87.1%)
End-to-side	1 (5.3%)			25 (12.9%)
pT stage						0.858^a
T0	0 (0.0%)			4 (2.0%)
T1	8 (40.0%)			54 (27.4%)
T2	3 (15.0%)			36 (18.3%)
T3	4 (20.0%)			46 (23.4%)
T4	5 (25.0%)			57 (28.9%)
Lymph node metastases						0.277
Yes	13 (65.0%)			103 (52.3%)
No	7 (35.0%)			94 (47.7%)
Pathological stage						0.941^a
0	0 (0.0%)			4 (2.0%)
I	7 (35.0%)			71 (36.0%)
II	4 (20.0%)			46 (23.4%)
III	9 (45.0%)			76 (38.6%)
Lymphovascular invasion						0.704
Yes	9 (45.0%)			80 (40.6%)
No	11 (55.0%)			117 (59.4%)
Nerve invasion						0.056
Yes	11 (55.0%)			66 (33.5%)
No	9 (45.0%)			131 (66.5%)

BMI, body mass index; CEA, carcinoembryonic antigen; pT, pathological T-staging.

Data are present as number (%) and mean ± standard deviation.

^a means Fischer's exact test.

3.2. Multivariate analysis of risk factors

Variables with P < 0.1 in the univariate analysis (sex, BMI group, smoking, and nerve invasion) and those that may be clinically related to RSS (age, hyperlipidaemia, anastomosis approach, length of the output loops, cholecystectomy, lymph node metastases and lymphovascular invasion) were included in the multivariate analysis. Finally, a statistically significant logistic model was obtained (χ2 = 10.452, p = 0.015), with a high percentage accuracy in classification (90.9%) and goodness of fit (Hosmer-Lemeshow test, p = 0.912). Consistent with the results of the univariate analysis, both sex and BMI group were revealed as independent risk factors for RSS (p = 0.049 and p = 0.043, respectively) (Table 2).

Table 2

Multivariate analysis of risk factors for RSS after distal gastrectomy with Roux-en-Y anastomosis.

Variable	β-coefficient	OR	OR 95%CI	p value
Sex	1.543	4.679	（1.004, 21.818）	0.049
(Male/Female)	1.543	4.679	（1.004, 21.818）	0.049
BMI group (kg/m²)				0.043
(<18.5/18.5-27.9)	1.575	4.829	(1.099, 21.210)	0.037
(≥28.0/18.5-27.9)	1.464	4.324	(0.742, 25.187)	0.103
Age				0.692
Smoking (Yes/No)				0.246
Hyperlipidemia (Yes/No)				0.609
Approach (Open/Laparoscopic)				0.476
Length of Output loops				0.209
Cholecystectomy (Yes/No)				0.267
Lymph node metastases (Yes/No)				0.355
Intravascular cancer thrombus (Yes/No)				0.972
Nerve invasion (Yes/No)				0.083

BMI, body mass index.

3.3. Nomogram construction and validation

Sex, BMI group, nerve invasion and smoking were used to construct the nomogram (Figure 3.1). The concordance index of our model was 0.710, representing a comparative discrimination performance. Calibration was assessed by graphically inspecting plots that compared the observed outcome frequencies with the predicted probabilities, as shown in Figure 3.2. The calibration curve revealed that the bias-corrected line was close to the ideal line, indicating decent goodness of fit.

Compared with other reconstruction methods, RSS is the most frequent surgical complication after distal gastrectomy with R-Y anastomosis for gastric cancer[13, 14]. In our study, the incidence of RSS for R-Y anastomosis was 9.1%, consistent with previous studies[16, 17]. A significantly high rate of RSS was observed to be associated with male sex and a polarized BMI in our study.

Our study showed that male sex was an independent risk factor for RSS. However, previous studies indicated no sex difference or female predominance[15, 16, 18, 19]. Our results were consistent with our observations from clinical practice. There are several possible reasons for these findings. First, the majority of the smokers were males. Smoking was identified as a potential risk factor for RSS in our univariate analysis (p = 0.082). When we excluded sex in the multivariate analysis, smoking became an independent risk factor for RSS (p = 0.04). Previous studies indicated that smoking increased the levels of prostaglandins, which have been proven to inhibit gastric motility through slow wave disruption[20]. Furthermore, vagotomy seems to be the major cause of slow gastric emptying[21], and a previous study showed that the vagal activity was larger in females than in males[22]. The higher incidence of RSS in males may be due to decreased vagal function after radical gastrectomy for distal gastric cancer.

Previous studies showed a high BMI in patients with RSS[15], consistent with our results. First, regardless of the operative approach, patients with obesity themselves have a higher incidence of gastrointestinal dysfunction than patients of normal weight due to neurohormonal factors, such as increased leptin levels and hyperactivation of the sympathetic nerve[23–26]. Second, obese patients have more visceral fat and more local inflammatory exudation caused by fat fragmentation in the surgical area, which affects postoperative gastrointestinal function recovery, mimicking the mechanism of the ileus[27]. Third, antecolic reconstruction is performed on all the patients in our center, and the hypertropic mesocolon of obese patients may cause the output loop to be angled in front of the colon, affecting food transportation. Interestingly, we found that patients in the RSS group had a polarized BMI. Therefore, not only obese patients but also lean patients are at an increased risk for RSS. In addition, for the prediction of RSS, underweight (BMI < 18.5 kg/m2) had a more statistically significant difference and a larger odds ratio (OR = 4.829 (1.099, 21.210)) in the multivariate analysis and a higher score in the nomogram than obesity (BMI ≥ 28.0 kg/m2). As most of the previous studies analysed BMI only as a continuous variable, neglecting to classify patients as underweight, normal or obese, the lack of a difference in BMI between groups with or without RSS may have been misleading[16]. We performed a chi-square test to analyse differences according to the BMI group and hypoproteinaemia, and no significant difference was observed (p = 0.599). This result indicated that patients in the underweight group did not have hypoproteinaemia. Previous studies indicated that low weight was associated with gastroparesis[28]. We hypothesize that underweight patients tend to have poor gastrointestinal function, which may increase the incidence of postoperative gastrointestinal dysfunction.

Previous studies have shown that the average Roux-Y limb length in patients with RSS is 41 cm, which is longer than that in patients without RSS (36 cm), and a Roux-Y limb with a length of more than 40 cm may increase the incidence of RSS[19]. Other studies suggested that the Roux limb was an isolated 40 cm segment of the jejunum that was not under appropriate electrical control[29]. Therefore, the Roux limb became dysfunctional. Although our results also showed a longer output loop in the RSS group, the difference was not significant (37.4 cm vs. 35.5 cm, p = 0.209). This may be because output loops in our center are mostly concentrated in 35 to 40 cm, resulting in poor discrimination between the two groups. In addition, the length of the output loop was not accurately measured because this study was performed retrospectively. It has also been reported that laparoscopic surgery is a risk factor for postoperative gastrointestinal dysfunction, suggesting that gastroparesis after laparoscopic surgery may be caused by energy-based devices[18]. However, our results showed no significant difference in the incidence of RSS after laparoscopic and open surgery.

A nomogram that included sex, BMI group, nerve invasion and smoking was created to evaluate the risk of RSS. On the one hand, sex and BMI group, which showed a significant difference in the univariate and multivariate analyses, were included in this model. On the other hand, we also included nerve invasion and smoking, which may be clinically related to RSS, to improve the prediction performance of the nomogram. This nomogram could help clinicians identify patients at high risk of developing RSS, allow patients to receive a good psychological evaluation in advance and remind clinicians to take measures to reduce the onset of RSS, such as prolong nasogastric tube decompression in patients with high risk and start pro-kinetic agents in the immediate post-operative period. Furthermore, our nomogram contains routine clinical variables that are readily available to clinicians, thus making it easy to adopt in practice.

Our study still has some potential limitations. First, this was a retrospective study. Second, antecolic reconstruction is the only approach used in our center; therefore, we were unable to compare retrocolonic and antecolic reconstruction. Some studies have shown that retrocolonic reconstruction is more likely to increase the risk of mechanical outflow obstruction and impede the smooth activities of the residual stomach, increasing the risk of RSS. In addition, some researchers have proposed that antiperistaltic anastomosis is a risk factor for RSS. However, all the gastrointestinal anastomoses in our center were isoperistaltic anastomoses, so we could not compare isoperistaltic and antiperistaltic anastomoses. Finally, our nomogram was not externally validated; thus, its effectiveness could not be determined. Therefore, a multi-center and large-sample cohort study should be proposed to further evaluate the risk factors for RSS after distal gastrectomy with R-Y reconstruction in patients with gastric cancer.

For patients with gastric cancer, both sex and BMI group are independent risk factors for RSS after distal gastrectomy with R-Y reconstruction. Male sex, underweight and obesity were associated with a significantly higher rate of RSS. We created a nomogram in which sex, BMI group, nerve invasion and smoking were included to predict RSS.

Funding

This work was supported by grants from the National Natural Science Foundation of China (Grant No.91959110), Natural Science Foundation of Beijing Municipality (Grant NO.7204324) and National multidisciplinary cooperative diagnosis and treatment capacity building project for major diseases: comprehensive diagnosis and treatment of gastrointestinal tumours.

Conflicts of interest

The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.

Author Contributions

All authors contributed to the study conception and design. Material preparation, data collection and analysis were performed by Yan Meng, Yanpeng Ma, Ruize Qu, Junren Ma, Hsinyi Lin and Siyi Lu. The first draft of the manuscript was written by Yan Meng, Yanpeng Ma and Ruize Qu and all authors commented on previous versions of the manuscript. All authors read and approved the final manuscript.

Data Availability

Dataset available from the Mendeley Data. ma, yanpeng (2021), “RSS”, Mendeley Data, V1, DOI: 10.17632/g86xsmc59b.1.

Ethics approval

This retrospective chart review study involving human participants was in accordance with the 1964 Helsinki Declaration and its later amendments or comparable ethical standards. Ethical approval for this study was obtained from the medical ethics research committee of our centre (IRB00006761-M2019173).

Consent to participate

Informed consent was obtained from all individual participants included in the study.

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No competing interests reported.

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Predictive factors for Roux stasis syndrome after distal gastrectomy with Roux-en-Y reconstruction in gastric cancer patients: A retrospective comparative cohort study

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Abstract

Figures

1. Introduction

2. Material And Methods

2.1. Patient Selection

2.2. Surgical Procedure

2.3. Data Collection

2.4. Identification of RSS

2.5. Statistical Analysis

3. Results

3.1. Univariate analysis of risk factors

3.2. Multivariate analysis of risk factors

3.3. Nomogram construction and validation

4. Discussion

5. Conclusion

Declarations

References

Additional Declarations

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