Risk Factors for Reoperation Following Radical Gastrectomy in Gastric Cancer Patients

Abstract

Background

Reoperation due to elective surgery complications is very mentally, physically, and economically detrimental to patients. This study investigated the potential risk factors associated with early reoperation after radical gastrectomy in gastric cancer patients and included an in-depth analysis of these risk factors.

Methods

This retrospective study reviewed 1568 patients with gastric cancer. Grade 3 or greater complications were defined as severe. Any factors related to reoperation after radical gastrectomy were analyzed in patients with severe local complications.

Results

Among 1537 patients undergoing radical gastrectomy, 115 (7.5%) patients had severe postoperative complications, 98 (6.38%) of whom experienced severe local complications. The most common local complication was anastomotic leakage (31, 2.02%), followed by intra-abdominal abscess (30, 1.95%), pancreatic leakage (22, 1.43%), duodenal stump leakage (18, 1.17%), intra-abdominal bleeding (12, .78%), intraluminal bleeding (8, .52%), small bowel obstruction (5, .32%), and chyle leakage (3, .19%). Of these patients, 26 (1.69%) underwent reoperation, and 6 (.39%) died. In the univariate analysis of clinical factors related to reoperation, intra-abdominal bleeding and small bowel obstruction were risk factors for reoperation, and intra-abdominal bleeding (odds ratio [OR] = 9.57, confidence interval [CI] = 2.65-40.20, P < .001) and small bowel obstruction (OR = 19.14, CI = 2.60-390.13, P = .011) were independent risk factors associated with reoperation in the multivariate analysis.

Conclusion

Intra-abdominal bleeding and small bowel obstruction are independent risk factors for reoperation following radical gastrectomy. Patients with postoperative intra-abdominal bleeding and small bowel obstruction need to be warned about reoperation.

Keywords

gastric cancer radical gastrectomy complications reoperation risk factors

Introduction

Gastrectomy with lymphadenectomy is considered the core of curative treatment for patients with gastric cancer.^1,2 However, unfortunately, 9.8∼31.1% of patients experience complications following gastrectomy.^3-6 These postoperative complications, especially surgery-related local complications, not only increase medical expenses and the length of the hospital stay but also constitute the main causes of reoperation and short-term mortality after gastrectomy.^7,8 Furthermore, postoperative complications requiring reoperation are very detrimental for both surgeons and patients because these complications directly affect the patient’s quality of life and survival.

For this reason, many surgeons have made significant efforts to reduce postoperative complications. As a result, many studies have assessed the incidence rates of postoperative complications and the risk factors and treatment methods associated with these complications.^9-14 However, there is limited information on the risk factors associated with reoperation following radical gastrectomy. Surgeons can predict and avoid operative mortality by understanding the factors affecting reoperation.^15-17

In this study, we analyzed the characteristics of patients who underwent reoperation and identified the risk factors for early reoperation after radical gastrectomy. In addition, an in-depth assessment of these risk factors was conducted.

Materials and Method

Patients and Data Source

A total of 1568 patients with histologically proven gastric cancer underwent surgery from January 2009 to December 2018 at two institutions. We retrospectively reviewed these patients’ electronic medical records. Patients with stage IV gastric cancer and those who underwent palliative surgery without gastrectomy and received neoadjuvant chemotherapy were excluded. A total of 1537 patients underwent curative radical gastrectomy for gastric cancer. Patients were classified according to the severity of postoperative complications. To analyze the characteristics of patients who underwent reoperation due to local complications, we screened patients with severe local complications, except for patients with wound problems alone. The study flowchart is shown Figure 1.

The following clinical data of all patients were collected and analyzed: the data included patient demographics (age, sex, body mass index (BMI), and underlying disease), operation data (operation time, American Society of Anesthesiologists score, operation type, extent of gastrectomy, lymph node dissection, and combined organ resection), clinicopathological results based on the eighth edition American Joint Committee on Cancer tumor-node-metastasis staging system,¹⁸ and progress of hospitalization (hospital days, postoperative complications, mortality, and reoperation). This study was approved by the Institutional Review Board of our institution (GNUH 2020-12-010).

Definition of Complications and Lymphadenectomy

Postoperative complications were defined as any deviations from the normal postoperative recovery course and were graded according to the Claven-Dindo Classification system.¹⁹ Grade 3 or greater complications were defined as severe complications. In addition, postoperative complications were divided into local complications and systemic complications. Local complications were defined as complications related to surgical techniques near the surgical site, such as wounds or intra-abdominal injury. Systemic complications were defined as complications not related to the surgical site.²⁰ Patients who underwent reoperation were defined as the reoperation group, and those who did not undergo reoperation were defined as the conservative group.

The recorded complications and their diagnostic criteria were as follows:

Anastomotic leakage: leakage confirmed by radiographic confirmation or bowel content seen in drainage.

Intra-abdominal bleeding: blood seen in drainage and a continuously decreasing hemoglobin level with or without hypotension and tachycardia or with radiographic confirmation.

Intraluminal bleeding: blood seen in the gastric tube and a continuously decreasing hemoglobin level with or without hypotension and tachycardia with endoscopic confirmation.

Small bowel obstruction: clinical symptoms with radiographic confirmation.

Intra-abdominal abscess: clinical symptoms with radiographic confirmation.

Pancreatic leakage: drain output of any measurable volume after postoperative day 3 with an amylase level greater than 3 times the upper limit of the normal serum level.

Chyle leakage: drain output of milky-colored fluid after postoperative day 3 with a triglyceride content ≥ 110 mg/dL.

The definition of lymphadenectomy follows Japanese gastric cancer treatment guidelines 2018 (fifth edition)²

Total gastrectomy

D1: No. 1-7, D1+: D1 + No. 8a, 9, 11p, D2: D1 + No. 8a, 9, 11p, 11d, 12a

Subtotal gastrectomy

D1: No. 1, 3, 4 sb, 4d, 5, 6, 7, D1+: D1 + No. 8a, 9, D2: D1 + No. 8a, 9, 11p, 12a.

Statistical Analysis

We analyzed the continuous variables using Student’s t test or Mann-Whitney test and the categorical variables using Fisher’s exact test or chi-square test as appropriate. Univariate and multivariate logistic regression analyses were performed to assess any clinical factors associated with reoperation to identify the risk factors for reoperation following gastrectomy. All values are expressed as the mean ± standard deviation or median (interquartile range, Q1, Q3). All data were analyzed using R (version 4.0.0, R Foundation for Statistical Computing, Vienna, Austria) statistical software. All tests were two-sided, and differences with P values < .05 were considered to be statistically significant for all analyses.

Results

Patient Demographics and Surgical Outcomes

Among the 1537 patients who underwent radical gastrectomy, 115 (7.5%) had severe postoperative complications, 98 (6.38%) of which were severe local complications. The demographics and clinicopathological factors of patients with severe local complications are summarized in Table 1. The most common local complication was anastomotic leakage (31, 2.02%), followed by intra-abdominal abscess (30, 1.95%), pancreatic leakage (22, 1.43%), duodenal stump leakage (18, 1.17%), intra-abdominal bleeding (12, .78%), intraluminal bleeding (8, .52%), small bowel obstruction (5, .32%), and chyle leakage (3, .19%). The overall reoperation and mortality rates due to local complications were 26% (1.69%) and 6% (.39%), respectively. The surgical outcomes are described in Table 2.

Table 1.

Patient Characteristics With or Without Severe Local Complications.

Variable	Total (N = 1537)	No (N = 1439, 93.62%)	Yes (N = 98, 6.38%)	P-value
Age, y	63.7 ± 11.8	63.6 ± 11.8	65.7 ± 11.8	.087
Sex (M:F)				.002
Male	1097 (71.4%)	1013 (70.4%)	84 (85.7%)
Female	440 (28.6%)	426 (29.6%)	14 (14.43%)
BMI (kg/m²)	23.2 ± 4.8	23.2 ± 4.9	23.0 ± 3.2	.523
Hospital days, d	14.7 ± 22.8	12.7 ± 20.4	44.3 ± 33.4	< .001
Underlying disease				.259
Yes	661 (43.0%)	613 (42.6%)	48 (49.0%)
No	876 (57.0%)	826 (57.4%)	50 (51.0%)
Operation time, min	264.6 ± 83.1	261.9 ± 80.4	304.7 ± 108.8	< .001
ASA score				.532
1	99 (6.4%)	92 (6.4%)	7 (7.1%)
2	1199 (78.0%)	1128 (78.4%)	71 (72.4%)
3	230 (15.0%)	211 (14.7%)	19 (19.4%)
4	9 (.6%)	8 (.6%)	1 (1.0%)
Operation type				.039
Open	447 (29.1%)	409 (28.4%)	38 (38.8%)
Laparoscopy	1090 (70.9%)	1030 (71.6%)	60 (61.2%)
Extent of gastrectomy				.011
Subtotal	1215 (79.1%)	1148 (79.8%)	67 (68.4%)
Total	322 (20.9%)	291 (20.2%)	31 (31.6%)
Lymph node dissection				.348
D1+	756 (49.2%)	714 (49.6%)	42 (42.9%)
D2	776 (50.5%)	720 (50.0%)	56 (57.1%)
D2+	5 (.3%)	5 (.3%)	0 (.0%)
Combined resection				.131
Yes	212 (13.8%)	193 (13.4%)	19 (19.4%)
No	1325 (86.2%)	1246 (86.6%)	79 (80.6%)
T Stage				.109
T1	986 (64.2%)	931 (64.7%)	55 (56.1%)
T2 ∼ T4	551 (35.8%)	508 (35.3%)	43 (43.9%)
N stage				.308
N0	1117 (72.7%)	1051 (73.0%)	66 (67.3%)
N1	151 (9.8%)	142 (9.9%)	9 (9.2%)
N2	117 (7.6%)	109 (7.6%)	8 (8.2%)
N3	152 (9.9%)	137 (9.5%)	15 (15.3%)
Stage				.644
Stage I	1067 (69.4%)	1003 (69.7%)	64 (65.3%)
Stage II	215 (14.0%)	200 (13.9%)	15 (15.3%)
Stage III	255 (16.6%)	236 (16.4%)	19 (19.4%)
In-hospital mortality				< .001
Yes	8 (.5%)	2 (.1%)	6 (6.1%)
No	1529 (99.5%)	1437 (99.9%)	92 (93.9%)

Abbreviations: BMI, body mass index; ASA, American Society of Anesthesiologists.

Table 2.

Surgical Outcomes in Patients With Severe Local Complications.

Variable	N (=98/1537, 6.38%)
Anastomotic leakage
Yes	31 (2.02%)
No	67
Duodenal stump leakage
Yes	18 (1.17%)
No	80
Intra-abdominal abscess
Yes	30 (1.95%)
No	68
Pancreatic leakage
Yes	22 (1.43%)
No	76
Intra-abdominal bleeding
Yes	12 (.78%)
No	86
Intraluminal bleeding
Yes	8 (.52%)
No	90
Small bowel obstruction
Yes	5 (.32%)
No	93
Chyle leakage
Yes	3 (.19%)
No	95
Others
Yes	7 (.45%)
No	91
Reoperation
Yes	26 (1.69%)
No	72
In-hospital mortality
Yes	6 (.39%)
No	92

Clinical Factors Associated with Reoperation due to Local Complications

The patients with severe local complications were classified into the reoperation and conservative groups. Table 3 shows the results of the univariate and multivariate analyses of clinical factors associated with reoperation in patients with severe local complications. We found no significant impact of reoperation on patient demographics, operative factors, or clinicopathological features of gastric cancer (P > .05). However, we found that intra-abdominal bleeding (OR 7.56, 95% CI 2.14-31.04, P = .002) and small bowel obstruction (OR 12.91, 95% CI 1.80-259.72, P = .025) were significantly related to reoperation in the univariate analysis. In the multivariate analysis, intra-abdominal bleeding (OR 9.57, CI 2.65 – 40.20, P < .001) and small bowel obstruction (OR 19.14, 95% CI 2.60 – 390.13, P < .011) were independent risk factors for reoperation.

Table 3.

Univariate and Multivariate Analyses of Clinical Factors Associated With Reoperation for Local cCmplications.

Variable	No (N = 72)	Yes (N = 26)	Univariate analysis		Multivariate analysis
			P-value	Odds ratio	P-value	Odds ratio
			P-value	(95% CI)	P-value	(95% CI)
Age, y	65.5 ± 12.0	66.2 ± 11.7	.820
Sex (M:F)	61:11	23:03	.642
BMI (kg/m²)	23.2 ± 3.4	22.3 ± 2.5	.211
Hospital days, d	41.8 ± 29.4	51.3 ± 42.5	.220
Underlying disease			.647
Yes	35 (48.6%)	14 (53.8%)
No	37 (51.4%)	12 (46.2%)
History of abdominal surgery			.274
Yes	12 (16.7%)	2 (7.7%)
No	60 (83.3%)	24 (92.3%)
Operation time, min	308.5 ± 110.5	294.3 ± 105.3	.571
ASA score			.389
1	4 (5.6%)	2 (7.7%)
2	54 (76.1%)	17 (65.4%)
3	13 (18.3%)	6 (23.1%)
4	0 (.00%)	1 (3.8%)
Operation type			.969
Open	28 (38.9%)	10 (38.5%)
Laparoscopy	44 (61.1%)	16 (61.5%)
Extent of gastrectomy			.175
Distal	52 (72.2%)	15 (57.7%)
Total	20 (27.8%)	11 (42.3%)
Lymph node dissection			.327
D1+	28 (38.9%)	13 (50.0%)
D2	44 (61.1%)	13 (50.0%)
Combined resection			.580
Yes	13 (18.1%)	6 (23.1%)
No	59 (81.9%)	20 (76.9%)
Intraoperative transfusion			.525
Yes	15 (20.8%)	7 (26.9%)
No	57 (79.2%)	19 (73.1%)
Stage			.910
Stage I	46 (63.9%)	18 (69.2%)
Stage II	11 (15.3%)	4 (15.4%)
Stage III	15 (20.8%)	4 (15.4%)
Anastomotic leakage			.067
Yes	70 (53.4%)	22 (50.0%)
No	61 (46.6%)	22 (50.0%)
Duodenal stump leakage			.053
Yes	17 (23.6%)	1 (3.8%)
No	55 (76.4%)	25 (96.2%)
Intra-abdominal abscess			.057
Yes	26 (36.1%)	4 (15.4%)
No	46 (63.9%)	22 (84.6%)
Pancreatic leakage			.131
Yes	19 (26.4%)	3 (11.5%)
No	53 (73.6%)	23 (88.5%)
Intra-abdominal bleeding			.002	7.56	< .001	9.57
Yes	4 (5.6%)	8 (30.8%)		(2.14-31.04)		(2.65-40.20)
No	68 (94.4%)	18 (69.2%)
Intraluminal bleeding			.468
Yes	5 (6.9%)	3 (11.5%)
No	67 (93.1%)	23 (88.5%)
Small bowel obstruction			.025	12.91	.011	19.14
Yes	1 (1.4%)	4 (15.4%)		(1.80-259.72)		(2.60-390.13)
No	71 (98.6%)	22 (84.6%)
Gastric outlet obstruction			.466
Yes	1 (1.4%)	1 (3.8%)
No	71 (98.6%)	25 (96.2%)
Chyle leakage			.787
Yes	2 (2.8%)	1 (3.8%)
No	70 (97.2%)	25 (96.2%)
Others			.074
Yes	3 (4.2%)	4 (15.4%)
No	69 (95.8%)	22 (84.6%)

Abbreviations: BMI, body mass index; ASA, American Society of Anesthesiologists. The P-value wrote in Bold means P < .05.

Analysis of Risk Factors for Reoperation (Intra-abdominal Bleeding and Small Bowel Obstruction)

Intra-abdominal bleeding was found in 12 (.78%) patients. Eight of them underwent reoperation, while 4 did not. Supplement Table 1 shows a comparison of the clinical characteristics of the reoperation and conservative groups in patients with intra-abdominal bleeding. There was no significant difference in mortality between the reoperation and conservative groups (2 vs 1, P = 1.00). Angiographic embolization was successful in all 4 patients in the conservative group but was only successful in 1 patient in the reoperation group (P = .023). The median time interval from operation to diagnosis was 2.5 (1.0, 5.5) days. The bleeding foci in the reoperation group were the mesocolic vessel (n = 1), gastroduodenal artery (n = 1), left inferior phrenic artery (n = 1), portal vein (n = 1), right gastric artery (n = 1), and short gastric vessel (n = 1), and those in the conservative group were the mesocolic vessel (n = 2) and splenic artery (n = 2). There were two cases of bleeding from unknown sources in the reoperation group.

Small bowel obstruction was identified in 5 (.32%) patients. Four of them underwent reoperation. In terms of operation type, extent of gastrectomy, and reconstruction type, there was no statistically significant difference between the reoperation and conservative groups. The median time interval to diagnosis in patients with small bowel obstruction was 15.0 (7.0, 15.0) days. The median time interval from diagnosis to reoperation was 1.0 (.0, 3.5) days in the reoperation group. Adhesive small bowel obstruction, afferent loop obstruction, and Petersen’s defect herniation were causes of reoperation. There was no mortality due to small bowel obstruction. The demographics and clinicopathological factors of patients who experienced small bowel obstruction are summarized in Supplementary Table 2.

Discussion

Although the rate of reoperation has decreased through advances in surgical skills and equipment, some patients still undergo reoperation due to postoperative complications after radical gastrectomy.^15-17 Reoperation has adverse effects on patients, such as prolonged hospital stays, increased hospital costs, and mortality, and it is also very stressful for surgeons. In this study, we investigated the risk factors for reoperation following radical gastrectomy and found that intra-abdominal bleeding (OR 9.57, CI 2.65-40.20, P < .001) and small bowel obstruction (OR 19.14, 95% CI 2.60-390.13, P < .011) were independent risk factors for reoperation.

The incidence rate of reoperation due to local complications following radical gastrectomy is known to be 1.1-7.9%.^14,20-23 The reoperation rate was 1.69% in the present study, similar to that in the previously reported literature. The common causes of reoperation in some previous studies were intestinal obstruction, anastomotic leakage, and intra-abdominal bleeding.^15-17,23 The most common cause of reoperation in our study was also intra-abdominal bleeding, followed by anastomotic leakage and small bowel obstruction.

Intra-abdominal bleeding was both an independent risk factor and the most common cause associated with reoperation following gastrectomy in our study. It has been reported that the prevalence rate of intra-abdominal bleeding is .63∼2.9% and that the rate of reoperation due to intra-abdominal bleeding following gastrectomy is .15∼.83%.^3,5-7,15-17 Based on the total number of patients, the incidence of intra-abdominal bleeding was .78%, and the reoperation rate was .45% in this study. Among the 12 patients with intra-abdominal bleeding in our study, 3 patients (25%) died. Two of them underwent reoperation, and one did not. In terms of mortality due to intra-abdominal bleeding, reoperation did not lead to a decrease in mortality. Similar results were reported in previous studies. Intra-abdominal bleeding is the most common local complication that leads to patient death, up to 25%.^15,24 Like this, intra-abdominal bleeding requiring surgical treatment is fatal to the patient’s life.

We also analyzed the bleeding focus in this study, and we found that the most common bleeding focus was the mesocolic vessels, followed by splenic vessels. There was no significant difference in the bleeding site compared to that in previous studies on bleeding focus, although there were differences in frequency.¹⁷ Therefore, surgeons should be able to sufficiently prevent bleeding through careful and delicate manipulation when performing dissection around these dangerous vessels.

Regarding the management of intra-abdominal bleeding, angiographic embolization was successfully performed in all 4 cases without reoperation, which was statistically significant in this study. A previous study reported that angiographic embolization can successfully manage postoperative bleeding.^24,25 Therefore, it is recommended to consider trying angiographic embolization first when treating patients with postoperative bleeding.

Another risk factor for reoperation is small bowel obstruction, with a total of 4 cases of reoperation in this study. One case without reoperation involved jejunojejunostomy stricture, which was resolved by endoscopic balloon dilatation. Previous studies have also referred to small bowel obstruction as one of the major causes of reoperation ^15-17 However, the difference from this study is that they included small bowel obstruction 30 days postoperatively.

There was no mortality after reoperation due to small bowel obstruction. The median time interval from diagnosis to reoperation was 1.0 (.0, 3.5) days in this study. All patients with small bowel obstruction had symptoms such as abdominal discomfort, nausea, and vomiting and were diagnosed with computed tomography (CT) scans. We performed reoperation immediately after diagnosis in 75% of patients with small bowel obstruction, and we think this is an important point in the lack of mortality. Previous studies also highlighted immediate CT examinations and early intervention if a small bowel obstruction, such as an afferent loop obstruction or an internal hernia, was suspected.^11,26 From this point of view, we recommend considering early reoperation without waiting if small bowel obstruction could be diagnosed on CT scans.

Body mass index was not a risk factor for reoperation in the current study. However, Li P et al reported that BMI > 25 kg/m² is an independent risk factor for reoperation after gastrectomy.²³ Since the mean BMI was 23.2 ± 4.8 kg/m² in this study, it is difficult to evaluate the relationship between obesity and reoperation with a high BMI. A recent Western study reported that high BMI did not increase complications after gastrectomy.²⁷ However, in general, it is known that patients with high BMI have longer operation times and increased blood loss.²³ If a patient with a high BMI deviate from the normal recovery process after gastrectomy, it is recommended to perform an abdominal evaluation using CT scans to exclude intra-abdominal bleeding and small bowel obstruction.

This study has some limitations. First, this study is a retrospective study. Second, the causes of reoperation following gastrectomy vary, and the number of reoperation cases is small. Additionally, the characteristics of patients who underwent reoperation were heterogeneous. Therefore, it was difficult to generalize when complications occurred and when reoperation should be performed. Despite these limitations, this study provides meaningful information about reoperation following gastrectomy through multivariate analysis.

Conclusion

We found that intra-abdominal bleeding and small bowel obstruction are independent risk factors for reoperation following radical gastrectomy. Patients with intra-abdominal bleeding and small bowel obstruction need to be warned of reoperation. Furthermore, surgeons need to be aware that intra-abdominal bleeding is detrimental to the prognosis of patients undergoing gastrectomy and that they must make quick decisions in the treatment of patients with small bowel obstruction following gastrectomy.

Supplemental Material

sj-pdf-1-asu-10.1177_00031348211050842 – Supplemental Material for Risk Factors for Reoperation Following Radical Gastrectomy in Gastric Cancer Patients

Supplemental Material, sj-pdf-1-asu-10.1177_00031348211050842 for Risk Factors for Reoperation Following Radical Gastrectomy in Gastric Cancer Patients by Dong-Hwan Kim, Ji-Ho Park, Tae Han Kim, Eun-Jung Jung, Chi-Young Jeong, Young-Tae Ju, Ju-Yeon Kim, Tae-Jin Park, Young-Joon Lee and Sang-Ho Jeong in The American Surgeon

Footnotes

Declaration of Conflicting Interests

The author(s) declared no potential conflicts of interest with respect to the research, authorship, and/or publication of this article.

Funding

The author(s) received no financial support for the research, authorship, and/or publication of this article.

Ethics Approval

All procedures followed were in accordance with the ethical standards of the responsible committee on human experimentation (institutional and national) and with the Helsinki Declaration of 1964 and later versions.

Supplemental Material

Supplemental material for this article is available online.

Consent to Participate

Patients were not required to give informed consent to the study because the analysis used anonymous clinical data, and this was approved by the Institutional Review Board (GNUH 2020–12–010)

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Supplementary Material

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