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Research ArticleClinical Studies

Increased Transumbilical Incision Complication Rates With Laparoscopic Colorectal Resection: A Single-center Propensity Score-matched Cohort Study

KODAI TOMIOKA, TAKESHI AOKI, MAKOTO WATANABE, YUTA ENAMI, AKIRA FUJIMORI, TOMOTAKE KOIZUMI, SATORU GOTO, KIMIYASU YAMAZAKI, KOJI OTSUKA and MASAHIKO MURAKAMI
Anticancer Research February 2022, 42 (2) 1115-1121; DOI: https://doi.org/10.21873/anticanres.15574
KODAI TOMIOKA
Division of Gastroenterological and General Surgery, Department of Surgery, School of Medicine, Showa University, Shinagawa, Japan
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TAKESHI AOKI
Division of Gastroenterological and General Surgery, Department of Surgery, School of Medicine, Showa University, Shinagawa, Japan
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  • For correspondence: takejp{at}med.showa-u.ac.jp
MAKOTO WATANABE
Division of Gastroenterological and General Surgery, Department of Surgery, School of Medicine, Showa University, Shinagawa, Japan
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YUTA ENAMI
Division of Gastroenterological and General Surgery, Department of Surgery, School of Medicine, Showa University, Shinagawa, Japan
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AKIRA FUJIMORI
Division of Gastroenterological and General Surgery, Department of Surgery, School of Medicine, Showa University, Shinagawa, Japan
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TOMOTAKE KOIZUMI
Division of Gastroenterological and General Surgery, Department of Surgery, School of Medicine, Showa University, Shinagawa, Japan
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SATORU GOTO
Division of Gastroenterological and General Surgery, Department of Surgery, School of Medicine, Showa University, Shinagawa, Japan
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KIMIYASU YAMAZAKI
Division of Gastroenterological and General Surgery, Department of Surgery, School of Medicine, Showa University, Shinagawa, Japan
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KOJI OTSUKA
Division of Gastroenterological and General Surgery, Department of Surgery, School of Medicine, Showa University, Shinagawa, Japan
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MASAHIKO MURAKAMI
Division of Gastroenterological and General Surgery, Department of Surgery, School of Medicine, Showa University, Shinagawa, Japan
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Abstract

Aim: To evaluate the complication rates and risk factors associated with transumbilical incision (TUI) and comprehensively examine differences according to the procedures using propensity score matching. Patients and Methods: The study involved 737 patients who underwent laparoscopic procedures between 2009 and 2017 (Japanese University-Hospital-Medical-Information-Network Clinical Trials Resistry No. 000040653). The occurrences of superficial surgical site infection (SSI) and TUI hernia were analyzed. Results: SSI occurred in 17 patients (2.31%) and hernia occurred in 29 (3.93%). Multivariate analysis revealed that female sex and diabetes mellitus were correlated with incisional hernia. Propensity score-matching analysis was performed to compare those who underwent colorectal resection with those who underwent other resections; the results showed that the former had a significantly higher rate of TUI hernia (p<0.001), as well as a significantly higher incidence of SSI (p=0.004). Conclusion: A significant higher incidence of SSI and TUI hernia in laparoscopic colorectal resection was found. The construction of the TUI was feasible with rationality.

Key Words:
  • Transumbilical incision
  • laparoscopic
  • surgical site infection
  • colorectal
  • hernia

Transumbilical incision, which has been utilized as the first port for access and organ removal during all laparoscopic procedures since the 1990s, has recently become a common standard technique for laparoscopic surgery. The primary advantage of this incision is that it forgoes the need for a new incision solely for organ removal, such as for the Pfannenstiel incision. At the beginning of surgery, a 12-mm port is created via a transumbilical incision, which can be craniocaudally adjusted for the size of the organs to be resected. Thereafter, the organ is removed through the transumbilical incision after wound protector attachment. Our group had already evaluated the usefulness of a transumbilical incision in laparoscopic surgery. Accordingly, the primary study in 2017 and 2018 revealed that colorectal resection involved significantly higher surgical site infection rates at the transumbilical incision and incisional hernia compared to gastric resection (1). Moreover, our analysis identified female sex and diabetes mellitus (DM), but not surgical site infection (SSI), as independent risk factors for hernia formation (1, 2). Our secondary study in 2020 and 2021, which examined cases which underwent laparoscopic surgery for parenchymal organs, identified a high body mass index (BMI) as a risk factor of hernia formation in laparoscopic hepatectomy, with none of the patients having developed transumbilical SSIs (3, 4). A number of studies have shown transumbilical SSI occurrence rates of 3.85%, 0.79%, 0%, and 0% and incisional hernia occurrence rates of 5.64%, 0.40%, 7.14%, and 5.77% following colorectal resection, gastric resection, hepatectomy, and pancreatectomy, respectively (1-4). The aforementioned results suggested that gastrointestinal surgeries led to higher SSI rates, perhaps due to the involvement of intestinal bacteria. Moreover, a simple comparison of incisional hernia incidences seemed meaningless given the differences in the number of cases. Furthermore, no detailed studies on transumbilical incision for organ removal or studies comparing incisions among multi-organ surgeries were available. The current single-center cohort study therefore aimed to evaluate complications and risk factors associated with transumbilical incision requiring wound extension for the removal of a resected specimen and to comprehensively examine differences according to the resected organs using propensity score matching (PSM).

Patients and Methods

Participants. Our study cohort comprised 737 consecutive patients who underwent laparoscopic procedures for malignant diseases requiring wound extension for organ removal at our Institution between November 2009 and December 2017. Exclusion criteria were patients who (i) received follow-up at another hospital, (ii) needed conversion to laparotomy, or (iii) were undergoing multiple procedures. Our study protocol was approved by the Ethics Committee of Showa University (approval number: 3465) and the study was registered with the Japanese University-Hospital-Medical-Information-Network Clinical Trials Resistry No. 000040653.

Data, including demographic characteristics, surgical details, tumor characteristics, postoperative outcomes, and transumbilical complication (SSIs and incisional hernias), were collected from our hospital database.

Definitions. SSIs were defined based on the criteria of the American College of Surgeons National Surgical Quality Improvement Program (5), whereas incisional hernias were defined based on the definition established by Tonouchi et al. (6). SSI development was identified by the Infection Control Team of our Department, who continuously and routinely assessed traunsumbilical incisions even during outpatient visits. Transumbilical incisional hernias were assessed via clinical examination and computed tomography during routine follow-up every 3 months within the first 2 years after surgery and 3-6 months thereafter.

Transumbilical incision. The navel was incised in the craniocaudal direction from its center, after which the first 12-mm port was inserted. The transumbilical incision was then minimally extended craniocaudally and adjusted according to the size of the organ to be resected (approximately 2-5 cm). The resected specimens were placed in a plastic bag in the abdominal cavity and were removed via the transumbilical incision after attaching a wound protector (Figure 1). Anastomosis was performed outside the body and above the incision as needed in some cases, especially in colorectal procedures. Standard wound closure and dressing methods were utilized. The anterior and posterior laminae of the rectal sheath in the incision were reliably nodule-sutured with an absorbable suture regardless of subcutaneous fat thickness. Buried interrupted dermal sutures were constructed using a 4-0 monofilament absorbable suture material after incisions were washed with 200 ml saline. The incision was sealed with 48 g of a hydrocolloid dressing after the procedures.

Figure 1.
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Figure 1.

Transumbilical incision. A: The incision was cut and extended to facilitate organ removal. B: The resected specimen of the stomach was removed. C: The resected specimen of the colon was removed. D: The incision after closure. E: The incision was covered with a hydrocolloid dressing.

Data were presented as the mean±standard deviation (SD), unless otherwise stated. Risk factors were investigated via univariate analyses through the chi-squaredbtest, Fisher’s exact test, Wilcoxon rank-sum test, Wilcoxon signed-rank test, and logistic regression. Significant variables were then analyzed via multivariate logistic regression analysis. PSM was used to balance the characteristics among procedures (colorectum or other) to reduce the bias for the occurrences of transumbilical incisional complications. Propensity scores to determine matched pairs between the groups were created using five patient background variables (sex, height, weight, BMI, history of DM) that may potentially influence the occurrence of transumbilical incisional complications. After calculating the propensity scores using a logistic regression model, patients were matched in a 1:1 ratio using a caliper width of 0.2 of the standard deviation from the propensity score logit. All analyses were performed using JMP Pro software version 14 (SAS Institute Inc., Cary, NC, the USA). Statistical assessments were two-sided, with a two-sided p-value of less than 0.05 indicating statistically significant differences.

Results

Among the 737 patients included herein, 434 (58.9%) and 303 were male and female (41.1%), respectively, with a mean age of 68.70±12.37 years (median=71.0 years, range=19-91 years). As shown in Table I, the targeted procedures for malignant diseases included gastric (n=253, 34.3%), colorectal (n=390, 52.9%), liver (n=42, 5.7%), and pancreatic (n=52, 7.1%) resections.

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Table I.

Surgical procedures and incidence of surgical site infections (SSI) and incisional hernias.

Short-term complications. SSI was observed in 17 cases (2.31%), among whom 15 and two cases underwent colorectal and gastric resection, respectively. Univariate analysis comparing cases with and without SSI showed that patients undergoing colorectal resection more frequently developed SSIs compared to those undergoing other procedures [3.85% vs. 0.58%; odds ratio (OR)=6.900, 95% confidence interval (CI)=1.567-30.391; p=0.002] (Table II).

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Table II.

Demographic data of patients with and without surgical site infection (SSI).

Long-term complications. Transumbilical incisional hernia was observed in 29 cases (3.93%), among whom 22, 1, 3 and 3 cases underwent colorectal resection, gastric resection, hepatectomy, and pancreatectomy, respectively. The median time until hernia development was 12 months (range=2-24 months). A comparison of the groups with and without transumbilical incisional hernias indicated significant differences according to sex (p=0.022), weight (p=0.004), BMI (p<0.001), DM (p<0.001), and procedure (colorectum or other) (p=0.013). Multivariate analysis of the three significant variables identified female sex (OR=4.861, 95% CI=1.345-18.984; p=0.019), DM (OR=5.230, 95% CI=2.077-12.809; p<0.001), and colorectal resection (OR=3.209, 95% CI=1.350-8.577; p=0.012) as variables significantly associated with increased risk of hernia (Table III). Based on these results, PSM was herein performed on the assumption that colorectal surgery caused more transumbilical incisional complications compared to other procedures. After PSM, however, no significant differences between the two groups were observed except for blood loss (Table IV). After comparing those who underwent colorectal resection with those who underwent other resections, our results indicated that the former led to significantly higher transumbilical incisional complication rates (OR=5.304, 95% CI=1.982-14.192; p<0.001), as well as significantly higher occurrences of both SSIs (OR=8.310, 95% CI=1.911-6.287; p=0.004) and incisional hernias (OR=3.158, 95% CI=1.126-8.858; p=0.037) (Table V).

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Table III.

Demographic data of patients with and without transumbilical incisional hernias.

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Table IV.

Demographic data of patients before and after propensity score matching.

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Table V.

Analysis of transumbilical incision complications after propensity score matching.

Discussion

Transumbilical incisions have been commonly utilized in modern laparoscopic surgery given their convenience and practicality. Before and during the early days of laparoscopic surgery, transumbilical incisions were generally avoided given that such an area was considered unsanitary and that the navel was connected to the ligamentum teres (7). Nonetheless, Jesus reported in 1963 that transumbilical incisions were a safe surgical technique in laparotomy (8), while Peas et al. reported in 1987 that the were no significant differences in the rates of transumbilical incision infections and hernias after comparing transumbilical incisions with techniques that avoided the navel using an arc shape (9). Considering such backgrounds, we have been utilizing transumbilical incisions for organ removal since the early period following the introduction of laparoscopic surgery. The main advantages of transumbilical incisions are that it (i) provides better cosmetic outcomes and ease of extension in the craniocaudal direction, (ii) forgoes the need for establishing another incision just for organ removal, such as the Pfannenstiel incision, and (iii) allows the abdominal cavity to be safely and directly reached via the shortest anatomical distance. Moreover, the size of the incision can be minimized by adjusting it to the size of organs resected using the extensibility of the skin.

Only a few investigations have focused on the transumbilical incision itself and its complications. Our group had previously highlighted the usefulness of a transumbilical incision and its complication in laparoscopic colectomy, gastrectomy, hepatectomy, and pancreatectomy. Our previous reports described the efficacy of transumbilical incision in laparoscopic gastrointestinal procedures, consequently finding that incidence rates of SSIs and incisional hernias correlated with transumbilical incisions were significantly higher following colorectal than gastric resection (1-4).

Although the incidence of transumbilical SSIs was only 2.31% following all procedures, the current study was able to identify obvious risk factors for SSIs. A number of detailed studies on laparoscopic colectomy have reported a 3-8% incidence of umbilical port site infections (10, 11), with a meta-analysis revealing an SSI incidence rate of 2.42% following laparoscopic gastrectomy (12). Moreover, another study showed that high BMI and DM were among the several risk factors for transumbilical SSIs (13).

The incidence of transumbilical incision hernias in the current study was 3.93% following all procedures, with female sex and DM having been identified as independent risk factors for hernia formation. Evidence has shown that high BMI to be significantly associated with a greater risk for incisional hernia following laparoscopic hepatectomy. On the other hand, our research found no apparent risk factors for hernia formation following laparoscopic pancreatectomy (3, 4). A systematic review by Owens et al. found an umbilical incisional hernia incidence rate of 1.47% following laparoscopic colorectal resection (14), while Laurent et al. reported a rate of 7.74% following laparoscopic rectal resection, which was lower than that following laparotomy for rectal cancer (15). On the other hand, a study by Oscar et al. in Spain revealed that 16.18% of those who underwent colorectal resection developed umbilical and supraumbilical incisional hernias. Furthermore, the Pfannenstiel incision had been introduced at their institution for removal of resected organs during left colectomy (16). Other research by Comanjucosas et al., who prospectively evaluated patients undergoing cholecystectomy in Spain, found an umbilical incisional hernia incidence rate of 25.9% (17), while Jang et al. reported that 5.3% of patients who underwent laparoscopic gastrectomy in Korea developed umbilical incisional hernia (18). The aforementioned results therefore suggest considerable differences in incidence rates according to the country or institution, ethnicity, and procedure. With regard to risk factors for transumbilical incisional hernia, Comanjuncosas et al. described that incision enlargement, SSI, DM, and obesity were associated with hernia formation (17), whereas Nassar et al. found that sarcolemmal deficit was a risk factor for hernia formation following laparoscopic cholecystectomy (19). Another study by Swank et al. revealed that the use of pyramidal trocars, 12-mm trocars, surgical duration, age, and BMI were risk factors for hernia formation (20).

Considering all of the aforementioned studies, the incidences of transumbilical incision complications were comparable to that presented herein. Moreover, it remains clear why numerous risk factors have been identified. However, given the absence of comparative studies between surgical procedures, the current study can be considered somewhat novel. In the present study, laparoscopic colorectal, gastric, liver, and pancreatic resections were all performed in one facility, whereas the establishment of the transumbilical incision, extension of incision, organ removal, wound closure, sealing methods, and tools were all standardized and unified, thereby minimizing selection bias.

Our preliminary research in 2017 regarding transumbilical incisions revealed that colectomy led to more complications than gastrectomy (1). Given that resected organs were removed via the transumbilical incision and that mesenteric resection and anastomosis were performed as needed, the effects of bacterial fall while working above the transumbilical incision on complications had been considered. Another 2018 study concluded that falling bacteria had negligible effects, suggesting that colectomy itself might be a risk factor for transumbilical incision complications (2). Similar evaluations regarding transumbilical incision had been conducted for laparoscopic hepatectomy and pancreatectomy, with subsequent results showing an SSI incidence of 0% in both procedures and an incisional hernia incidence of 7.14% and 5.77%, respectively (3, 4). Differences between intestinal organs, such as the colorectum and stomach, which have been correlated with intestinal bacteria, and parenchymal organs, such as the liver and pancreas, had also been considered. Accordingly, previous studies have hypothesized that more transumbilical incision complications occur following intestinal resection or laparoscopic colectomy than following parenchymal organ resection or other procedures. As such, the current study was conducted to clarify differences in the incidence of transumbilical incision complications between surgical procedures. From these perspectives, propensity score analysis was conducted to adjust for confounding factors between surgical procedures. Firstly, a comparison of cases with or without hernia showed no significant difference in complications between surgical procedures for the intestinal tract and those for parenchymal organ resection. However, a significant difference had been noted between colectomy and the other procedures. Therefore, considering the possibility that colectomy itself might be a risk factor, PSM analysis was performed to eliminate background confounding factors between surgical procedures as much as possible. As hypothesized, those who underwent laparoscopic colorectal resection more frequently exhibited transumbilical incision complications compared to those who underwent other organ resection. Several possible factors might have caused this result. The most important factor to be considered was whether the resection or anastomosis had been performed outside the body, particularly above the transumbilical incision, for some colectomies. Moreover, concerns were present regarding the effects of Escherichia coli contamination due to improper handling of the intestinal tract, as well as the effects of a larger incisional length, given the need to place the entire mesentery outside the body. While it remains unclear to what extent bacterial fall affects wound infection, reports have shown that SSI does not contribute to hernia formation (1). Although the lengths of transumbilical incision were unclear due to the retrospective nature of the study, parenchymal organ resection, especially hepatectomy, often involves the removal of a large specimen via the transumbilical incision. Moreover, the need for a larger incision length with colectomy, relative to other procedures, cannot be clearly justified, with no such impression having been noted in actual clinical practice. Furthermore, it is obvious that the incisional length does not depend on the tumor diameter, thereby making its effect negligible. However, further prospective studies are certainly needed. SSIs were observed in parenchymal organ resection, suggesting that intestinal bacteria may have some effect. Although transumbilical incision hernias are expected to occur with any surgical procedure, more attention should be paid especially after colectomy.

Our multivariate analysis identified female sex and DM were as independent risk factors for transumbilical incision hernia formation. Furthermore, although BMI was not identified as a significant risk factor for complications during multivariate analysis, patients with a high BMI should remain vigilant regarding the development of transumbilical incision hernias after surgery. Considering that women have a relatively higher amount of subcutaneous fat than males and that DM causes obesity, including high BMI factors, achieving full-thickness suturing of the rectal sheath nodule might be difficult in such patients, with such technical factors perhaps sufficiently contributing to the occurrence of transumbilical incision hernias. Moreover, obese patients may be at risk for transumbilical incision hernias due to higher intra-abdominal pressure. Based on the aforementioned findings, rectal sheath nodule suturing in patients with factors related to obesity should be undertaken with even greater care and caution.

The findings presented herein should be interpreted in light of our study limitations. This retrospective study included patients from a single institution, potentially introducing selection bias. Furthermore, the possibility of a type 2 statistical error cannot be ruled out. Prospective randomized studies are therefore need in the near future. Nevertheless, given that only a few studies have focused on transumbilical incisional complications, we are confident that the findings presented herein would have a positive impact on future laparoscopic surgery. Based on available evidence thus far, it can be concluded that our transumbilical incision with wound closure and covering methods is feasible, with good tolerability and rationality for modern laparoscopic abdominal surgery.

Footnotes

  • Conflicts of Interest

    All Authors declare that they have no conflicts of interest or financial ties to disclose.

  • Authors’ Contributions

    KT, TA, and MM contributed to the design and implementation of the research. KT, TA, YE, AF, TK, SG, KY, MW, KO, and MM contributed to the analysis of the results and writing of the article. All Authors have read and approved the article.

  • Received December 2, 2021.
  • Revision received December 16, 2021.
  • Accepted December 19, 2021.
  • Copyright © 2022 International Institute of Anticancer Research (Dr. George J. Delinasios), All rights reserved.

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Anticancer Research
Vol. 42, Issue 2
February 2022
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Increased Transumbilical Incision Complication Rates With Laparoscopic Colorectal Resection: A Single-center Propensity Score-matched Cohort Study
KODAI TOMIOKA, TAKESHI AOKI, MAKOTO WATANABE, YUTA ENAMI, AKIRA FUJIMORI, TOMOTAKE KOIZUMI, SATORU GOTO, KIMIYASU YAMAZAKI, KOJI OTSUKA, MASAHIKO MURAKAMI
Anticancer Research Feb 2022, 42 (2) 1115-1121; DOI: 10.21873/anticanres.15574

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Increased Transumbilical Incision Complication Rates With Laparoscopic Colorectal Resection: A Single-center Propensity Score-matched Cohort Study
KODAI TOMIOKA, TAKESHI AOKI, MAKOTO WATANABE, YUTA ENAMI, AKIRA FUJIMORI, TOMOTAKE KOIZUMI, SATORU GOTO, KIMIYASU YAMAZAKI, KOJI OTSUKA, MASAHIKO MURAKAMI
Anticancer Research Feb 2022, 42 (2) 1115-1121; DOI: 10.21873/anticanres.15574
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  • The Efficacy of Chemical Bowel Preparation Against Incisional Surgical Site Infection in Colorectal Cancer Surgery: A Propensity Score Matching Study
  • Laparoscopic Colorectal Cancer Surgery for Patients With Severe Chronic Heart Failure
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Keywords

  • transumbilical incision
  • laparoscopic
  • surgical site infection
  • colorectal
  • Hernia
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