Abstract
Objectives:
Parastomal hernia (PSH) is a common complication of colostomy; however, its risk factors remain poorly investigated. In this study, we examined the associations between sarcopenia, visceral and subcutaneous fat, and PSH in patients who underwent transperitoneal colostomy for colorectal cancer.
Methods:
This retrospective, single-center, cohort study included 60 patients who underwent laparoscopic or robot-assisted abdominoperineal resection or Hartmann's procedure for colorectal cancer between November 2010 and February 2022. Stoma creation was uniformly performed using the transperitoneal approach, and PSH was diagnosed via abdominal computed tomography (CT) at 1 year postoperatively. Visceral fat areas (VFAs) and subcutaneous fat areas (SFAs) were measured through preoperative CT images using an image analysis system. Risk factors for PSH were retrospectively analyzed.
Results:
PSH was diagnosed in 13 (21.7%) patients. In the univariate analysis, PSH was significantly associated with body mass index >22.3 kg/m2 (p=0.002), operation time >319 min (p=0.027), estimated blood loss >230 mL (p=0.008), postoperative complications (p=0.028), stoma diameter >18.6 mm (p=0.015), VFA >89.2 cm2 (p=0.005), and SFA >173.2 cm2 (p=0.001). Multivariate analyses confirmed that SFA >173.2 cm2 (odds ratio: 16.7, 95% confidence interval 1.29-217.2, p=0.031) was an independent risk factor for PSH.
Conclusions:
Subcutaneous fat area is significantly associated with the development of PSH after transperitoneal colostomy. Applying these insights could help to prevent PSH.
Keywords: parastomal hernia, subcutaneous fat area, permanent colostomy, colorectal cancer
Introduction
Minimally invasive surgical techniques for colorectal cancer are commonly applied, and these approaches have allowed the preservation of anal function in many patients. However, even with these advanced surgical procedures, some patients are forced to undergo permanent colostomy for this malignancy.
Parastomal hernia (PSH) is a common complication of abdominoperineal resection (APR) or the Hartmann procedure for rectal cancer[1]. Carne et al. reported that the incidence of PSH in cases of permanent colostomies is approximately 13%[2]. Once a PSH develops, curative repair is often difficult[3]. Further, PSH impairs patients' physical appearance and social activity, profoundly affecting their quality of life (QOL). Given that a permanent stoma adversely affects patient QOL, it is important for surgeons to manage complications associated with permanent colostomy, as well as treat the primary disease. Previous reports have suggested that physical components, such as skeletal muscle, visceral fat, and subcutaneous fat are significantly associated with both short- and long-term outcomes in colorectal cancer surgery[4]. However, the association between physical components and PSH development remains unclear, and only few reports have addressed this association.
The extraperitoneal colostomy method, which was first reported in 1958 by Goligher, is associated with a lower risk of PSH development than that of the transperitoneal method[5,6]. However, traditionally, colostomy creation is performed via the transperitoneal approach, particularly during laparoscopic colorectal surgery, because the extraperitoneal route requires complicated procedures, such as adequate mobilization of the colon and tunneling of the intestine between the peritoneal and abdominal wall muscles[7]. Therefore, identifying the risk factors for PSH in cases of transperitoneal stoma creation in essential, even for prevention. Therefore, in the present study, we aimed to assess the risk factors for PSH following a transperitoneal colostomy procedure for colorectal cancer. In addition, we provided a detailed analysis of physical status, particularly of sarcopenia, visceral fat area (VFA), and subcutaneous fat area (SFA).
Methods
Patients and methods
This retrospective study included 60 patients diagnosed with colorectal cancer who underwent transperitoneal colostomy for colorectal cancer at the International University of Health and Welfare Hospital between November 2010 and February 2022.
The operative methods were either laparoscopic or robot-assisted APR or the Hartmann's procedure. This study was conducted in accordance with the Declaration of Helsinki, and was approved by the institutional review board of the International University of Health and Welfare Hospital (approval no: 21-B-22). All data were subjected to strict privacy policies. Patients and their family members had the right to withdraw from the study at any time. The requirement for informed consent was waived due to the retrospective design of the study.
Patient management and stoma creation method
Basic surveillance after surgery included tumor marker monitoring, computed tomography (CT), and colonoscopy. Tumor markers were examined routinely every 3 months, whereas chest and abdominal enhanced CTs were performed every 6 months and colonoscopies were conducted every 1 or 2 years[8].
In cases of permanent colostomy, the transperitoneal method was used[9]. In all cases, a permanent colostomy was created in the left lower quadrant of the abdomen, passing through the left abdominal rectus muscle, utilizing the sigmoid or descending colon, and guided by a preoperatively marked skin site.
Data collection
Fifteen variables were evaluated as potential risk factors for parastomal hernia, including sex, age, body mass index (BMI), smoking status, pathological stage (according to the 3rd English Edition of the Japanese Classification of Colorectal, Appendiceal, and Anal Carcinoma)[10], administration of adjuvant chemotherapy, operation time, estimated blood loss, development of postoperative complications, concomitant diabetes mellitus, presence of sarcopenia/recurrence, stoma diameter, VFA, and SFA. The cut-off values of continuous variables (age, BMI, operative time, blood loss, stoma diameter, VFA, and SFA) were determined based on receiver operating characteristics (ROC) curves. ROC curves were drawn using the development states of parastomal hernia, and cut-off values were determined by Youden's Index (the maximum points of “sensitivity + specificity －1”). Postoperative complications were evaluated according to the Clavien-Dindo classification within 30 days after surgery.
Definition of parastomal hernia
The stoma diameter was measured using the first postoperative abdominal CT scan, and defined as the width of the divided abdominal rectus muscle into which the colostomy penetrated (Figure 1A). Parastomal hernia was diagnosed based on abdominal CT conducted 1 year after the primary surgery, regardless of whether the patient was symptomatic or asymptomatic (Figure 1B)[11].
Figure 1.
Measurement of stoma diameter and detection of parastomal hernia.
(A) Stoma diameter was measured using computed tomography (CT) images and represented by the length of the white dotted line.
(B) Presence of parastomal hernia (PSH) is verified through abdominal CT image. A case of a patient who developed PSH is highlighted in yellow circles.
Measurement of the SFA, VFA, and psoas muscle area
The VFA and SFA were preoperatively measured at the level of the umbilicus through abdominal CT image using an image analysis system (Ziosoft1 Inc., Tokyo, Japan) (Figure 2A, 2B). Sarcopenia was defined as falling below the sex-specific median size of the psoas muscle mass area at the third lumbar vertebra, which was calculated as the length of the major axes × the length of the minor axes × π[12].
Figure 2.
Analysis of visceral fat areas and subcutaneous fat areas.
Computed tomography imaging analysis at the level of the umbilicus, in the axial plane; areas marked in red indicate visceral fat areas (VFAs), whereas areas marked in blue indicate subcutaneous fat areas (SFAs).
(A) A patient with a large SFA.
(B) A patient with a small SFA.
Statistical analyses
All statistical analyses were conducted using STATA Statistical Software (StataCorp, College Station, TX, USA), and p-values <0.05 were considered statistically significant. Continuous variables were compared using the Mann-Whitney U test, and categorical variables were compared using the chi-square test. Multivariable logistic regression analysis to identify independent risk factors was performed on all variables with p-values <0.05 on univariate analysis. The results of the multivariate analysis are shown as p-values, odds ratio (OR) and corresponding 95% confidence interval (CI).
Results
The demographic and clinicopathological characteristics of the patients are summarized in Table 1. The cohort comprised 44 (73.3%) men and 16 (26.7%) women, with a median age of 73.5 years. The median BMI was 22.2 kg/m2, and 23 (38.3%) patients were diagnosed with sarcopenia. The median operative time was 346.7 min, and the median intraoperative blood loss was 150.3 mL. Robot-assisted surgery was performed in 11 (18.3%) patients. The pathological findings revealed moderately differentiated tubular adenocarcinoma in 33 (55.0%), well-differentiated tubular adenocarcinoma in 23 (38.3%), and other findings in 4 (6.7%) patients. Pathological stage I was observed in 13 (21.7%), stage II in 18 (30.0%), stage III in 25 (41.7%), stage IV in 3 (5.0%), and stage 0 in 1 (1.7%) patient. Adjuvant chemotherapy was administered to 27 (45.0%) patients, and 30 (50.0%) patients experienced postoperative complications, including surgical site infections (SSIs) in 17 (28.3%), ileus in 15 (25.0%), and intra-abdominal abscesses in 2 (3.3%) cases. During the follow-up period, 20 (33.3%) patients experienced recurrence and 17 (28.3%) died.
Table 1.
Demographic and Clinicopathological Characteristics of the Patient Cohort.
| Variables | Total | |
|---|---|---|
| Patients, number | 60 | |
| Age, years | 73.5 (66.8-79.0) | |
| Sex | Men | 44 (73.3%) |
| Women | 16 (26.7%) | |
| Body mass index, kg/m2 | 22.2 (19.9-24.1) | |
| Smoking status | 35 (58.3%) | |
| Histopathology, n (%) | ||
| Tub1 | 23 (38.3%) | |
| Tub2 | 33 (55.0%) | |
| Others | 4 (6.7%) | |
| Pathological stage, n (%) | ||
| 0 | 1 (1.7%) | |
| I | 13 (21.7%) | |
| II | 18 (30.0%) | |
| III | 25 (41.7%) | |
| IV | 3 (5.0%) | |
| Adjuvant chemotherapy | 27 (45.0%) | |
| Operation time, min | 343.5 (305-391) | |
| Intra-operative blood loss, mL | 80 (30-200) | |
| All complications | 30 (50.0%) | |
| Surgical site infection | 17 (28.3%) | |
| Ileus | 15 (25.0%) | |
| Abscess | 2 (3.3%) | |
| Diabetes mellitus | 12 (20.0%) | |
| Sarcopenia | 23 (38.3%) | |
| Robot-assisted surgery | 11 (18.3%) | |
| Recurrence | 20 (33.3%) | |
| Death | 17 (28.3%) | |
| Visceral fat area, cm2 | 104.3 (60-150) | |
| Subcutaneous fat area, cm2 | 106.6 (57-167) | |
Data are expressed as means with standard deviation or medians with interquartile range and number (%).
Abbreviations: Tub1, well-differentiated tubular adenocarcinoma; Tub2, moderately differentiated tubular adenocarcinoma
The results of the univariate analyses are presented in Table 2. PSH was diagnosed in 13 (21.7%) patients. Univariate analysis revealed that PSH was significantly associated with a BMI >22.3 kg/m2 (p=0.002), operation time >319 min (p=0.027), estimated blood loss >230 mL (p=0.008), postoperative complications (p=0.028), stoma >18.6 mm (p=0.015), VFA >89.2 cm2 (p=0.005), and SFA >173.2 cm2 (p=0.001). Multivariate analyses revealed that SFA >173.2 cm2 (odds ratio: 16.7, 95% confidence interval 1.29-217.2, p=0.031) was an independent risk factor for PSH (Table 3).
Table 2.
Pre- and Peri-Operative Risk Factors for Parastomal Hernia.
| Variables | PSH | Non-PSH | Univariate analysis | |
|---|---|---|---|---|
| n (%) or median (range) | p-value | |||
| Patients | 13 (21.7%) | 47 (78.3%) | ||
| Age >65, years | 12 (92.3%) | 40 (85.1%) | 0.49 | |
| Sex | Men | 7 (53.8%) | 37 (78.7%) | 0.073 |
| Women | 6 (46.1%) | 10 (21.3%) | ||
| BMI >22.3 kg/m2 | 12 (92.3%) | 21 (44.7%) | 0.002 | |
| Smoking status | 7 (53.8%) | 28 (59.6%) | 0.758 | |
| Pathological stage | 0.57 | |||
| 0 | 0 (0%) | 1 (2.1%) | ||
| I | 2 (15.4%) | 11 (23.4%) | ||
| II | 6 (46.2%) | 12 (25.5%) | ||
| III | 5 (38.5%) | 20 (42.6%) | ||
| IV | 0 (0%) | 3 (6.4%) | ||
| Adjuvant chemotherapy | 7 (53.8%) | 20 (42.6%) | 0.47 | |
| Operation time >319 min | 12 (92.3%) | 28 (59.6%) | 0.027 | |
| Blood loss >230 mL | 6 (46.2%) | 6 (12.8%) | 0.008 | |
| All complications | 10 (76.9%) | 20 (42.6%) | 0.028 | |
| Diabetes mellitus | 2 (15.4%) | 10 (21.3%) | 1.00 | |
| Sarcopenia | 7 (53.8%) | 16 (34.0%) | 0.19 | |
| Recurrence | 4 (30.7%) | 16 (34.0%) | 0.82 | |
| Stoma diameter >18.6 mm | 11 (84.6%) | 22 (46.8%) | 0.015 | |
| VFA >89.2 cm2 | 12 (92.3%) | 23 (48.9%) | 0.005 | |
| SFA >173.2 cm2 | 8 (61.5%) | 7 (14.9%) | 0.001 | |
Abbreviations: BMI, body mass index; PSH, parastomal hernia; VFA, visceral fat area; SFA, subcutaneous fat area
Table 3.
Results of Multivariate Analysis for Parastomal Hernia.
| Variables | Multivariate analysis | |
|---|---|---|
| OR (95% CI) | p-value | |
| BMI >22.3 kg/m2 | 7.73 (0.45-130.9) | 0.15 |
| Operation time >319 min | 6.14 (0.46-80.5) | 0.17 |
| Blood loss >230 mL | 9.01 (0.59-136.1) | 0.11 |
| All complications | 6.73 (0.70-64.2) | 0.09 |
| Stoma diameter >18.6 mm | 9.59 (0.58-158.3) | 0.114 |
| VFA >89.2 cm2 | 0.34 (0.01-10.7) | 0.539 |
| SFA >173.2 cm2 | 16.7 (1.29-217.2) | 0.031 |
Abbreviations: BMI, body mass index; CI, confidence interval; OR, odds ratio; VFA, visceral fat area; SFA, subcutaneous fat area
Discussion
In the present study, we reported that SFA was an independent risk factor for PSH following colostomy with the transperitoneal approach. To the best of our knowledge, this is the first study to investigate the potential role of physical components, including sarcopenia, VFA, and SFA, contribute to the development of PSH.
It is well known that complications associated with permanent colostomy reduce patient QOL. In particular, PSH not only causes cosmetic problems, but also leads to bowel obstruction and strangulation. Generally, the results of PSH repair are relatively poor[3]. The postoperative complication rate reportedly ranges from 20-60%, with relapse, wound infection, and intra-abdominal abscess being the most common complications[13]. Moreover, no standardized repair strategies for PSH have been established. Consequently, it is critical for surgeons to focus on the prevention of PSH and identification and management of its preoperative risk factors. Previous studies have indicated that higher BMI is significantly associated with PSH[14,15]. While BMI can be used for a rapid evaluation of a patient's physical health, it lacks precision and does not provide accurate information regarding physical components, such as muscle, visceral, or subcutaneous fat[16]. More detailed assessments of physical and nutritional parameters, such as sarcopenia and the ratio of visceral to subcutaneous fat, are associated with postoperative complications in gastrointestinal cancer, and may be have a considerable effect on patient outcomes[17,18]. Likewise, identifying additional detailed individual PSH risk predictors may be helpful in the prevention of PSH.
The mechanism underlying PSH stemming from high SFAs may be explained by two theories. Firstly, the excessive adipose tissue may be responsible for protracted wound healing by stimulating local inflammatory lesions through cytokines[19]. Subcutaneous fat has been identified as a risk factor for incisional hernia after gastric and colorectal cancer surgery[20,21]. In this context, Yamada et al. hypothesized that excessive subcutaneous fat may inhibit fascial closure. A permanent colostomy generally necessitates dissection of the fascia of the rectus abdominis muscles to create a stoma, and the dissected fascia is not usually sutured. The impairment of fascial closure around the colostomy site may be more directly actualized by excessive subcutaneous adipose tissue in contact with the dissected fascia. This mechanism of delayed fascial closure and wound healing may be a contributing factor in the development of PSH. Second, thick subcutaneous fat is a known risk factor for surgical site infections (SSIs)[22]. Dense subcutaneous fat makes it difficult for surgeons to obtain an adequate surgical field during abdominal surgery, thus necessitating a larger surgical incision. Permanent colostomies are no exception. Obesity, longer wound sites, and stoma creation are well-known risk factors of SSI[23]. In such infection states, local inflammation is elevated, and wound healing is prominently delayed. Moreover, SSIs were reported to be a representative risk factor for wound dehiscence and incisional hernia[24]. Since the stomal site is constantly exposed to intestinal fluid and intestinal bacteria around the wound, minor infections and inflammation usually arise and occur concomitant with SSI. Excessive subcutaneous fat may create both an inflammatory and infectious environment and facilitate PSH.
In several studies, the extraperitoneal colostomy method was shown to significantly prevent PSH compared to the transperitoneal route[5,7]. The extraperitoneal technique for colostomy was initially reported by Goligher in 1958, and this technique was specifically outlined for laparotomy. Furthermore, in recent years, Hamada reported a method of extraperitoneal colostomy for laparoscopic surgery[6,25,26]. Moreover, Ota et al. demonstrated that laparoscopic extraperitoneal colostomy can reduce the risk of PSH in comparison to laparotomy[27]. However, the extraperitoneal method is more complicated and requires a longer operative time than the transperitoneal procedure. Performing extraperitoneal colostomy in all patients who undergo APR or Hartmann's procedure may not be realistic. Therefore, surgeons should consider opting the extraperitoneal method for permanent colostomy, particularly in those higher-risk patients, such as those with obesity and high SFA, to prevent PSH.
This study had several limitations. First, this was a single-institution retrospective study with a small sample size, potentially introducing selection bias. Second, the surgical procedures for colostomy were not standardized. Moreover, our data analysis only included the transperitoneal method of stoma creation, which is associated with a higher risk of PSH than that of the extraperitoneal method. As such, the risk factors for PSH after extraperitoneal stoma creation remain unclear. Finally, some confounding factors of PSH were not completely excluded. To address these limitations, further multi-institutional studies with larger cohorts should be conducted.
In conclusion, our study highlights SFA as an independent risk factor for PSH after transperitoneal colostomy for colorectal cancer. Our findings contribute to enhancing our understanding of PSH prevention and risk prediction.
Conflicts of Interest
There are no conflicts of interest.
Author Contributions
TA and TK wrote the manuscript. YS supervised the study and served as the attending surgeon of the presented patients. All the authors have read and approved the final version of the manuscript. Takashi Aida and Teppei Kamada contributed equally to this work.
Approval by Institutional Review Board (IRB)
This study was approved by the Institutional Review Board of the International University of Health and Welfare Hospital (approval no: 21-B-22).
Consent for Publication
The patients have provided consent for the publication of images.
Availability of Data and Material
All data generated or analyzed during this study are included in this published article.
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