Abstract
Objectives:
Sarcopenia is generally defined based on the age-related muscle mass and weakness. However, it has been reported that patients with Crohn's disease, who develop severe inflammation of the gastrointestinal tract, are more likely to develop sarcopenia. We retrospectively investigated the effect of the iliopsoas muscle area, which is an indicator of sarcopenia, on postoperative complications in patients with Crohn's disease.
Methods:
We included 98 patients with Crohn's disease who underwent surgery in our department between January 2016 and December 2021, and performed retrospectively analyzed. The psoas muscle index (PMI) was calculated as the average of the left and right iliopsoas muscles (L3, cm2) / height2. We divided patients into the low PMI (men <2.33 cm2/m2, women <1.85 cm2/m2) and normal PMI groups and compared their preoperative and intraoperative factors and postoperative outcomes.
Results:
The median age of the 98 patients was 37.0 (17-77) years. Complications were noted in 40 patients (40.8%), including 10 (10.2%) with anastomotic leakage. There were 26 (26.5%) patients with a low PMI. The incidence of all postoperative complications, grade ≥2 complications, anastomotic leakage and surgical site infection (SSI) were significantly higher in the low-PMI group than in the normal-PMI group. According to a multivariate analysis, low PMI (p=0.04) was only independent predictor for grade 2 or above postoperative complications.
Conclusions:
A low PMI is associated with postoperative complications, especially anastomotic leakage, in patients with Crohn's disease.
Keywords: Crohn's disease, Postoperative complications, PMI
Introduction
Crohn's disease (CD) is an intractable inflammatory bowel disease that often develops in young individuals. Despite the advancements in medical therapy for Crohn's disease, the disease repeatedly relapses and goes into remission during the long course of the disease. Due to severe stenosis, fistula, or abscess during the course of the disease, intestinal resection is frequently indicated. The aim of surgical treatment is to improve these issues, in order to preserve the patient's quality of life. This includes an early restart of medical therapy to maintain disease control and an early return to society. Therefore, it is necessary to complete surgical treatment without postoperative complications in order to achieve the desired outcome[1,2]. The preoperative nutritional status of patients with Crohn's disease is often poor. Additionally, intestinal anastomosis is associated with various postoperative complications, including anastomotic leakage. Recently, sarcopenia has been reported to be a prognostic factor for various diseases[3-5]; however there have been few reports on the association between sarcopenia and postoperative complications in patients with Crohn's disease[6-8]. We conducted this retrospective study to investigate the relationship between sarcopenia and postoperative complications in patients with CD.
Methods
Patients
We retrospectively analyzed 98 patients with Crohn's disease who underwent surgery at our department between January 2016 and December 2021. In all cases, the left and right iliopsoas muscle areas at the L3 level were measured on preoperative CT scans, and the mean value was divided by the square of the height (m2) to calculate the psoas muscle index (PMI). All clinical data are shown in Table 1. Postoperative complications were defined as those occurring within 30 days after surgery and were classified according to the Clavien-Dindo classification (CDC) system.
Table 1.
Clinical Characteristics of 98 Patients with Crohn’s Disease.
| Clinical features | n=98 | |
|---|---|---|
| Sex | Male | 79 (80.6%) |
| Female | 19 (19.4%) | |
| Age (years)* | Mean (SD) | 37 (12.2) |
| BMI* | Mean (SD) | 20.1 (3.3) |
| Biological products | − | 25 (25.5%) |
| + | 73 (74.5%) | |
| Steroid medicines | − | 81 (82.7%) |
| + | 17 (17.3%) | |
| Alcohol | − | 86 (90.5%) |
| + | 9 (9.5%) | |
| Smoker | − | 65 (68.4%) |
| + | 30 (31.6%) | |
| Comorbidities | Heart disease | 5 (5.1%) |
| Lung disease | 8 (8.2%) | |
| Diabetes mellitus | 2 (2.0%) | |
| Site of lesion | Small intestine | 63 (64.3%) |
| Colon | 16 (16.3%) | |
| Small intestine and colon | 7 (0.07%) | |
| Rectum | 1 (0.01%) | |
| Anus | 2 (0.02%) | |
| Indications for surgery | Stenosis | 62 (63.2%) |
| Abscess | 12 (12.2%) | |
| Fistula | 12 (12.2%) | |
| Perforation | 10 (10.2%) | |
| Cancer | 1 (0.01%) | |
| Severe ulcer | 1 (0.01%) | |
| Number of anastomosis | 0 | 12 (12.2%) |
| 1 | 74 (75.5%) | |
| 2 | 11 (11.2%) | |
| 3 | 1 (1.0%) | |
| Type of anastomosis | End-to-end anastomosis | 46 (46.9%) |
| Side-to-side anastomosis | 36 (36.7%) | |
| Operative time (min)* | Mean (SD) | 222 (99.8) |
| Intraoperative bleeding (ml)* | Mean (SD) | 115 (460) |
| Postoperative complications | ||
| All | 40 (40.8%) | |
| Surgical Site Infection (SSI) | 28 (28.6%) | |
| Anastomotic leakage | 10 (10.2%) | |
| Remote infection | 4 (4.1%) | |
| Post operative ileus (POI) | 8 (8.2%) | |
| CDC grade | ||
| I | 1 (1.0%) | |
| II | 17 (17.3%) | |
| IIIa | 15 (15.3%) | |
| IIIb | 7 (7.1%) |
Continuous parameters are presented as the mean (SD)*, and categorical parameters are presented as n (%). BMI body mass index, PNI prognostic nutritional index, Alb albumin, Biological products Biological treatment within 30 days prior to surgery, Steroid medicines steroid treatment within 30 days prior to surgery, CDC Clavien-Dindo classification, SSI superficial and deep incisional and organ cavity surgical site infection, POI post operative ileus.
Postoperative complications
Table 1 shows the postoperative complications. These were defined as in-hospital morbidity or mortality occurring within 30 days of surgery and were classified according to the CDC system[9]. Surgical site infection (SSI), anastomotic leakage, remote infection, and postoperative ileus (POI) were included as postoperative complications.
SSI and Remote infection were also diagnosed by surgeons according to the CDC guidelines[10]. POI was defined in cases with symptoms such as nausea, vomiting, and abdominal bloating as well as dilation of the small intestine without obvious obstruction confirmed on imaging[11]. Anastomotic leakage was defined according to the international criteria established by the International Study Group of Rectal Cancer (ISREC, 2010) as a disruption of anastomotic integrity, resulting in the leakage of intestinal contents into the abdominal cavity or through a drain. The diagnosis was made when clinical symptoms such as fever, abdominal pain, or purulent or fecal drainage from the drain were observed[12]. In such cases, abdominal computed tomography (CT) was performed, and the presence of an intra-abdominal abscess or extraluminal air was considered indicative of anastomotic leakage. Additionally, water-soluble contrast enema was performed, and if an abnormal communication between the intra- and extraluminal compartments was confirmed, the diagnosis of anastomotic leakage was established.
Psoas muscle index (PMI)
The preoperative PMI was calculated using CT/MRI images obtained within 30 days prior to the operation. CT-based PMI measurements were performed by two independent investigators who were blinded to the corresponding clinical background data. The final PMI value was determined as the average of their measurements. The left and right iliopsoas muscle areas was measured retrospectively in a transverse section at the L3 level by blinded researchers. The mean right and left area was used for the statistical analyses, and the psoas muscle index (PMI) was calculated by correcting this for height (m2). The primary endpoint of this study is the incidence of postoperative complications in the low-PMI and normal-PMI groups.
Statistical analyses
Continuous variables are described as median values (interquartile range [IQR]). Univariate analyses were performed using the chi-square test or Fisher's exact test for categorical variables. Multivariate analyses, that included variables with p values of <0.1 in the univariate analyses and items that is able to associated with anastomotic leakage in patients with Crohn's disease were performed using a logistic regression model to identify predictors grade 2 or above postoperative complications. Odds ratios (ORs) and 95% confidence intervals (CIs) were calculated. All statistical analyses were performed using EZR (Saitama Medical Center, Jichi Medical University, Saitama, Japan), which is a graphical user interface for R (The R Foundation for Statistical Computing, Vienna, Austria)[13].
Ethics approval and consent to participate
The study was carried out with the approval of the ethics committee of our institution (Osaka Metropolitan University Graduate School of Medicine, reference number 3798) and with the informed consent of the participants. All research methods were carried out in accordance with the relevant guidelines and regulations.
Results
Patient characteristics
A total of 98 (males, n=79; females, n=19) patients were included in this study. The median age was 37.0 years (17-77) (Table 1). Twenty-six patients were classified into the low-group and 72 patients were classified into the normal-PMI (Figure 1, 2). The mean disease duration was 10 years (SD 9.0); 73 patients used biologics preoperatively and 17 used steroids within 30 days prior to surgery.
Figure 1.
ROC curve for males.
According to the ROC curve analysis, the cutoff value for predicting postoperative complications in males was 2.33.
Figure 2.
ROC curve for females.
According to the ROC curve analysis, the cutoff value for predicting postoperative complications in females was 1.85.
Psoas muscle index (PMI)
In the present study, the median PMI for males was 2.856 (1.418-5.190), while the median PMI for females was 1.885 (1.335-3.236). An ROC curve analysis was used to determine the cutoff values of the PMI. According to this analysis, the cutoff value for low-PMI was <2.33 cm2/m2 and the specificity was 0.911, and the sensitivity was 0.382 in males and <1.85 cm2/m2 and the specificity was 0.769, and the sensitivity was 1.000 in females (Figure 1, 2). The patients were classified into the low-PMI and normal-PMI groups according to these cutoff values.
Correlation between the PMI and clinical characteristic factors
Regarding the preoperative factors, the low-PMI group showed a significant differences in female (p=0.04), low BMI (p=0.0001), low albumin (p=0.0000001), and low PNI (p=0.0000002) (Table 2). Regarding the intraoperative factors, blood loss >115 ml was significantly more frequent in the low-PMI group. Postoperative complications occurred in 40 of 98 patients (40.8%), 39 (39.8%) had grade >2 complications, 28 (28.6%) had SSI and 10 (10.2%) had anastomotic leakage. The incidence rates of all postoperative complications (p=0.0001), grade >2 complications (p=0.0001), SSI (p=0.002) and anastomotic leakage (p=0.003) were significantly higher in the low-PMI group than in the normal-PMI group.
Table 2.
Clinical Background Factors Associated with a Preoperative Decrease in Skeletal Muscle Mass.
| Back ground | Low PMI (n=26) | Normal PMI (n=72) | P-value |
|---|---|---|---|
| Sex | |||
| Female | 9 (37.4%) | 10 (13.9%) | 0.04 |
| Age (years)* | |||
| mean (SD) | 38.3 (10.8) | 38.1 (12.8) | 0.94 |
| BMI* | |||
| mean (SD) | 18.6 (2.2) | 21.4 (3.3) | 0.0001 |
| Alcohol | 1 (3.8%) | 8 (11.6%) | 0.44 |
| Smoker | 9 (34.6%) | 21 (30.4%) | 0.81 |
| Comorbidities | |||
| Heart disease | 0 (0%) | 5 (6.9%) | 0.32 |
| Lung disease | 1 (3.8%) | 7 (9.7%) | 0.68 |
| Diabetes mellitus | 0 (0%) | 2 (2.8%) | 1 |
| PNI* | |||
| mean (SD) | 35.9 (6.9) | 44.3 (6.3) | 0.0000002 |
| Alb (g/dL)* | |||
| mean (SD) | 3.07 (0.60) | 3.79 (0.52) | 0.0000001 |
| Biological Products | |||
| Positive | 18 (69.2%) | 55 (76.4%) | 0.60 |
| Steroid medicines | |||
| Positive | 4 (15.4%) | 13 (18.1%) | 1.00 |
| Indication for surgery | |||
| Penetrating type | 14 (53.8%) | 23 (31.9%) | 0.06 |
| Operative procedure | |||
| Open surgery | 17 (65.4%) | 26 (36.1%) | 0.01 |
| Emergency operation | |||
| Positive | 3 (11.5%) | 5 (6.9%) | 0.43 |
| Type of Surgery | |||
| Colectomy | 10 (38.5%) | 14 (18.3%) | 0.058 |
| Type of Anastomosis | |||
| End-to-end | 13 (65.0%) | 33 (53.2%) | 0.441 |
| Number of anastomosis | |||
| ≥2 | 4 (15.4%) | 8 (11.1%) | 0.728 |
| Operative time (min) | |||
| mean (SD) | 293.88 (160.24) | 221.04 (57.37) | 0.001 |
| Intraoperative bleeding (ml) | |||
| mean (SD) | 500.96 (778.19) | 170.83 (222.63) | 0.001 |
| ASA* | |||
| mean (SD) | 2.0 (0) | 1.99 (0.12) | 0.55 |
| All complications | 19 (73.1%) | 21 (29.2%) | 0.0001 |
| SSI | 14 (53.8%) | 14 (19.4%) | 0.002 |
| Anastomotic leakage | 7 (26.9%) | 3 (4.2%) | 0.003 |
| Remote infection | 2 (7.7%) | 2 (2.8%) | 0.29 |
| POI | 2 (7.7%) | 6 (8.3%) | 1.00 |
| CDC | |||
| Grade ≥2 | 19 (73.1%) | 20 (27.8%) | 0.0001 |
Continuous parameters are presented as the mean (SD)*, and categorical parameters are presented as n (%). BMI body mass index, PNI prognostic nutritional index, Alb albumin, Biological products Biological treatment within 30 days prior to surgery, Steroid medicines steroid treatment within 30 days prior to surgery, CDC Clavien–Dindo classification, SSI superficial and deep incisional and organ cavity surgical site infection, POI post operative ileus, P<0.05.
Univariate and multivariate analyses for grade 2 or above postoperative complication
Table 3 shows the results of a univariate analysis of grade 2 or above postoperative complications. The univariate analysis showed that open surgery (p=0.005) and low-PMI (p=0.0001) were significantly associated with grade 2 or above postoperative complications. In the multivariate analysis, low-PMI (p=0.02) was only independent predictor of grade 2 or above postoperative complications.
Table 3.
Clinical Characteristics Associated with Grade 2 or Above Postoperative Complications.
| Univariate analysis | Multivariate analysis | |||||
|---|---|---|---|---|---|---|
| Variable | Hazard | 95%CI | P-value | Hazard | 95%CI | P-value |
| Sex | ||||||
| Female | 0.64 | 0.22-1.87 | 0.42 | |||
| Age | ||||||
| 1.02 | 0.98-1.05 | 0.34 | ||||
| BMI | ||||||
| 0.97 | 0.85-1.09 | 0.58 | ||||
| PNI | ||||||
| 0.95 | 0.90-1.01 | 0.11 | 1.36 | 0.18-10.10 | 0.762 | |
| Alb | ||||||
| 0.54 | 0.28-1.08 | 0.08 | 0.588 | 0.09-3.65 | 0.569 | |
| Biological Products | ||||||
| Positive | 0.41 | 0.16-1.03 | 0.06 | 0.37 | 0.101-1.41 | 0.148 |
| Steroid medicines | ||||||
| Positive | 0.58 | 0.19-1.79 | 0.34 | |||
| Indication for surgery | ||||||
| Penetrating type | 1.80 | 0.78-4.15 | 0.17 | |||
| Operative procedure | ||||||
| Open surgery | 3.37 | 1.45-7.84 | 0.005 | 2.450 | 0.625-9.60 | 0.198 |
| Emergency operation | ||||||
| positive | 1.57 | 0.37-6.69 | 0.54 | |||
| Type of Surgery | ||||||
| Colectomy | 3.91 | 1.46-10.50 | 0.0068 | 3.960 | 0.954-16.4 | 0.058 |
| Type of Anastomosis | ||||||
| End-to-end | 2.18 | 0.86-5.55 | 0.10 | 2.33 | 0.79-6.82 | 0.121 |
| Number of anastomosis | ||||||
| ≥2 | 1.61 | 0.48-5.40 | 0.44 | |||
| Operative time (min) | ||||||
| 1.82 | 0.80-4.14 | 0.15 | ||||
| Intraoperative bleeding (ml) | ||||||
| 2.18 | 0.95-4.97 | 0.07 | 1.21 | 0.342-4.24 | 0.771 | |
| PMI | ||||||
| Low PMI | 7.06 | 2.57-19.3 | 0.0001 | 4.16 | 1.06-16.30 | 0.040 |
BMI body mass index, PNI prognostic nutritional index, Alb albumin, Biological products Biological treatment within 30 days prior to surgery, Steroid medicines steroid treatment within 30 days prior to surgery, P<0.05.
Discussion
The reoperation rate for Crohn's disease has been reported as 22-28% at 5 years, 30-40% at 10 years, and approximately 55% at 15 years[14,15]. This indicates that the likelihood of requiring surgical intervention during the treatment course of Crohn's disease is significantly high. If patients with Crohn's disease can undergo surgical treatment without postoperative complications, early initiation of pharmacological therapy becomes possible. Therefore, predicting the occurrence of postoperative complications is crucial.
In this study, a low psoas muscle index (PMI) was significantly associated with female sex, low body mass index (BMI), and poor nutritional indicators such as prognostic nutritional index (PNI) and albumin levels. Among the Crohn's disease phenotypes, patients with a low PMI were more frequently classified as the penetrating type. Sarcopenia is a condition characterized by a progressive decline in skeletal muscle mass, muscle strength, and physical function due to aging or disease. While originally defined as primary sarcopenia related to aging, sarcopenia caused by disease or malnutrition is classified as secondary sarcopenia. Sarcopenia associated with Crohn's disease falls into the category of secondary sarcopenia[16]. Patients with Crohn's disease are prone to malnutrition due to malabsorption, protein loss from the intestinal tract, and increased energy demands driven by chronic inflammation. Consequently, they frequently experience diarrhea and loss of appetite, which further predisposes them to sarcopenia. Furthermore, the penetrating type of Crohn's disease is often accompanied by fistulas and abscesses, leading to chronic inflammation that may accelerate the development of sarcopenia.
There is limited discussion on sex differences in Crohn's disease. While previous reports have described muscle mass reduction in Crohn's disease patients[17], few studies have explored sex differences in detail. However, some reports suggest that females have a higher prevalence of penetrating-type Crohn's disease and exhibit stronger inflammatory responses[18]. Considering the heightened inflammatory response and increased prevalence of the penetrating phenotype in females, they may be more susceptible to muscle mass reduction. Our study also showed a tendency for lower PMI in female Crohn's disease patients, supporting this hypothesis.
Additionally, the low PMI group had a higher proportion of open surgeries and greater intraoperative blood loss. The association between open surgery and penetrating-type Crohn's disease can be attributed to the frequent presence of fistulas and abscesses, making laparoscopic surgery technically challenging and leading to a preference for open surgery. Consequently, open surgery tends to result in higher intraoperative blood loss compared to laparoscopic surgery[19]. The findings of our study were consistent with these observations.
Anastomotic leakage is one of the major postoperative complications in Crohn's disease surgery, with a reported incidence of approximately 10%[20]. Risk factors for anastomotic leakage include nutritional status, disease phenotype, medication use (e.g., steroids), surgical history, and surgical approach[21-24]. In our study, anastomotic leakage occurred in 10.2% of patients, which is consistent with previous reports.
Univariate analysis in our study showed that colectomy, cases where the colon was involved in an anastomosis, open surgery, and low PMI were significantly associated with postoperative complications of grade 2 or higher in Crohn's disease patients. Compared to small bowel anastomosis, colonic anastomosis carries a higher risk of infectious complications and anastomotic failure, leading to a higher incidence of postoperative complications. The relationship between open surgery and postoperative complications has been a longstanding topic of debate in gastrointestinal surgery. While open surgery is generally considered to have a higher postoperative complication rate than laparoscopic surgery[25], some reports suggest no significant difference. Similar trends have been observed in Crohn's disease surgery, with some studies reporting fewer postoperative complications following laparoscopic surgery[26,27].
The impact of anti-TNF therapy and steroid use on postoperative complications in Crohn's disease surgery remains a widely debated topic. The ECCO-ESCP consensus suggests that anti-TNF therapy may increase the risk of postoperative sepsis, intra-abdominal abscess, anastomotic leakage, surgical site infections, and hospital readmissions. However, there is no clear data on the optimal duration of drug discontinuation before surgery. Similarly, steroid use has been identified as a risk factor for anastomotic leakage and infections[21,22]. However, in our study, there was no significant association between postoperative complications and the use of anti-TNF therapy or steroids. Additionally, previously established predictors of anastomotic leakage, such as PNI, smoking, and the number and type of anastomosis[28], did not show a significant correlation with postoperative complications in our study.
Our study revealed that PMI, an indicator of muscle mass, was associated with postoperative complications in Crohn's disease surgery. Moreover, in multivariate analysis, PMI was identified as an independent predictor of postoperative complications. Previous studies have reported that preoperative sarcopenia is associated with postoperative complications in gastrointestinal cancer patients[29-31]. Recent research has provided increasing insights into the pathophysiology of Crohn's disease, suggesting that inflammatory cytokines play a significant role in disease progression[32]. Pedersen et al. have reported that inflammatory cytokines promote sarcopenia[33]. Patients requiring surgery for Crohn's disease often exhibit elevated inflammatory cytokines and severe malnutrition, predisposing them to sarcopenia and, consequently, an increased risk of postoperative complications. PMI strongly correlates with skeletal muscle mass and serves as a useful marker for diagnosing sarcopenia[34]. Therefore, a low PMI may be an independent risk factor for postoperative complications. Since PMI can be easily measured using abdominal CT scans, it is a practical tool for preoperative risk assessment. PMI can be obtained from L3-level CT images and is reported as a convenient alternative marker correlating with the skeletal muscle index (SMI)[35]. Our institution has also reported the relationship between PMI and cancer, demonstrating that PMI measurement via CT can be performed without special equipment[36,37]. Given that many Crohn's disease surgeries are performed as emergency procedures, the simplicity of preoperative risk assessment is crucial. Our study demonstrated that PMI was associated with postoperative complications, particularly anastomotic leakage. If a low PMI predicts a high risk of anastomotic failure, modifications to surgical strategy, such as considering stoma creation instead of primary anastomosis, may be warranted, especially in cases involving open colectomy and colonic anastomosis. Moreover, the ability to predict postoperative complications could facilitate early intervention, such as delaying the initiation of oral intake or administering prophylactic antibiotics.
Limitations
There are several limitations to our study. First, this was a retrospective study conducted at a single institution with a relatively small sample size. Second, although the PMI cutoff value was determined based on ROC curve analysis, standardized methods for establishing the optimal cutoff value are needed. Further large-scale prospective studies are required to validate the utility of preoperative PMI in predicting postoperative complications.
Conclusion
Low preoperative PMI was identified as an independent risk factor for postoperative complications in patients with Crohn's disease. Crohn's disease patients often have poor preoperative nutritional status, and improving these conditions may be necessary for effective surgical treatment.
Conflicts of Interest
There are no conflicts of interest.
Author Contributions
Maho Sasaki designed the study, performed the statistical analysis, and drafted the manuscript; Tatsunari Fukuoka designed the study, performed the statistical analysis and drafted the manuscript; Masatsune Shibutani collected the clinical data and critically revised the manuscript; Hiroaki Kasashima collected the clinical data and critically revised the manuscript; and Kiyoshi Maeda designed the study and critically reviewed the manuscript. All authors have read and approved the final manuscript.
Ethics Approval and Consent to Participate
The study was carried out with the approval of the ethics committee of our institution (Osaka Metropolitan University Graduate School of Medicine, reference number 3798) and with the informed consent of the participants. All research methods were carried out in accordance with the relevant guidelines and regulations.
References
- 1.Tillinger W, Mittermaier C, Lochs H, et al. Health-related quality of life in patients with Crohn's disease: influence of surgical operation--a prospective trial. Dig Dis Sci. 1999 May;44(5):932-8. [DOI] [PubMed] [Google Scholar]
- 2.Nakase H, Uchino M, Shinzaki S, et al. Evidence-based clinical practice guidelines for inflammatory bowel disease 2020. J Gastroenterol. 2021 Jun;56(6):489-526. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 3.Kudou K, Saeki H, Nakashima Y, et al. Prognostic Significance of Sarcopenia in Patients with Esophagogastric Junction Cancer or Upper Gastric Cancer. Ann Surg Oncol. 2017 Jul;24(7):1804-10. [DOI] [PubMed] [Google Scholar]
- 4.Deng CY, Lin YC, Wu JS, et al. Progressive Sarcopenia in Patients With Colorectal Cancer Predicts Survival. AJR Am J Roentgenol. 2018 Mar;210(3):526-32. [DOI] [PubMed] [Google Scholar]
- 5.Gruber ES, Jomrich G, Tamandl D, et al. Sarcopenia and sarcopenic obesity are independent adverse prognostic factors in resectable pancreatic ductal adenocarcinoma. PLoS One. 2019 May;14(5):e0215915. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 6.Zhang C, Yu D, Hong L, et al. Prevalence of Sarcopenia and Its Effect on Postoperative Complications in Patients with Crohn's Disease. Gastroenterol Res Pract. 2021 Sep;2021:3267201. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 7.Zhang T, Cao L, Cao T, et al. Prevalence of Sarcopenia and Its Impact on Postoperative Outcome in Patients With Crohn's Disease Undergoing Bowel Resection. JPEN J Parenter Enteral Nutr. 2017 May;41(4):592-600. [DOI] [PubMed] [Google Scholar]
- 8.Zager Y, Khalilieh S, Ganaiem O, et al. Low psoas muscle area is associated with postoperative complications in Crohn's disease. Int J Colorectal Dis. 2021 Mar;36(3):543-50. [DOI] [PubMed] [Google Scholar]
- 9.Dindo D, Demartines N, Clavien PA. Classification of surgical complications: a new proposal with evaluation in a cohort of 6336 patients and results of a survey. Ann Surg. 2004 Aug;240(2):205-13. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 10.Berríos-Torres SI, Umscheid CA, Bratzler DW, et al. Centers for Disease Control and Prevention Guideline for the Prevention of Surgical Site Infection, 2017. JAMA Surgery. 2017 Aug;152(8):784-91. [DOI] [PubMed] [Google Scholar]
- 11.Vather R, Trivedi S, Bissett I. Defining postoperative ileus: results of a systematic review and global survey. J Gastrointest Surg. 2013 May;17(5):962-72. [DOI] [PubMed] [Google Scholar]
- 12.Rahbari NN, Weitz J, Hohenberger W, et al. Definition and grading of anastomotic leakage following anterior resection of the rectum: a proposal by the International Study Group of Rectal Cancer. Surgery. 2010 Mar;147(3):339-51. [DOI] [PubMed] [Google Scholar]
- 13.Kanda Y. Investigation of the freely available easy-to-use software ‘EZR’ for medical statistics. Bone Marrow Transplant. 2013 Mar;48(3):452-8. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 14.Trnka YM, Glotzer DJ, Kasdon EJ, et al. The long-term outcome of restorative operation in Crohn's disease: influence of location, prognostic factors and surgical guidelines. Ann Surg. 1982 Sep;196(3):345-55. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 15.Ozuner G, Fazio VW, Lavery IC, et al. Reoperative rates for Crohn's disease following strictureplasty. Long-term analysis. Dis Colon Rectum. 1996 Nov;39(11):1199-203. [DOI] [PubMed] [Google Scholar]
- 16.Cruz-Jentoft AJ, Bahat G, Bauer J, et al. Sarcopenia: revised European consensus on definition and diagnosis. Age Ageing. 2019 Jul;48(4):601. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 17.Ryan E, McNicholas D, Creavin B, et al. Sarcopenia and Inflammatory Bowel Disease: A Systematic Review. Inflamm Bowel Dis. 2019 Jan;25(1):67-73. [DOI] [PubMed] [Google Scholar]
- 18.Gargallo-Puyuelo CJ, Ricart E, Iglesias E, et al. Sex-Related Differences in the Phenotype and Course of Inflammatory Bowel Disease: SEXEII Study of ENEIDA. Clin Gastroenterol Hepatol. 2024 Nov;22(11):2280-90. [DOI] [PubMed] [Google Scholar]
- 19.Patel SV, Patel SV, Ramagopalan SV, et al. Laparoscopic surgery for Crohn's disease: a meta-analysis of perioperative complications and long term outcomes compared with open surgery. BMC Surg. 2013 May;13:14. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 20.Johnston WF, Stafford C, Francone TD, et al. What Is the Risk of Anastomotic Leak After Repeat Intestinal Resection in Patients With Crohn's Disease? Dis Colon Rectum. 2017 Dec;60(12):1299-306. [DOI] [PubMed] [Google Scholar]
- 21.Yamamoto T, Allan RN, Keighley MR. Risk factors for intra-abdominal sepsis after surgery in Crohn's disease. Dis Colon Rectum. 2000 Aug;43(8):1141-5. [DOI] [PubMed] [Google Scholar]
- 22.Post S, Betzler M, von Ditfurth B, et al. Risks of intestinal anastomoses in Crohn's disease. Ann Surg. 1991 Jan;213(1):37-42. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 23.Heimann TM, Greenstein AJ, Mechanic L, et al. Early complications following surgical treatment for Crohn's disease. Ann Surg. 1985 Apr;201(4):494-8. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 24.Simillis C, Purkayastha S, Yamamoto T, et al. A meta-analysis comparing conventional end-to-end anastomosis vs. other anastomotic configurations after resection in Crohn's disease. Dis Colon Rectum. 2007 Oct;50(10):1674-87. [DOI] [PubMed] [Google Scholar]
- 25.Yamamoto S, Inomata M, Katayama H, et al. Short-term surgical outcomes from a randomized controlled trial to evaluate laparoscopic and open D3 dissection for stage II/III colon cancer: Japan Clinical Oncology Group Study JCOG 0404. Ann Surg. 2014 Jul;260(1):23-30. [DOI] [PubMed] [Google Scholar]
- 26.Pak SJ, Kim YI, Yoon YS, et al. Short-term and long-term outcomes of laparoscopic vs open ileocolic resection in patients with Crohn's disease: Propensity-score matching analysis. World J Gastroenterol. 2021 Nov;27(41):7159-72. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 27.Maartense S, Dunker MS, Slors JF, et al. Laparoscopic-assisted versus open ileocolic resection for Crohn's disease: a randomized trial. Ann Surg. 2006 Feb;243(2):143-9; discussion 50-3. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 28.Avellaneda N, Rodrigues Coy CS, Sarubbi Fillmann H, et al. Risk factors for major complications after surgical treatment of primary ileocecal Crohn's disease. A multicentric Latin American experience. Cir Esp (Engl Ed). 2023 Dec;101(12):824-32. [DOI] [PubMed] [Google Scholar]
- 29.Chen XY, Li B, Ma BW, et al. Sarcopenia is an effective prognostic indicator of postoperative outcomes in laparoscopic-assisted gastrectomy. Eur J Surg Oncol. 2019 Jun;45(6):1092-8. [DOI] [PubMed] [Google Scholar]
- 30.Ida S, Watanabe M, Yoshida N, et al. Sarcopenia is a Predictor of Postoperative Respiratory Complications in Patients with Esophageal Cancer. Ann Surg Oncol. 2015 Dec;22(13):4432-7. [DOI] [PubMed] [Google Scholar]
- 31.Yang J, Zhang T, Feng D, et al. A new diagnostic index for sarcopenia and its association with short-term postoperative complications in patients undergoing surgery for colorectal cancer. Colorectal Dis. 2019 May;21(5):538-47. [DOI] [PubMed] [Google Scholar]
- 32.Masuta Y, Minaga K, Kurimoto M, et al. Activation of nucleotide-binding oligomerization domain 2 by muramyl dipeptide negatively regulates Toll-like receptor 9-mediated colonic inflammation through the induction of deubiquitinating enzyme A expression. Int Immunol. 2023 Feb;35(2):79-94. [DOI] [PubMed] [Google Scholar]
- 33.Pedersen BK, Febbraio MA. Muscle as an endocrine organ: focus on muscle-derived interleukin-6. Physiol Rev. 2008 Oct;88(4):1379-406. [DOI] [PubMed] [Google Scholar]
- 34.Hamaguchi Y, Kaido T, Okumura S, et al. Proposal for new diagnostic criteria for low skeletal muscle mass based on computed tomography imaging in Asian adults. Nutrition. 2016 Nov-Dec;32(11-12):1200-5. [DOI] [PubMed] [Google Scholar]
- 35.Hong JT, James S, Tran A, et al. Sarcopenia measurements and clinical outcomes in Crohn's disease surgical patients. ANZ J Surg. 2022 Dec;92(12):3209-13. [DOI] [PubMed] [Google Scholar]
- 36.Kusunoki Y, Fukuoka T, Sugimoto A, et al. Impact of Changes in Psoas Muscle Index on Prognosis in Patients With Colorectal Liver Metastases. Cancer Diagn Progn. 2025 Jan-Feb;5(1):72-82. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 37.Fukuoka T, Maeda K, Nagahara H, et al. Change in PMI During Neoadjuvant Therapy Is a Predictive Prognostic Marker in Rectal Cancer. Anticancer Res. 2019 Sep;39(9):5157-63. [DOI] [PubMed] [Google Scholar]