Abstract
Crohn disease (CD) is a chronic inflammatory bowel disease and is associated with malnutrition. Sarcopenia is an indicator of poor nutrition status. This study evaluated the impact of preoperative and postoperative sarcopenia on postoperative outcomes including complications and recurrence. This single-center, retrospective study included patients who underwent abdominal surgery for CD between January 2006 and December 2016. This study analyzed the data using abdominal computed tomography (CT) images at the inferior endplate level of the third lumbar vertebra taken within 1 month before surgery. The skeletal muscle index (SMI) was calculated as total abdominal muscle area (TAMA)/height2 and sarcopenia was defined as an SMI of ≤49.0 cm2/m2 for men and ≤31.0 cm2/m2 for women using Korean-specific cutoff value. Of the 569 patients enrolled, 412 patients (72.4%) had preoperative sarcopenia (sarcopenia group, SG) and 157 patients (27.6%) were within the normal range (non-sarcopenia group, NSG). The SG had significantly younger age at diagnosis, a higher proportion of male patients, and a lower mean BMI compared with the NSG. On multivariable analysis, preoperative sarcopenia was an independent risk factor for postoperative complications (relative risk [RR] = 1.88, 95% confidence interval [CI]: 1.00–3.53; P = .049). Checking the change of postoperative sarcopenia using the follow-up CT, 240 patients (58.2%) of the SG still showed sarcopenia (post-SG) and 154 patients (37.4%) recovered from sarcopenia (post-NSG). The post-SG had significantly lower 5-year surgical recurrence-free survival, compared with the post-NSG (88.7% ± 2.1% vs 93.8% ± 1.5%, P = .019). More than 70% of patients with CD undergoing intestinal surgery had preoperative sarcopenia. Preoperative sarcopenia was an independent risk factor for postoperative complications, and persistent postoperative sarcopenia was associated with surgical recurrence. Sarcopenia assessment may be a useful tool for risk stratification in surgical CD patients.
Keywords: Crohn disease, postoperative complication, recurrence, sarcopenia, surgery
1. Introduction
Crohn disease (CD) is a chronic inflammatory disease affecting any site of the alimentary tract and is associated with malnutrition and lower body mass index (BMI).[1-3] Three-fourths of patients hospitalized due to CD are malnourished and one-third have a low BMI status[4] and the reasons of malnutrition in CD are associated with limited food intake, malabsorption, and treatment adverse events. Considering that up to 80% of patients with CD require abdominal surgery during their lifetime,[5] surgeons easily encounter these malnourished patients with CD and worry about the patient’s complications after surgery. When planning to perform intestinal surgery on malnourished patients, surgeons should identify and correct modifiable factors associated with postoperative complications, and one of the correctable factors is nutritional status.[6]
Recently, the relationships between body composition and clinical outcomes have been extensively studied in the field of cancer research.[7] Body composition parameters such as sarcopenia, visceral obesity, and muscle mass are now recognized as prognostic factors predicting toxicity and response to chemotherapy, and postoperative complications in cancer research.[7] A similar approach can be observed in the treatment of chronic diseases such as cancer and CD, where a combination of ongoing surgical interventions and medical treatments is necessary. In addition to medical intervention, correcting lifestyle habits and maintaining a healthy nutritional status are crucial for sustaining the effectiveness of the treatment. Therefore, muscle mass, which can predict nutritional status and the patient’s condition, can be considered a significant factor in CD. The patients with CD had alterations in their body composition (lean and fatty tissue) that a simple BMI assessment may fail to detect.[8-10] The altered composition in CD is associated with more severe phenotypes and may negatively impact the clinical course of the disease, response to biologics treatment, need for surgery, and quality of life.[4,11-13]
Sarcopenia is a progressive and generalized muscle disorder that is associated with increased likelihood of adverse outcomes and sarcopenia is affected by nutritional status,[14] immobility, and chronic catabolic diseases.[15] Patients with sarcopenia had significantly elevated costs of care during hospitalization regardless of whether they were young or old.[16] Additionally, sarcopenia has been linked to increased morbidity and mortality rates, particularly in elderly individuals.[17,18] Patients with CD who require surgical intervention are relatively young, but if sarcopenia is a complication-related factor, a longer hospital stay and an increase in medical costs are also expected regardless of age. Until now, sarcopenia is used mainly in research rather than in clinical practice. However, if sarcopenia is considered as one of the nutritional factors associated with postoperative complications in patients with CD, it could be identified as a modifiable factor in clinical practice. By managing sarcopenia, healthcare providers may potentially improve patient outcomes in terms of postoperative complications, recovery, and overall treatment success. However, the serial changes in sarcopenia after surgery and their association with CD recurrence remain insufficiently studied.
The aims of the current study were to assess the body composition of the patients with CD who underwent intestinal surgery and to investigate the association between the body composition and clinical outcomes including postoperative complications and recurrence.
2. Materials and methods
2.1. Patients and variables
This retrospective study evaluated all consecutive patients who underwent intestinal surgery for CD at the Asan Medical Center, Seoul, Korea between January 2006 and December 2016. Patients were included if they had undergone intestinal resection surgery, or strictureplasty to resolve CD pathology. Patients were excluded if they had undergone biopsy, stoma formation or closure surgery, and they were aged 16 years or younger at the time of surgery. A flow diagram of patient selection is presented (Fig. 1). The following variables were collected: demographics, preoperative CD characteristics using the Montreal classification, history of previous abdominal and perineal surgery, history of perineal disease, duration of CD, preoperative medication, preoperative nutritional state (BMI, albumin, hemoglobin, replacement of fluid or feeding, sarcopenia index), operative finding (operative approach [open or laparoscopy], emergency operation, indication for surgery, method of anastomosis [hand-sewn or stapled], types of anastomosis [end-to-end, end-to-side, side-to-side], operation time, detailed operation name, and diverting ostomy), postoperative outcomes (postoperative length of hospital stay, complications [overall, infectious, or intra-abdominal], recurrence-free survival [RFS; clinical and surgical]).
Figure 1.
Study progress flow chart. CT = computed tomography, SMI = skeletal muscle index.
Postoperative complications were defined as any complications occurring within 30 days of the index surgery and were assessed overall and further classified as infectious or intra-abdominal complications. Infectious complications included wound infection, abdominal abscess, anastomotic leak, enterocutaneous fistula, pneumonia, and urinary tract infection. Recurrence was classified into clinical and surgical recurrence. Clinical recurrence was defined as imaging or colonoscopic findings indicating worsening of CD inflammation, following the development of clinical symptoms. Surgical recurrence was defined as reoperation for CD.
The study protocol was approved by the institutional review board of the Asan Medical Center (registration no. 2020-0328), and the study was performed in accordance with the Declaration of Helsinki. The requirement for informed consent was waived due to the retrospective nature of the study.
2.2. Assessment of sarcopenia and nutritional state
The visceral fat area (VFA, cm2) and subcutaneous fat area (SFA, cm2) were demarcated using the adipose tissue thresholds on CT. Visceral obesity (VO) was defined as a VFA ≥ 100 cm2. The skeletal muscle index (SMI) was calculated as total abdominal muscle area (TAMA)/height2. Body composition on CT was evaluated with artificial intelligence software (AID-UTM, iAID inc, Seoul, Korea), a fully automatic deep learning system for both L3 selection and body composition assessment.[19] Then, 3 experienced operators checked the quality of the muscle segmentation in all images. Sarcopenia was defined by an SMI of ≤49.0 cm2/m2 for men and ≤31.0 cm2/m2 for women using Korean-specific cutoff value.[20] Korean-specific cutoffs were used due to ethnic differences in body size and skeletal muscle mass distribution, leading to population-specific cutoffs proposed by European Working Group on Sarcopenia in Older People and Asian Working Group for Sarcopenia.[14,21] The BMI was calculated as weight (kg)/height2 (m2). A BMI above 25 was considered obesity and a BMI below 18.5 was considered underweight.
Preoperative anemia was defined as a hemoglobin level of <12 g/dL for women and 14 g/dL for men according to World Health Organization criteria. Hypoalbuminemia was defined as the level of serum albumin <3.0 g/dL. Among the malnourished patients, those who received nutritional support for weight maintenance during preoperative hospitalization were categorized as receiving either oral support (administration of the marketed oral nutritional supplements) or parenteral support. Malnourished status was defined as a state requiring nutritional support before surgery and unintentional weight loss >10% of the usual body weight over a period of 6 to 12 months.
To examine the impact of sarcopenia on clinical outcomes, the patients were categorized into 2 groups based on the presence of sarcopenia: the sarcopenia group (SG) and the non-sarcopenic group (NSG). Additionally, in this study, changes in sarcopenia were calculated using follow-up CT performed between 6 and 18 months after intestinal resection surgery, and the effects of these changes on the outcomes of recurrences were investigated.
2.3. Statistical analysis
Discrete variables, including demographic and preoperative characteristics, operative methods, and operative details were analyzed using the χ2 test to compare the SG group with NSG group. Continuous variables including, age at surgery, hospital stay, disease duration, and follow-up duration, were compared using unpaired Student t test. The RFS rate was examined using the Kaplan–Meier method and compared using the log-rank test. Multivariable analyses using binary logistic regression were used to assess the risks of developing postoperative complication. Multicollinearity among the independent variables in the multivariable model was assessed using the variance inflation factor (VIF), with a VIF > 5 considered indicative of significant multicollinearity. Statistical significance was defined as P < .05, and all statistical analyses were performed using SPSS Statistics for Windows, version 21 (IBM Corp, Armonk).
3. Results
3.1. Baseline characteristics
A total of 569 patients were included, of whom 412 (72.4%) had preoperative sarcopenia. The SG was significantly younger at diagnosis (25.3 ± 9.3 vs 27.5 ± 10.4 years, P = .02), had a higher proportion of male patients (81.8% vs 38.2%, P = .001), and had a lower mean BMI (17.55 ± 2.52 vs 20.46 ± 3.32, P = .001) compared with the NSG. The SG also had a significantly higher prevalence of perianal disease history, hypoalbuminemia (75.2% vs 63.7%, P = .003), and anemia (90.8% vs 75.8%, P = .001), and required more preoperative nutritional support (7.5% vs 2.5%, P = .03). In the Montreal classification, only age category differed, with a higher A1 ratio in the SG (12.9% vs 8.3%, P = .03). There were no significant differences in age at operation, disease duration, follow-up duration, family history, smoking history, previous abdominal surgery, or preoperative transfusion between the 2 groups (Table 1).
Table 1.
Demographics of the sarcopenia group and the non-sarcopenia group.
| Variables | Sarcopenia | Non-sarcopenia | P |
|---|---|---|---|
| (n = 412) | (n = 157) | ||
| Age at operation, yr | 31.2 ± 9.4 | 32.6 ± 9.8 | .12 |
| Age at diagnosis, yr | 25.3 ± 9.3 | 27.5 ± 10.4 | .02 |
| Sex, female/male | 75 (18.2)/337 (81.8) | 97 (61.8)/60 (38.2) | .001 |
| Duration of disease, mo | 75.1 ± 62.6 | 66.8 ± 58.4 | .14 |
| Follow-up duration, mo | 88.8 ± 36.1 | 88.9 ± 34.0 | .97 |
| BMI at operation, kg/m2 | 17.55 ± 2.52 | 20.46 ± 3.32 | .001 |
| Classification of BMI | .001 | ||
| Underweighted | 272 (66.0) | 55 (35.0) | |
| Normal range | 137 (33.3) | 84 (53.5) | |
| Overweighted | 3 (0.7) | 18 (11.5) | |
| Family history of CD | .99 | ||
| Yes | 14 (3.4) | 5 (3.2) | |
| No | 398 (96.6) | 152 (96.8) | |
| History of smoking | .28 | ||
| None | 261 (63.3) | 107 (68.2) | |
| Ex-smoker | 104 (25.2) | 39 (24.8) | |
| Current smoker | 47 (11.4) | 11 (7.0) | |
| History of previous abdominal surgery | .8 | ||
| Yes | 130 (31.6) | 51 (32.5) | |
| No | 282 (68.4) | 106 (67.5) | |
| History of previous perianal surgery | .013 | ||
| Yes | 184 (44.8) | 51 (33.1) | |
| No | 227 (55.2) | 105 (66.9) | |
| History of perianal fistula | .001 | ||
| Yes | 232 (56.3) | 63 (40.1) | |
| No | 180 (43.7) | 94 (59.9) | |
| Montreal classification age, years | .03 | ||
| ≤16 (A1) | 53 (12.9) | 13 (8.3) | |
| >16, ≤40 (A2) | 329 (79.9) | 123 (78.3) | |
| >40 (A3) | 30 (7.3) | 21 (13.4) | |
| Montreal classification behavior | .84 | ||
| Non-stricturing, non-penetrating (B1) | 20 (4.9) | 6 (3.8) | |
| Stricturing (B2) | 145 (35.2) | 54 (34.4) | |
| Penetrating (B3) | 247 (60.0) | 97 (61.8) | |
| Montreal classification location | .19 | ||
| Ileum (L1) | 143 (34.7) | 65 (44.4) | |
| Colon (L2) | 35 (8.5) | 8 (5.1) | |
| Ileocolon (L3) | 234 (56.8) | 84 (53.5) | |
| Preoperative level of serum albumin | .003 | ||
| Hypoalbuminemia (<3.5 mg/dL) | 314 (76.2) | 100 (63.7) | |
| Normal range | 98 (23.8) | 57 (36.3) | |
| Preoperative level of hemoglobulin | .001 | ||
| Anemia (woman < 12 mg/dL, man < 14 mg/dL) | 374 (90.8) | 119 (75.8) | |
| Normal range | 38 (9.2) | 38 (13.4) | |
| Preoperative transfusion | .26 | ||
| Yes | 183 (44.4) | 61 (38.9) | |
| No | 229 (55.6) | 96 (61.1) | |
| Preoperative nutritional support | .03 | ||
| Yes | 31 (7.5) | 4 (2.5) | |
| No | 381 (92.5) | 153 (97.5) |
Results reported as mean ± SD or number (%) of patients.
Bold, P < .05.
BMI = body mass index, CD = Crohn disease, SD = standard deviation.
3.2. Operative characteristics
When analyzing the operation details, the rate of emergency operation was higher in the NSG than in the SG (14.6% vs 6.8%, P = .005). The indication for surgery was not significantly different between the 2 groups, except that the peritonitis was higher in the NSG than the SG (15.3% vs 8.0%, P = .012). More patients in the SG had stoma formation, compared with the NSG (18.7% vs 13.4%, P = .015). The SG had longer mean operation time (170.9 ± 64.9 vs 158.2 ± 61.3, P = .034). There were no significant differences in operative approach, type of anastomosis, and operative details between the SG and NSG (Table 2).
Table 2.
Operative details of the sarcopenia group and the non-sarcopenia group.
| Variables | Sarcopenia | Non-sarcopenia | P |
|---|---|---|---|
| (n = 412) | (n = 157) | ||
| Operative approach | .36 | ||
| Open | 352 (85.4) | 129 (82.2) | |
| Laparoscopy | 60 (14.6) | 28 (17.8) | |
| Emergency operation | 28 (6.8) | 23 (14.6) | .005 |
| Indication for surgery | |||
| Abscess at the time of surgery | 99 (24.0) | 34 (21.7) | .58 |
| Obstruction at the time of surgery | 130 (31.6) | 46 (29.3) | .69 |
| Fistula at the time of surgery | 125 (30.3) | 47 (29.9) | .99 |
| Peritonitis at the time of surgery | 33 (8.0) | 24 (15.3) | .012 |
| Others | 25 (6.1) | 6 (3.8) | .14 |
| Methods of anastomosis | .015 | ||
| Hand-sewn | 16 (3.9) | 0 (0) | |
| Stapled | 319 (77.4) | 136 (86.6) | |
| Stoma formation without anastomosis | 77 (18.7) | 21 (13.4) | |
| Types of anastomosis | .73 | ||
| End-to-end | 21 (6.3) | 6 (4.4) | |
| End-to-side | 30 (9.0) | 13 (9.6) | |
| Side-to-side | 284 (84.8) | 117 (68.0) | |
| Operation time, min | 170.9 ± 64.9 | 158.2 ± 61.3 | .034 |
| Operative details | .39 | ||
| Small bowel surgery (SBS) only | 101 (24.5) | 48 (30.6) | |
| ICR with or without SBS | 122 (29.6) | 52 (33.1) | |
| RHC with or without SBS | 102 (24.8) | 37 (23.6) | |
| TC with or without SBS | 41 (10.0) | 11 (7.0) | |
| TPC with or without SBS | 23 (5.6) | 6 (3.8) | |
| LHC, AR, or LAR with or without SBS | 13 (3.1) | 1 (0.6) | |
| APR or Hartmann procedure | 10 (2.5) | 2 (1.3) |
Results reported as number (%) of patients.
Bold, P < .05.
APR = abdominoperineal resection, AR = anterior resection, ICR = ileocecal resection, LAR = low anterior resection, LHC = left hemicolectomy, RHC = right hemicolectomy, SBS = small bowel surgery, TC = total colectomy, TPC = total proctocolectomy.
3.3. Postoperative outcomes
The SG tended to have longer postoperative length of hospital stay, compared with the NSG (14.8 ± 15.2 vs 12.2 ± 11.4, P = .05). In terms of postoperative complications, there were no significant differences in overall, infectious, intra-abdominal, and Clavien–Dindo classification grade ≥ III complications between the SG and NSG (Table 3). However, on multivariable analysis, preoperative sarcopenia emerged as an independent risk factor for overall complications (RR = 1.88, 95% CI: 1.00–3.53; P = .049), suggesting that the effect was masked by confounding baseline characteristics such as BMI, anemia, and hypoalbuminemia. The VIF values for all variables in the multivariable model ranged from 1.018 to 1.289, indicating no significant multicollinearity. Also, history of previous perianal surgery (RR = 2.607, 95% CI: 1.336–5.089; P = .005), history of perianal fistula (No; RR = 0.449, 95% CI: 0.228–0.885; P = .021), preoperative transfusion (yes; RR = 1.772, 95% CI: 1.039–2.739; P = .023), BMI (underweighted; RR = 1.711, 95% CI: 1.024–2.86; P = .004), and operative approach (laparoscopy; RR = 0.327, 95% CI: 0.153–0.699; P = .004) were risk factors for overall complications (Table 4). On RFS analyses, the 5-year clinical (SG, 43.7% ± 2.6% vs NSG, 44.5% ± 4.1%, P = .96) and 5-year surgical RFS (SG, 92.2% ± 1.4% vs NSG, 90.2% ± 2.5%, P = .98) were not significantly different between the SG and NSG (Fig. 2).
Table 3.
Operative outcomes of the sarcopenia group and the non-sarcopenia group.
| Variables | Sarcopenia | Non-sarcopenia | P |
|---|---|---|---|
| (n = 412) | (n = 157) | ||
| Postoperative length of hospital stay, d | 14.8 ± 15.2 | 12.2 ± 11.4 | .05 |
| Total postoperative complication, yes | 117 (28.4) | 40 (25.5) | .53 |
| Infectious complication, yes | 90 (21.8) | 29 (18.5) | .42 |
| Intra-abdominal complication, yes | 47 (11.4) | 17 (10.8) | .99 |
| Clavien–Dindo classification grade ≥ III complications | 54 (13.1) | 24 (15.3) | .5 |
| 5-yr clinical recurrence-free survival, % | 43.7 ± 2.6 | 44.5 ± 4.1 | .96 |
| 5-yr surgical recurrence-free survival, % | 92.2 ± 1.4 | 90.2 ± 2.5 | .98 |
Bold, P < .05.
Table 4.
Multivariable analysis for the overall postoperative complication.
| Variables | Univariable | Multivariable | 95% CI | P-value |
|---|---|---|---|---|
| P-value | Exp(B) | |||
| Sex | .014 | .051 | ||
| History of previous abdominal surgery | .91 | |||
| History of previous perianal surgery | .005 | |||
| No | 1 | |||
| Yes | 2.607 | 1.336–5.089 | ||
| History of perianal fistula | .3 | .021 | ||
| Yes | 1 | |||
| No | 0.449 | 0.228–0.885 | ||
| Montreal classification, age | .87 | .61 | ||
| Montreal classification, behavior | .007 | .2 | ||
| Montreal classification, location | .006 | .31 | ||
| Preoperative hypoalbuminemia | .75 | .22 | ||
| Preoperative anemia | .41 | .34 | ||
| Preoperative nutritional support | .13 | .09 | ||
| Preoperative blood transfusion | .001 | .023 | ||
| No | 1 | |||
| Yes | 1.772 | 1.039–2.739 | ||
| Preopearative sarcopenia* | .53 | .049 | ||
| Yes | 1 | |||
| No | 0.532 | 0.283–0.998 | ||
| BMI | .64 | .04 | ||
| Normal or overweighted | 1 | |||
| Underweighted | 1.711 | 1.024–2.86 | ||
| Smoking | .55 | .77 | ||
| Emergency operation | .14 | .29 | ||
| Operative approach | .001 | .004 | ||
| Open | 1 | |||
| Laparoscopy | 0.327 | 0.153–0.699 | ||
| Method of anastomosis | .034 | .061 | ||
| Types of anastomosis | .07 | .26 |
BMI = body mass index, CI = confidence interval.
Bold, P < .05.
In the text, the RR for sarcopenia was reported as the inverse value (1/0.532 = 1.88) for ease of interpretation.
Figure 2.
Clinical (A, C) and surgical (B, D) recurrence-free survivals in terms of the sarcopenia or the non-sarcopenia according to the pre- and postoperative period. RFS = recurrence-free survival.
3.4. Changes of sarcopenia and those effects on recurrence
Subgroup analysis was performed by dividing the changes in sarcopenia before and after surgery. Among the SG, 18 patients (4.4%) and among the NSG, 6 patients (3.8%) did not undergo follow-up CT, and therefore the change in sarcopenia status could not be confirmed. These patients were excluded from the subgroup analysis; however, given the small number, the impact on the overall results is considered to be minimal. Among the SG before surgery, 240 patients (58.2%) still showed sarcopenia (persistent-SG) and 154 patients (37.4%) recovered from sarcopenia (improved-SG) on postoperative follow-up CT. Of the NSG before surgery, 142 patients (90.4%) remained non-sarcopenic (persistent-NSG) and only 4 patients (5.7%) changed to sarcopenia (worsened-NSG) after bowel surgery (Fig. 3). On RFS analyses, the 5-year clinical RFS was not significantly different between the persistent-SG and persistent-NSG (persistent-SG, 39.3% ± 3.2% vs NSG, 46.7% ± 3.0%, P = .24), but the persistent-SG had significantly lower 5-year surgical RFS, compared with the persistent-NSG (88.7% ± 2.1% vs 93.8% ± 1.5%, P = .019; Fig. 3). When subgroup analysis was performed on the change in sarcopenia within each group, of the preoperative SG, the 5-year surgical RFS rate of the persistent-SG was significantly lower than that of the improved-NSG (89.1% ± 2.1% vs 96.6% ± 1.5%, P = .03), but the 5-year clinical RFS was not significantly different between the 2 postoperative groups (39.9% ± 3.2% vs 47.3% ± 4.2%, P = .53). On subgroup analysis, among the preoperative NSG, the 5-year clinical (22.2% ± 13.9% vs 45.2% ± 4.3%, P = .004) and surgical RFS (77.8% ± 13.9% vs 91.0% ± 2.5%, P = .038) in the worsened-NSG was significantly lower than in the persistent-NSG (Fig. 3).
Figure 3.
Clinical (A, C) and surgical (B, D) recurrence-free survivals in terms of the change of sarcopenia status according to the preoperative sarcopenia or non-sarcopenia. NSG = non-sarcopenia group, RFS = recurrence-free survival, SG = sarcopenia group.
4. Discussion
The current study showed the incidence of sarcopenia in patients with CD who received intestinal surgery was 72.4%. According to a recently published meta-analysis on sarcopenia and CD, the incidence of sarcopenia in CD patients was 52%,[22] and studies on inflammatory bowel disease including UC showed varying results from 11% to 32%.[4,23-26] Although direct comparison seems difficult due to the heterogeneity in the definition of sarcopenia and ethnicity, the incidence in the current study seems to be quite high. The high incidence of sarcopenia in patients with CD is attributed to the prolonged duration of CD requiring surgery or the severe nature of the disease. While the evidence regarding sarcopenia as an exacerbating factor for CD remains unclear, it shows promise as an indicator of advanced CD. The current study showed that the SG had more history of perianal fistula or perianal surgery, indicating uncontrolled CD activity. Perianal diseases such as fistula, abscess, and fissure are not only one of the major manifestations of CD but also represent 1 factor that influences the severity of CD, as reflected in the CDAI (Crohn Disease Activity Index) score. The incidence of perianal inflammation in patients with CD ranges from 25% to 80%.[27] While the causal relationship between this uncontrolled activity and sarcopenia remains unclear, there could be a potential association.
In this study, significant hypoalbuminemia and anemia were observed in the SG. Nutritional status, which is related to the immune system and inflammation, is considered a predictor of sarcopenia. Considering these factors, it is thought that nutritional status could influence the progression of CD. As a method of evaluating nutritional status, serum albumin, and hemoglobin levels in addition to muscle volume can be measured. The synthesis of albumin and hemoglobin involves various hormones and pathways. However, inflammation can disrupt this process, and it is closely linked to the development of CD. It is believed that the distinction between the 2 groups was attributed to the inhibitory effect of interleukin-6, which is associated with active CD, on albumin synthesis or its impact on degradation.[28] Although hemoglobin is not an inflammatory marker and considering that it is known that anemia can occur when chronic inflammation persists, it is possible to explain that anemia was more common in the SG in this study as a secondary effect of inflammation.[29]
Sarcopenia and malnutrition in CD had a multifactorial etiology. Insufficient energy intake, malabsorption, enteric nutrient loss, and drug-related effects collectively influence each other to cause sarcopenia. Reduction of the general condition due to these various causes eventually led to a decrease in the patient’s performance and mobilization and led to atrophy of the muscle as well as a decrease in muscle development. In addition, there were reports that sarcopenia was associated with the severity of IBD,[30] and there were results that it helped to make treatment decisions in IBD patients.[31] The decision on the timing of operation is an important factor in the operation of CD patients. The current study showed that emergency surgery was performed more frequently in the NSG due to peritonitis. Because the general condition was relatively good in the NSG, medical treatment was continued, and it is thought that emergency surgery was performed for peritonitis due to treatment failure of the medical treatment. In the SG, where the activity of CD was relatively poorly controlled, it can be assumed that bowel inflammation and bowel edema were more severe than in the NSG, and therefore the operation time and stoma formation rate were higher than those of the NSG.
In the current study, preoperative sarcopenia was found to be an influencing factor on the overall postoperative outcome. In general, it was expected that the nutritional status and the general condition of the SG was poor. Like the current study, Zhang et al compared the postoperative outcomes with and without sarcopenia in the patients with CD and reported that the presence of sarcopenia undergoing bowel resection was a factor that increased postoperative complications.[32] The use of the SMI index together for sarcopenia with evaluation of nutritional status might be a cornerstone of the treatment process.[32] Kubo et al reported that there were no differences in postoperative outcomes such as hospital day, incidence of Clavien–Dindo grade ≥ 2 complications, and in-hospital mortality among sarcopenia patients with panperitonitis.[33] The current study also showed that there was no significant difference in hospital stay and postoperative complication between the SG and NSG groups and such results may be explained by the fact that the patient’s condition was already worse than that of general patients.
In many recent studies, sarcopenia is recognized as a poor prognostic factor in patients with various types of cancer, such as pancreas, gastrointestinal tract, ovary.[34-36] From the point of view of a disease that requires chronic and continuous treatment, it is thought that the persistence of sarcopenia in CD as well as cancer was associated with poor prognosis. When the presence or absence of sarcopenia was analyzed 6 to 18 months after surgery, there was a difference only in 5-year surgical RFS, and it is thought that recovery of the patient’s nutritional status after surgery could be used as 1 predictor of disease control. In addition, subgroup analysis was performed according to the presence or absence of sarcopenia before surgery and recovery after surgery. Regardless of the preoperative sarcopenia status, persistent sarcopenia at 6 to 18 months after surgery was associated with a higher rate of surgical recurrence, suggesting that postoperative sarcopenia assessment may serve as an indicator for considering escalation of medical treatment in CD. Persistent sarcopenia is one of several host factors in patients with CD. Rather than being a direct contributor to disease recurrence, persistent postoperative sarcopenia likely represents a surrogate marker of unresolved systemic inflammation and suboptimal nutritional rehabilitation following surgery. From this perspective, failure to recover skeletal muscle mass may serve as a clinical indicator of inadequately controlled disease activity, which may necessitate escalation of therapeutic strategies.
The findings of this study suggest that sarcopenia assessment before surgery may be useful for identifying high-risk patients with CD. Preoperative nutritional optimization in sarcopenic patients could be considered to reduce postoperative complications. Additionally, as persistent postoperative sarcopenia was associated with surgical recurrence, sarcopenia status on routine follow-up imaging may provide additional prognostic information for guiding treatment strategies.
The current study has several limitations. First, as a retrospective study, selection bias may occur; however, this was minimized by including all consecutive patients who underwent intestinal surgery for CD during the study period without artificial exclusion. Second, the study was conducted at a single medical center, which may limit the generalizability of the results. However, we believe that the bias would have been reduced because the surgeries were performed by IBD-specialized surgeons with consistent management protocols. Third, sarcopenia was assessed solely based on CT-derived skeletal muscle index, without incorporating functional assessments such as grip strength or gait speed, which may limit the comprehensive evaluation of sarcopenia. Fourth, the long study period (2006–2016) may encompass changes in medical treatment strategies for CD, which could have influenced clinical outcomes. Fifth, the heterogeneous timing of postoperative follow-up CT (6–18 months) could not be further stratified for sensitivity analysis, which may introduce measurement bias in the assessment of postoperative sarcopenia status. The relatively wide range in the timing of follow-up APCT was mainly because routine surveillance APCT was generally scheduled at around 12 months, but it was performed earlier when patients developed symptoms; additionally, in our tertiary referral center, some 12-month follow-up examinations were delayed due to scheduling and waiting times for imaging. Sixth, although our analysis focused on identifying independent risk factors using relative risks, the absence of absolute risk reporting may limit the direct assessment of the actual clinical burden in specific patient subgroups.
5. Conclusions
More than 70% of patients with CD undergoing intestinal surgery had preoperative sarcopenia. Preoperative sarcopenia was an independent risk factor for postoperative complications, and persistent postoperative sarcopenia was associated with surgical recurrence. Sarcopenia assessment may be a useful tool for risk stratification in surgical CD patients.
Author contributions
Conceptualization: Gun-Hee Yi, Chan Wook Kim, Yong Sik Yoon, In Ja Park, Seok-Byung Lim, Chang Sik Yu, Jong Lyul Lee.
Data curation: Gun-Hee Yi, Seok-Byung Lim, Jong Lyul Lee.
Formal analysis: Jong Lyul Lee.
Investigation: Gun-Hee Yi, Kyung Won Kim, Chan Wook Kim, Yong Sik Yoon, In Ja Park, Seok-Byung Lim, Chang Sik Yu, Jong Lyul Lee.
Resources: Chan Wook Kim, Yong Sik Yoon, In Ja Park, Seok-Byung Lim.
Writing – original draft: Gun-Hee Yi.
Writing – review & editing: Jong Lyul Lee.
Abbreviations:
- BMI
- body mass index
- CD
- Crohn disease
- CI
- confidence interval
- CT
- computed tomography
- NSG
- non-sarcopenia group
- RFS
- recurrence-free survival
- RR
- relative risk
- SFA
- subcutaneous fat area
- SG
- sarcopenia group
- SMI
- skeletal muscle index
- TAMA
- total abdominal muscle area
- VFA
- visceral fat area
- VIF
- variance inflation factor
- VO
- visceral obesity.
The authors have no funding and conflicts of interest to disclose.
The datasets generated during and/or analyzed during the current study are available from the corresponding author on reasonable request.
How to cite this article: Yi G-H, Lee JL, Kim KW, Kim CW, Yoon YS, Park IJ, Lim S-B, Yu CS. Impact of sarcopenia on postoperative outcomes and recurrence in patients with Crohn disease: A retrospective cohort study. Medicine 2026;105:21(e48930).
Contributor Information
Gun-Hee Yi, Email: lizamong@naver.com.
Kyung Won Kim, Email: crscwkim@amc.seoul.kr.
Chan Wook Kim, Email: crscwkim@amc.seoul.kr.
Yong Sik Yoon, Email: yoonys@amc.seoul.kr.
In Ja Park, Email: ipark@amc.seoul.kr.
Seok-Byung Lim, Email: sblim@amc.seoul.kr.
Chang Sik Yu, Email: csyu@amc.seoul.kr.
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