Prevalence and outcome of sarcopenia in patients with inflammatory bowel disease: a follow-up study

Vikram Dharap; Devendra Desai; Philip Abraham; Tarun Gupta; Pavan Dhoble; Nirad Mehta; Jagdish Modhe

doi:10.5217/ir.2024.00096

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Original Article Prevalence and outcome of sarcopenia in patients with inflammatory bowel disease: a follow-up study: Vikram Dharap¹, Devendra Desai¹, Philip Abraham^1,, Tarun Gupta¹, Pavan Dhoble¹, Nirad Mehta², Jagdish Modhe²; DOI: https://doi.org/10.5217/ir.2024.00096
Published online: January 23, 2025

¹Division of Gastroenterology, P. D. Hinduja Hospital and Medical Research Centre, Mumbai, India

²Department of Radiology, P. D. Hinduja Hospital and Medical Research Centre, Mumbai, India

Correspondence to Philip Abraham, Division of Gastroenterology, P. D. Hinduja Hospital and Medical Research Centre, Mahim, Mumbai 400016, India. E-mail: dr_pabraham@hindujahospital.com

• Received: June 24, 2024 • Revised: October 15, 2024 • Accepted: October 19, 2024

This is an Open Access article distributed under the terms of the Creative Commons Attribution Non-Commercial License (http://creativecommons.org/licenses/by-nc/4.0/) which permits unrestricted non-commercial use, distribution, and reproduction in any medium, provided the original work is properly cited.

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Abstract
INTRODUCTION
METHODS
RESULTS
DISCUSSION
NOTES
REFERENCES

Abstract

Background/Aims
Sarcopenia is implicated in inflammatory bowel disease (IBD) complications and surgical outcomes. This study aimed to investigate the prevalence and follow-up of sarcopenia in patients with IBD.
Methods
Consecutive consenting patients with IBD aged > 18 years were included. Patients with associated sarcopenic diseases were excluded. All had measurements of anthropometry, body mass index (BMI), mid-arm muscle circumference, muscle strength, physical performance, and muscle mass (on computed tomography scan). They were followed up for up to 12 months, and incidence of flares, fractures, and surgery was noted.
Results
Of 157 patients screened, 35 refused participation; 5 with associated sarcopenic diseases were excluded. Of 117 patients (median age, 41 years; interquartile range, 18–81 years; 65 men), 73 had ulcerative colitis, 42 Crohn’s disease, and 2 IBD-unclassified. Forty (34.2%) had probable sarcopenia; 47 (40.2%) had sarcopenia (29 ulcerative colitis and 18 Crohn’s disease) including 10 (8.5%) with severe sarcopenia. Ten (21.3%) were in disease remission. Of factors associated with sarcopenia in univariate analysis, only BMI was significant in multivariate analysis. Ninety-nine patients followed up for a median of 7 months (interquartile range, 2–12 months). Freedom from flares was 5.3% in patients with sarcopenia and 46.1% in those without (P= 0.004). Three patients (1 with sarcopenia, 2 without) required surgery.
Conclusions
Sarcopenia was present in 40% of patients with IBD; one-fifth of these had severe sarcopenia. One-fifth were in remission. Low BMI correlated with sarcopenia. More patients with sarcopenia had disease flare. Screening for sarcopenia should be considered in patients with IBD.
Keywords: Crohn disease; Malnutrition; Nutrition; Prognosis; Ulcerative colitis

INTRODUCTION

Sarcopenia is defined as a progressive and generalized skeletal muscle disorder with significant reduction in skeletal muscle mass associated with low muscle strength and low physical performance [1]. Patients with inflammatory bowel disease (IBD) often have malnutrition and sarcopenia. About two-thirds have lower skeletal muscle mass when compared to healthy controls [2]. In one study, 28% of patients with IBD had sarcopenia versus only 1% of a healthy population [3].

Sarcopenia is associated with high morbidity and mortality in patients with IBD [4]. It is associated with bone demineralization and pathological fractures, with a higher probability of hospitalization and reduction in mobility [5]. Sarcopenia has been used as a predictive marker for surgical intervention and is a predictive factor of surgical outcomes, increasing the rate of postoperative complications, in patients with Crohn’s disease (CD) [4,6]. It is important to detect sarcopenia at early stages of the disease; corrective measures such as nutrition supplementation and exercise have been shown to improve sarcopenia [7,8].

There is paucity of data on sarcopenia in patients with IBD in India. One retrospective study included only patients with CD and showed prevalence of sarcopenia to be 43% [9]. Another study, a prospective one, included only patients with ulcerative colitis (UC) [10]. The current study was a prospective follow-up study including both UC and CD to evaluate the prevalence and outcome of sarcopenia and the factors associated with it.

METHODS

We conducted this study in compliance with the principles of the Declaration of Helsinki. The study protocol was reviewed and approved by the Institutional Review Board of P. D. Hinduja Hospital (Project No. 1445-21-PA). Written informed consent was obtained from all participants. The study was conducted in the Division of Gastroenterology between June 1, 2021, and November 30, 2022. All patients aged > 18 years, of either sex, with IBD–UC, CD, or IBD-unclassified (IBD-U), diagnosed as per the Copenhagen criteria [11,12]–seen during this period were eligible for enrolment in this prospective follow-up study. Patients with history of associated malignancy, pregnant patients, and those with systemic diseases such as congestive heart failure, chronic kidney disease, chronic obstructive pulmonary disease, chronic liver disease, malignancy, and any other condition that in the opinion of the treating physician could contribute to sarcopenia, were excluded.

1. Methods

At the first study visit, details of demographic data; history; physical examination; investigations; disease location, extent, activity and behavior; extraintestinal manifestations; and treatment received were entered in a worksheet. Disease activity was defined using the partial Mayo score for UC [13] and Harvey-Bradshaw index for CD [14]. Disease activity was also scored [13,15]. Disease location, extent and behavior were classified as per the Montreal classification for UC and CD [16].

2. Evaluation of Sarcopenia

Patients’ weight and height were noted and body mass index (BMI) was calculated. The methods used to evaluate sarcopenia were as follows: (1) muscle strength was evaluated by handheld dynamometer to assess handgrip strength; (2) muscle mass was measured on computed tomography (CT) scan at L3 level as skeletal muscle area (SMA) [1], including as skeletal muscle area (SMA), including cross-sectional areas of muscles (psoas, erector spinae, quadratus lumborum, transversus abdominis, external and internal obliques, and rectus abdominis) (Figs. 1 and 2). SMA was quantified using tissue-specific Hounsfield unit thresholds of –29 to +150. The image analysis software packages used for calculating this was Synapse 3D (Fuji Corp., Tokyo, Japan). SMA was then normalized for stature by dividing by height squared (cm²/m²) to obtain skeletal muscle index (SMI); (3) physical performance was assessed by asking the patient to walk a distance of 4 m and the time taken was measured to calculate gait speed (m/sec).

The revised operational definition of sarcopenia according to the European Working Group on Sarcopenia in Older People (EWGSOP2) [1] is as follows: (1) probable sarcopenia is diagnosed when only low muscle strength is detected; (2) sarcopenia is diagnosed when the diagnosis is confirmed by the presence of low muscle quantity (muscle mass); or (3) severe sarcopenia is diagnosed when low muscle strength, low muscle quantity, and low physical performance are all detected.

The parameters used to define sarcopenia are mentioned in Table 1. The normative values and cutoff values for diagnostic parameters, including muscle strength, SMI, and gait speed, were taken from a study done on an Indian population [17]. Patients were then grouped into the EWGSOP2 categories for sarcopenia [1].

3. Follow-up

Patients were followed up for up to 12 months to note number of flares, incidence of fractures, and need for surgery.

4. Sample Size Calculation

The sample size of 117 patients was calculated considering an earlier study by Ryan et al. [4] that showed prevalence of sarcopenia in IBD patients to be 41%, at 95% confidence level and margin of error 9%.

5. Statistical Analysis

Statistical analysis was done using SPSS version 23.0 (IBM Corp., Armonk, NY, USA). Continuous variables are described as mean (standard deviation; compared using Student t-test for unpaired data) or median (interquartile range [IQR]). Categorical variables are described as percentage and compared using the chi-square test or Fischer exact test. Multivariate analysis was done using binary logistic regression on variables that were significant on univariate analysis. Freedom from flares was analyzed using Kaplan-Meier analysis. Difference between the 2 groups was calculated using log-rank test for significance. P-value of < 0.05 was considered significant.

RESULTS

Of 157 consecutive patients screened, 35 patients refused participation and 5 patients were excluded due to associated disease that could contribute to sarcopenia (2 had human immunodeficiency virus infection, and 1 each had chronic pancreatitis, rheumatoid arthritis and carcinoma buccal mucosa). Of 117 patients enrolled, 73 had UC, 42 CD, and 2 IBD-U. Median age at recruitment was 41 years (IQR, 18–81 years) and 65 (55.5%) were men. Mean BMI was 23.6 ± 4.9 kg/m². Sixty-seven patients (57.3%) had active disease (partial Mayo score > 2 for UC and Harvey-Bradshaw index > 5 for CD, and/or fecal calprotectin > 250 mg/g). Twenty-three patients (19.7%) were on steroid therapy, 18 (15.4%) were on biologic therapy, and 11 (9.5%) had history of undergoing IBD-related surgery in the past–4 had small bowel stricture resection and anastomosis, 3 had ileocolonic resection, 2 had fistulectomy, and 1 each had sigmoid colectomy and diversion ileostomy, and total proctocolectomy with ileal-pouch anal anastomosis. The disease profile is shown in Table 2.

1. Prevalence of Sarcopenia

According to the EWGSOP2 definition, 40 patients (34.2%) had probable sarcopenia and 47 (40.2%) had sarcopenia; of the latter, 10 (8.5% of total) had severe sarcopenia.

2. Factors Affecting Sarcopenia

The factors taken into consideration were age; sex; weight; BMI; disease subtype (CD, UC, or IBD-U), duration, extent and activity; and prior therapy.

The mean age of patients with and without sarcopenia was comparable. About one-third (32.3%) of male patients, and 50% of female patients, had sarcopenia (P= 0.052). Body weight was lower in patients with sarcopenia (P< 0.001) than in those without. The difference in BMI between those with and without sarcopenia was also significant (P< 0.001). Hemoglobin level was lower in patients with sarcopenia (P= 0.030).

Patients with CD (42.9%) had a similar prevalence of sarcopenia as those with UC (39.7%); 55% of patients with active disease versus 20% of those in remission had sarcopenia (P< 0.001). Duration, location and extent of disease were similar in those with and without sarcopenia. Twenty-three of 117 patients were on steroid, of whom 12 (52.1%) had sarcopenia. Nine of 37 (24.2%) with active disease amongst patients with sarcopenia were on steroids, but whether it was steroid use or disease activity that contributed to sarcopenia in them could not be determined. History of use of biologics was significantly more frequent in those with sarcopenia (P= 0.049).

Univariate analysis showed low weight, low BMI, low hemoglobin level, disease activity, and use of biologics to be associated with sarcopenia (P< 0.05) (Table 3). On multivariate analysis, only low BMI was associated with sarcopenia (odds ratio, 0.722; P< 001) (Table 4); for every 1 unit rise in BMI there was 27.8% chance of the patient not having sarcopenia.

3. Follow-up

Of 117 patients, 18 did not follow-up. The median duration of follow-up among 99 patients was 7 months (IQR, 2–12 months). Six patients each had clinical and biochemical flares whereas 13 patients had both clinical and biochemical flares; endoscopy was not routinely done during flare. Freedom from flares during follow-up was 5.3% in patients with sarcopenia and 46.1% in those without (P= 0.004) (Fig. 3).

Of 50 patients who were in clinical remission at inclusion, 10 had sarcopenia. Four of these 10 (40%) had flares on follow-up (2 each had clinical flare and a combination of clinical and biochemical flare) while only 10 of 40 (25%) without sarcopenia at inclusion (P< 0.02) had flares on follow-up (7 had both clinical and biochemical flare, 2 had only clinical flare, and 1 had only biochemical flare).

No patient had fracture. Three (1 with sarcopenia, 2 without) patients required surgery. The patient with sarcopenia underwent fistulectomy. One patient without sarcopenia who underwent colectomy for recurrent bleeding continued to have intermittent bleeding; the other patient is well after resection surgery for jejunal stricture.

DISCUSSION

Our study is probably the first prospective study from India to evaluate sarcopenia in patients with IBD, including both UC and CD, with follow-up for up to one year. We showed 40% prevalence of sarcopenia (similar in CD and UC), with 8.5% having severe sarcopenia. On multivariate analysis, only low BMI was associated with sarcopenia. On follow-up, only 5.3% of those with sarcopenia had freedom from flares compared to 46.1% of those without.

In a retrospective study from India in patients with CD, sarcopenia was present in 43%, being more in females but independent of age and disease severity, behavior and location [9]. A recent cross-sectional study from India showed sarcopenia to be present in 21.9% of patients with UC; multivariate analysis showed a significant correlation between disease activity and lower BMI [10].

Since the initial recognition of the concept of sarcopenia in 1989 by Rosenberg, modified later with primary description being age-related sarcopenia [18,19], several groups have tried formulating consensus definitions and diagnostic criteria for sarcopenia. Cutoff values vary depending on ethnicity and the patient population being studied (Table 5). Zhang et al. [20], for example, used SMI cutoff of 55 cm²/m² for males and 39 cm²/m² for females. Lee et al. [27] used SMI cutoff of 49 cm²/m² for males and 31 cm²/m² for females. Western studies suggested SMI cutoff level of 52.4 cm²/m² for males and 38.5 cm²/m² for women [22]. The mean muscle mass in Asians is approximately 15% lower than that in Westerners even after adjustment for height [31,32]. The normative values for SMI and handheld dynamometry that we used are based on studies done in a normal Asian population and cutoffs of SMI were derived using L3 level CT scan [17]. We used L3 level CT scan, which is currently considered to be the gold standard to measure SMA [1]; the radiation dose is minimal (0.1–0.2 mSv compared to 10 mSv in a whole-abdomen CT scan) as it involved only a single 5-mm slice [33].

In general, it appears that sarcopenia is more prevalent in Asian countries compared to the West, which could be due to lower BMI. Zhang et al. [6] reported the prevalence of sarcopenia as 33.8% and it correlated with disease activity. Forty-two percent of patients in a study from Japan had sarcopenia, which is comparable with our study; more patients with CD and sarcopenia in that study underwent intestinal resection [23]. In an Italian study, sarcopenia was found in 28% of patients with IBD compared with 1% of healthy controls and 36% of healthy elderly; it was associated with fatigue as well as reduction in quality of life [3].

Factors implicated in sarcopenia include sex, age, weight and BMI, all of which are associated with skeletal muscle volume [2]. With age there is an overall decline in size and number of skeletal muscle fibers, mainly the type 2 or fast-twitch muscle fibers, and infiltration of fibrous and adipose tissue into the skeletal muscle [34]. There is progressive muscle loss that cannot be controlled, with annual rate of decline of 1%–2% from as early as age 50 years, and muscle strength decline of 1.5% per year between ages 50 and 60, increasing to 3% annually thereafter [35]. Several studies suggest differential sex-specific rates of muscle loss, greater in men than in women [36].

Patients with higher BMI may also have sarcopenia (sarcopenic obesity). Despite the high levels of BMI, obese patients with CD are actually sarcopenic because of chronic inflammation and could benefit from nutritional intervention. An increased prevalence of obesity has been reported in patients with CD [37]; none of our patients fitted this description. Sarcopenic obesity has been identified as a negative predictor of survival in cancer patients, cirrhosis, and other cardio-metabolic diseases [38,39]. Adipose tissue could play a role in the inflammation related to IBD by release of adipokines, adipocyte stress response, and macrophage stimulation [40]. Obese patients with CD could have worse perianal disease, require more hospitalizations, and have poorer surgical outcomes as compared to matched non-obese patients with CD [41].

Malnutrition has been reported in 65%–75% of patients with CD and in 18%–62% of patients with UC [3]. Macronutrient intake is usually preserved, but micronutrient deficiency can occur more frequently. Anemia is known to decrease physical performance and strength and increase disability, and is associated with increased mortality [42]. Iron deficiency is the most frequent cause of anemia in patients with IBD, as in healthy people, with prevalence estimated at up to 70% of pediatric patients and up to 50% of adult patients [43]. The association of hemoglobin levels was found to be stronger for muscle function than for muscle mass and in men than in women; older adults with anemia had a higher risk of sarcopenia and muscle weakness [44].

The persistent low-grade inflammatory status in IBD, as seen by increased circulating levels of pro-inflammatory cytokines, such as tumor necrosis factor-α, interleukin-6, and myostatin (“inflamm-aging”), is important [45]. This can be considered as the starting point for the development of muscle loss by activating multiple pathways in common with sarcopenia [5]. Tumor necrosis factor-α is considered the key driver of intestinal damage, by stimulating macrophages to produce pro-inflammatory cytokines, inducing apoptosis of intestinal epithelial cells and stimulating the synthesis of proteases [46].

Other factors that have been described in sarcopenia included more frequent alcohol consumption, IBD-related complications, higher C-reactive protein and erythrocyte sedimentation rate, and higher Mayo score [10].

There is growing evidence to show that sarcopenia has a detrimental effect on patients’ physiological reserve and their ability to recover postoperatively [47]. Recent studies show that IBD is associated with increased risk of sarcopenia, which negatively impacts the quality of life, clinical course, response to therapy, and surgical outcomes [48]. The latter includes increased postoperative complications, higher rates of blood transfusion, ICU admission, postoperative sepsis, and venous thrombosis [20,24]. A recent Indian study showed that sarcopenia and visceral fat independently predict poor outcomes in CD [9]. In our study, more patients with sarcopenia had disease flares on follow-up. A meta-analysis showed depleted skeletal muscle mass radiologically in 27% to 61% of patients with IBD, a majority being those with CD; these patients were more likely to be men and have lower median BMI and SMI than patients with normal body mass composition [4]. The study found a direct correlation between sarcopenia and perioperative mortality in a wide variety of surgical conditions.

Our study has a few limitations: it was conducted at a single institution and our findings may not be applicable to a wider population although our study cohort was from a cosmopolitan city with diverse populations. The number in each group was small; a larger study group will help to corroborate the data. Finally, we had no follow-up data on the progression or regression of sarcopenia.

In summary, this is the first prospective Indian study on the prevalence of sarcopenia and its follow-up in patients with IBD (UC and CD). The population studied was from the cosmopolitan city of Mumbai, which has residents from all over India. Our study showed prevalence of sarcopenia to be 40%, with 8.5% having severe sarcopenia. On multivariate analysis, only low BMI was associated with sarcopenia. On follow-up for up to 1 year, patients with sarcopenia had a significantly higher number of disease flares than those without, with only 5.3% of patients with sarcopenia being free from flares. Our prevalence rate is in accordance with those reported from Asia and higher than in Western studies. We recommend screening for sarcopenia (maybe using a simple handgrip strength) in all patients with IBD, and confirmation in detected patients with L3 level CT scan to fulfill the criteria for sarcopenia, as early detection and targeted management may improve the outcome of this disease.

NOTES

Funding Source

This work was supported by National Health & Education Society (Project No. 1445-21-PA).

Conflict of Interest

No potential conflict of interest relevant to this article was reported.

Data Availability Statement

The de-identified participant data is available in our hospital records and will be shared on reasonable request to the corresponding author.

Author Contributions

Conceptualization: Dharap V, Desai D, Abraham P, Gupta T, Dhoble P. Data curation: all authors. Formal analysis: Dharap V, Desai D, Abraham P. Funding acquisition: Desai D, Modhe J. Investigation: Dharap V. Methodology: Dharap V, Desai D, Abraham P, Gupta T. Project administration: Dharap V, Desai D, Abraham P. Resources: Dharap V, Desai D. Software: Dharap V, Mehta N, Modhe J. Supervision: Dharap V, Desai D, Abraham P, Gupta T, Dhoble P. Validation: Desai D, Abraham P, Mehta N. Visualization: Desai D, Abraham P. Writing - original draft: Dharap V. Writing - review & editing: Dharap V, Desai D, Abraham P, Gupta T, Dhoble P. Approval of final manuscript: all authors.

Additional Contributions

We acknowledge Dr. Dipin Singh (P.D. Hinduja Hospital and Medical Research Centre, Mumbai, India) for his help in patient recruitment.

Fig. 1.

L3 level computed tomography scan with calculated normal- range skeletal muscle area (outlined in green).

Fig. 2.

L3 level computed tomography scan with calculated lowrange skeletal muscle area (outlined in green).

Fig. 3.

Kaplan-Meier analysis of freedom from flare.

Table 1.

Criteria for Defining Sarcopenia

Diagnostic parameter	Cutoff for defining sarcopenia
Muscle strength (hand and forearm muscles)	Male < 27 kg, female < 16 kg
Muscle mass	Male < 42 cm²/m², female < 38 cm²/m²
Physical performance	< 0.8 m/sec

Table 2.

Disease Profile in Enrolled Patients

Variable	Value (n = 117)
Disease duration (yr)
Crohn’s disease	3.5 (1.0–6.3)
Ulcerative colitis	4 (2-10)
IBD-U	5.5
Disease location, behavior, and extent^a
Crohn’s disease (n = 42)
L1	10 (22.7)
L2	8 (19.0)
L3	15 (32.7)
L1+ L4	9 (21.4)
B1	26 (61.9)
B2	13 (30.9)
B3	3 (7.14)
Perianal disease	8 (19.0)
Ulcerative colitis (n = 73)
E1	2 (2.7)
E2	31 (42.4)
E3	40 (54.7)
IBD-U (n = 2)	2 (1.7)

Values are presented as median (interquartile range) or number (%).

^a Location: L1, ileal disease; L2, colonic disease; L3, ileo-colonic involvement of disease; L4, upper gastrointestinal tract involvement. Behavior: B1, non-stricturing and non-penetrating disease; B2, stricturing disease; B3, penetrating disease. Extent: E1, involvement limited to rectum or rectosigmoid junction; E2, involvement limited to proportion of colorectum distal to splenic flexure; E3, involvement extending proximal to splenic flexure.

IBD-U, inflammatory bowel disease unclassified.

Table 3.

Univariate Analysis of Factors Affecting Sarcopenia

Descriptive data	Subgroup	Sarcopenia (n = 47)	No sarcopenia (n = 70)	P-value
Age (yr)		40.2 ± 14.9	43.9 ± 15.6	0.202
Sex	Male	21 (44.7)	44 (62.9)	0.052
	Female	26 (55.3)	26 (37.1)
Weight (kg)		55.6 ± 15.4	66.1 ± 13.8	< 0.001
Height (m)		1.6 ± 0.1	1.6 ± 0.1	0.233
BMI (kg/m²)		20.7 ± 4.3	25.5 ± 4.3	< 0.001
IBD type	CD	18 (38.3)	24 (34.3)	0.478
	UC	29 (61.7)	44 (62.9)
	IBD-U	0	2 (2.9)
Disease activity	Active	37 (78.7)	30 (42.9)	< 0.001
	Remission	10 (21.3)	40 (57.1)
Disease extent	CD	18	24	0.135
	L1	2 (11.1)	8 (33.3)
	L2	2 (11.1)	6 (25.0)
	L3	9 (50.0)	6 (25.0)
	L1+L4	5 (27.8)	4 (16.7)
	UC	29	44	0.365
	E1	0	2 (4.5)
	E2	11 (37.9)	20 (45.5)
	E3	18 (62.1)	22 (50.0)
Duration of disease (yr)		3 (1–9)	4 (2–10)	0.420
Hemoglobin (g/dL)		11.4 ± 1.7	12.2 ± 2.0	0.033
WBC (/cm³)		7,957 ± 3,262	7,461 ± 3,044	0.420
Platelets (/cm³)		3.4 ± 1.2	3.0 ± 1.0	0.065
Steroids		12 (25.5)	11 (15.7)	0.237
Biologics		11 (23.4)	7 (10.0)	0.049
Surgery		4 (8.5)	7 (10.1)	1.000

Values are presented as mean±SD, number (%), or median (interquartile range).

BMI, body mass index; IBD, inflammatory bowel disease; CD, Crohn’s disease; UC, ulcerative colitis; IBD-U, IBD-unclassified; WBC, white blood cell; SD, standard deviation.

Table 4.

Multivariate Analysis of Factors Affecting Sarcopenia

Variable	P-value	Odds ratio
Body mass index	0.001	0.722
Hemoglobin	0.485	0.914
Disease activity	0.073	0.409
Biologics	0.343	0.550

Table 5.

Cutoff Levels of SMI Used for Defining Sarcopenia in IBD and Its Prevalence in Various Studies

Author (year)	Country	Type of study	SMI (cm²/m²) or ASMI (kg/m²)		Prevalence of sarcopenia (%)	Method used for SMI/ASMI	Conclusions /comments
Author (year)	Country	Type of study	Male	Female	Prevalence of sarcopenia (%)	Method used for SMI/ASMI	Conclusions /comments
Bryant et al. (2015) [21]	Australia	Prospective	NA	NA	12	DEXA scan (ASMI)	Low muscle mass and sarcopenia common in IBD. Grip strength should be used routinely in clinical practice
Adams et al. (2017) [22]	USA	Retrospective	SMI: < 52.4	SMI: < 38.5	45	CT at L3 (SMI)	Sarcopenia common in overweight patients with IBD and may predict need for surgery
Bamba et al. (2017) [23]	Japan	Retrospective	SMI: < 42	SMI: < 38	42	CT at L3 (SMI)	Sarcopenia predictive factor for intestinal resection in admitted patients with CD
Pedersen et al. (2017) [24]	USA	Retrospective review	NA	NA	24.7	CT at L3, total psoas index (SMI)	Sarcopenia assessment can improve pre-operative outcomes
Zhang et al. (2017) [6]	China	Prospective	SMI: < 55	SMI: < 39	33.8	CT at L3 (SMI)	Skeletal muscle depletion correlates with disease activity in UC and is reversed after colectomy
Carvalho et al. (2019) [25]	Portugal	Retrospective	SMI: 52.4	SMI: 38.5	41.4	CT at L3 (SMI)	Sarcopenia diagnosis necessary for management of patients with CD
Pizzoferrato et al. (2019) [3]	Italy	Prospective	ASMI: 7.23	SMI: 5.6	28	DEXA (ASMI)	Sarcopenia associated with increased postoperative complications and mortality
Grillot et al. (2020) [26]	France	Retrospective	SMI: 52.4	SMI: 38.5	58	CT at L3 (SMI)	Sarcopenia and obesity associated with adverse outcomes in CD
Lee et al. (2020) [27]	South Korea	Retrospective	SMI: < 49	SMI: < 31	51	CT at L3 (SMI)	Sarcopenia predictive for intestinal resection in admitted patients with CD
Boparai et al. (2021) [9]	India	Retrospective	SMI: < 36.5	SMI: < 30.2	43	CT at L3 (SMI)	Combination of sarcopenia and high visceral fat predict poor outcomes in patients with CD
Celentano et al. (2021) [28]	UK	Retrospective	SMI: < 43.1	SMI: < 32.7	38	MRI at L3 (SMI)	Psoas muscle area can be used from MR enterography to calculate SMI
Ünal et al. (2021) [29]	Turkey	Prospective	NA	NA	41.3	EWGSOP2 (SMI)	Need for screening for sarcopenia and nutrition even when in clinical remission
Liu et al. (2022) [30]	China	Prospective	ASMI: 7	SMI: 5.7	50.8	DEXA scan (ASMI)	Patients with sarcopenia had poorer outcomes
Neelam et al. (2024) [10]	India	Prospective	ASMI: < 6.11	SMI: < 4.61	21.9 (patients with UC)	DEXA (ASMI)	Prevalence of sarcopenia higher in patients with active diseasewithUC

SMI, skeletal muscle index; IBD, inflammatory bowel disease; ASMI, appendicular SMI; DEXA, dual energy X-ray absorptiometry; CT, computed tomography; CD, Crohn’s disease; UC, ulcerative colitis.

NA, not available.

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Prevalence and outcome of sarcopenia in patients with inflammatory bowel disease: a follow-up study

DOI: https://doi.org/10.5217/ir.2024.00096

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Prevalence and outcome of sarcopenia in patients with inflammatory bowel disease: a follow-up study

Fig. 1. L3 level computed tomography scan with calculated normal- range skeletal muscle area (outlined in green).

Fig. 2. L3 level computed tomography scan with calculated lowrange skeletal muscle area (outlined in green).

Fig. 3. Kaplan-Meier analysis of freedom from flare.

Fig. 1.

Fig. 2.

Fig. 3.

Prevalence and outcome of sarcopenia in patients with inflammatory bowel disease: a follow-up study

Diagnostic parameter	Cutoff for defining sarcopenia
Muscle strength (hand and forearm muscles)	Male < 27 kg, female < 16 kg
Muscle mass	Male < 42 cm²/m², female < 38 cm²/m²
Physical performance	< 0.8 m/sec

Variable	Value (n = 117)
Disease duration (yr)
Crohn’s disease	3.5 (1.0–6.3)
Ulcerative colitis	4 (2-10)
IBD-U	5.5
Disease location, behavior, and extent^a
Crohn’s disease (n = 42)
L1	10 (22.7)
L2	8 (19.0)
L3	15 (32.7)
L1+ L4	9 (21.4)
B1	26 (61.9)
B2	13 (30.9)
B3	3 (7.14)
Perianal disease	8 (19.0)
Ulcerative colitis (n = 73)
E1	2 (2.7)
E2	31 (42.4)
E3	40 (54.7)
IBD-U (n = 2)	2 (1.7)

Descriptive data	Subgroup	Sarcopenia (n = 47)	No sarcopenia (n = 70)	P-value
Age (yr)		40.2 ± 14.9	43.9 ± 15.6	0.202
Sex	Male	21 (44.7)	44 (62.9)	0.052
	Female	26 (55.3)	26 (37.1)
Weight (kg)		55.6 ± 15.4	66.1 ± 13.8	< 0.001
Height (m)		1.6 ± 0.1	1.6 ± 0.1	0.233
BMI (kg/m²)		20.7 ± 4.3	25.5 ± 4.3	< 0.001
IBD type	CD	18 (38.3)	24 (34.3)	0.478
	UC	29 (61.7)	44 (62.9)
	IBD-U	0	2 (2.9)
Disease activity	Active	37 (78.7)	30 (42.9)	< 0.001
	Remission	10 (21.3)	40 (57.1)
Disease extent	CD	18	24	0.135
	L1	2 (11.1)	8 (33.3)
	L2	2 (11.1)	6 (25.0)
	L3	9 (50.0)	6 (25.0)
	L1+L4	5 (27.8)	4 (16.7)
	UC	29	44	0.365
	E1	0	2 (4.5)
	E2	11 (37.9)	20 (45.5)
	E3	18 (62.1)	22 (50.0)
Duration of disease (yr)		3 (1–9)	4 (2–10)	0.420
Hemoglobin (g/dL)		11.4 ± 1.7	12.2 ± 2.0	0.033
WBC (/cm³)		7,957 ± 3,262	7,461 ± 3,044	0.420
Platelets (/cm³)		3.4 ± 1.2	3.0 ± 1.0	0.065
Steroids		12 (25.5)	11 (15.7)	0.237
Biologics		11 (23.4)	7 (10.0)	0.049
Surgery		4 (8.5)	7 (10.1)	1.000

Variable	P-value	Odds ratio
Body mass index	0.001	0.722
Hemoglobin	0.485	0.914
Disease activity	0.073	0.409
Biologics	0.343	0.550

Author (year)	Country	Type of study	SMI (cm²/m²) or ASMI (kg/m²)		Prevalence of sarcopenia (%)	Method used for SMI/ASMI	Conclusions /comments
Author (year)	Country	Type of study	Male	Female	Prevalence of sarcopenia (%)	Method used for SMI/ASMI	Conclusions /comments
Bryant et al. (2015) [21]	Australia	Prospective	NA	NA	12	DEXA scan (ASMI)	Low muscle mass and sarcopenia common in IBD. Grip strength should be used routinely in clinical practice
Adams et al. (2017) [22]	USA	Retrospective	SMI: < 52.4	SMI: < 38.5	45	CT at L3 (SMI)	Sarcopenia common in overweight patients with IBD and may predict need for surgery
Bamba et al. (2017) [23]	Japan	Retrospective	SMI: < 42	SMI: < 38	42	CT at L3 (SMI)	Sarcopenia predictive factor for intestinal resection in admitted patients with CD
Pedersen et al. (2017) [24]	USA	Retrospective review	NA	NA	24.7	CT at L3, total psoas index (SMI)	Sarcopenia assessment can improve pre-operative outcomes
Zhang et al. (2017) [6]	China	Prospective	SMI: < 55	SMI: < 39	33.8	CT at L3 (SMI)	Skeletal muscle depletion correlates with disease activity in UC and is reversed after colectomy
Carvalho et al. (2019) [25]	Portugal	Retrospective	SMI: 52.4	SMI: 38.5	41.4	CT at L3 (SMI)	Sarcopenia diagnosis necessary for management of patients with CD
Pizzoferrato et al. (2019) [3]	Italy	Prospective	ASMI: 7.23	SMI: 5.6	28	DEXA (ASMI)	Sarcopenia associated with increased postoperative complications and mortality
Grillot et al. (2020) [26]	France	Retrospective	SMI: 52.4	SMI: 38.5	58	CT at L3 (SMI)	Sarcopenia and obesity associated with adverse outcomes in CD
Lee et al. (2020) [27]	South Korea	Retrospective	SMI: < 49	SMI: < 31	51	CT at L3 (SMI)	Sarcopenia predictive for intestinal resection in admitted patients with CD
Boparai et al. (2021) [9]	India	Retrospective	SMI: < 36.5	SMI: < 30.2	43	CT at L3 (SMI)	Combination of sarcopenia and high visceral fat predict poor outcomes in patients with CD
Celentano et al. (2021) [28]	UK	Retrospective	SMI: < 43.1	SMI: < 32.7	38	MRI at L3 (SMI)	Psoas muscle area can be used from MR enterography to calculate SMI
Ünal et al. (2021) [29]	Turkey	Prospective	NA	NA	41.3	EWGSOP2 (SMI)	Need for screening for sarcopenia and nutrition even when in clinical remission
Liu et al. (2022) [30]	China	Prospective	ASMI: 7	SMI: 5.7	50.8	DEXA scan (ASMI)	Patients with sarcopenia had poorer outcomes
Neelam et al. (2024) [10]	India	Prospective	ASMI: < 6.11	SMI: < 4.61	21.9 (patients with UC)	DEXA (ASMI)	Prevalence of sarcopenia higher in patients with active diseasewithUC

Table 1. Criteria for Defining Sarcopenia

Table 2. Disease Profile in Enrolled Patients

Values are presented as median (interquartile range) or number (%).

Location: L1, ileal disease; L2, colonic disease; L3, ileo-colonic involvement of disease; L4, upper gastrointestinal tract involvement. Behavior: B1, non-stricturing and non-penetrating disease; B2, stricturing disease; B3, penetrating disease. Extent: E1, involvement limited to rectum or rectosigmoid junction; E2, involvement limited to proportion of colorectum distal to splenic flexure; E3, involvement extending proximal to splenic flexure.

IBD-U, inflammatory bowel disease unclassified.

Table 3. Univariate Analysis of Factors Affecting Sarcopenia

Values are presented as mean±SD, number (%), or median (interquartile range).

BMI, body mass index; IBD, inflammatory bowel disease; CD, Crohn’s disease; UC, ulcerative colitis; IBD-U, IBD-unclassified; WBC, white blood cell; SD, standard deviation.

Table 4. Multivariate Analysis of Factors Affecting Sarcopenia

Table 5. Cutoff Levels of SMI Used for Defining Sarcopenia in IBD and Its Prevalence in Various Studies

SMI, skeletal muscle index; IBD, inflammatory bowel disease; ASMI, appendicular SMI; DEXA, dual energy X-ray absorptiometry; CT, computed tomography; CD, Crohn’s disease; UC, ulcerative colitis.