Abstract
Background
Osteosarcopenia based on computed tomography (CT) is gaining attention as a predictor of adverse outcomes in older adults with cancer.
Aims
We examined whether preoperative radiographic osteosarcopenia was associated with overall mortality (OM) among older patients with colorectal cancer (CRC).
Methods
Data of older patients (aged ≥ 60 years) who had undergone CRC surgery between October 2018 and February 2024 were retrospectively analyzed. A preoperative abdominal CT scan was used to assess skeletal muscle index (SMI) (cm2/m2) and vertebral bone density (VBD) in Hounsfield units. Patients were assigned into the following categories according to their VBD and SMI status: (i) normal VBD and SMI; (ii) low VBD only; (iii) low SMI only; or (iv) radiographic osteosarcopenia defined as the combination of low VBD and low SMI. The associations between radiographic osteosarcopenia and overall mortality were examined using survival analysis.
Results
In total, 235 older patients (mean age: 71.8 years) were included in the analysis. Of the 235 patients, 90 (38.3%) had normal VBD and SMI, 28 (11.9%) had low VBD alone, 75 (31.9%) had low SMI alone, and 42 (17.9%) had radiographic osteosarcopenia based on low VBD and low SMI. In multivariable analysis, radiographic osteosarcopenia was associated with a significantly higher risk of OM (hazard ratio (HR): 3.43, 95%CI: 1.42–8.23, p = 0.006) compared to normal VBD and SMI status. Low VBD alone or low SMI alone were not significantly associated with OM.
Conclusions
Radiographic osteosarcopenia is significantly associated with OM in older patients undergoing CRC surgery.
Supplementary Information
The online version contains supplementary material available at 10.1007/s40520-026-03372-w.
Keywords: Osteoporosis, Sarcopenia, Osteosarcopenia, Computed tomography, Cancer, Colorectal cancer, Surgery, Postoperative complications, Mortality
Introduction
Colorectal cancer (CRC) was the fourth most common cancer in the United States, accounting for approximately 53,000 deaths in 2025 [1]. Risk stratification beyond disease characteristics is essential to guide treatment decisions and informing targeted strategies to optimize patient care and outcomes after a CRC diagnosis.
Radiographic assessment of pre-treatment muscle quantity has gained attention in the oncology research for predicting clinical outcomes among patients with CRC [2–6]. Most studies have assessed muscle mass based on skeletal muscle index (SMI), which is derived by dividing the cross-sectional area of the skeletal muscle by the square of the patient’s body height in meters [7]. A common finding among several studies is that low SMI is associated with a greater risk of overall mortality among patients with CRC [2–6]. According to a recent meta-analysis of 16,031 patients with CRC, low SMI was associated with 28% higher risk of overall mortality compared to normal SMI [5].
In addition to low SMI, radiographic assessment of bone density may also be relevant for risk stratification, especially among older patients who often suffer from osteopenia or osteoporosis. Several studies in oncology have examined the combination of low SMI and low bone density using opportunistic computed tomography (CT) scans, to better understand the prognostic value of “radiographic osteosarcopenia” [8–10]. It is important to note, however, that radiographic osteosarcopenia is an imaging-based construct that does not represent a clinical diagnosis of osteosarcopenia given the lack of functional and strength criteria [11].The results of these studies suggest that radiographic osteosarcopenia is an independent predictor of overall mortality among patients with gastrointestinal cancer [8–10]. However, the dichotomization of participants as osteosarcopenic versus non-osteosarcopenic based on CT in some studies [8, 9, 12] precludes understanding the independent impacts of low SMI and low bone density on overall mortality. Similarly, radiographic osteosarcopenia based on CT is emerging as a predictor of postoperative complications after surgery for CRC [8] and gastric cancer [12].
Given the increasing interest in the prognostic value of radiographic osteosarcopenia through available CT scans along with the current limitations in the literature, further research is warranted. Therefore, the primary objective of this study was to examine whether preoperative radiographic osteosarcopenia was associated with overall mortality among a cohort of older patients undergoing CRC surgery. Additionally, the associations between radiographic osteosarcopenia and severe postoperative complications were evaluated in an exploratory analysis.
Methods
Study setting and participants
This was a retrospective cohort study of older patients (aged ≥60 years) who had been treated with surgery for CRC at the Our Lady of the Lake (OLOL) Hospital in Baton Rouge, Louisiana between October 2018 and February 2024. Patients were eligible for inclusion in the analysis if they were ≥ 60 years old at the time of surgery, had undergone a laparoscopic, robotic-assisted, or open procedure for CRC, and had an abdominal preoperative CT scan ≤ 6 months before surgery. Patients with stage IV disease, as well as those with artifacts and poor-quality CT scans were excluded.
Study data
The OLOL tumor registry was used to identify participants who met the inclusion criteria. Subsequently, data were retrieved from electronic medical records (EMRs) and the Vizient® Clinical Data Base (CDB) (Vizient, Inc. (2025). Clinical Data Base. Irving, TX: Vizient, Inc. Retrieved July 30, 2024). Data included patients’ demographic and disease characteristics, type of surgery, Charlson Comorbidity Index (CCI), CT-based SMI and bone density as described below, overall mortality, and social vulnerability. Social vulnerability was assessed via the Vizient Vulnerability Index™ (VVI) which uses ZIP codes to provide information on social vulnerability across nine domains: (i) Economic; (ii) education; (iii) healthcare access; (iv) neighborhood resources; (v) housing; (vi) clean environment; (vii) social environment; (viii) transportation; and (ix) public safety [13, 14]. These domains along with the overall VVI are calculated as standard deviations from the national mean with scores > 1 indicating high vulnerability. The VVI is gaining attention as a reliable measure of social vulnerability and a predictor of clinical outcomes across clinical populations [13, 14]. Study data were retrieved after approval by the Institutional Research Board at the Louisiana State University Health New Orleans (ID: 7224). Given the study design, the requirement for obtaining informed consent from study participants was waived. Data from the Vizient CDB were used with the permission of Vizient (all rights reserved).
Assessment of skeletal muscle index and vertebral bone density
A preoperative abdominal CT scan was used to assess SMI and vertebral bone density (VBD). The cross-sectional area (cm2) of the skeletal muscle area at the third lumbar vertebra (L3) was identified through a semi-automated Hounsfield unit (HU) threshold-based segmentation approach using a medical imaging software (Visage 7.1.18, Visage Imaging, Inc., San Diego, CA, US) that is integrated into our picture archiving and communication systems (PACS). The range of the HUs for skeletal muscle segmentation was set from − 29 to + 150 [15]. Subsequently, the entire cross-sectional area of the skeletal muscle (cm2) at the L3 level was divided by the patient’s square of body height to derive the SMI (cm2/m2). VBD was assessed based on the average attenuation (HU) of trabecular bone from the first to the fourth (L1 to L4) vertebrae per previous work [16]. An ovoid region of interest was manually placed in the center of the vertebral body from L1 to L4 avoiding areas of cortical bone (Fig. 1). All images were processed by a member of the study team (EP) with experience in tissue segmentation via CT. The assessor was blinded to the outcomes during measurement of VBD and SMI. Low SMI was defined per Martin et al. [17], in line with previous studies [18, 19]. Among men with a BMI < 25 kg/m2, low SMI was defined as < 43cm2/m2, whereas a cutoff of < 53 cm2/m2 was used for men with a BMI ≥ 25 kg/m2 [17]. Among women, low SMI was defined as < 41 cm2/m2 [17]. Low VBD was defined as a HU value of < 110 [20]. Patients were classified into the following categories based on their SMI and VBD status: (i) normal VBD and SMI; (ii) low VBD only; (iii) low SMI only; or (iv) radiographic osteosarcopenia (low VBD and low SMI). Radiographic osteosarcopenia, however, does not constitute a clinical diagnosis of osteosarcopenia as measures of muscle strength and function were not available.
Fig. 1.
Assessment of skeletal muscle cross-sectional area and vertebral bone density
Primary outcome
Overall mortality was assessed from the day of surgery until loss to follow up or death from any cause until April 2024. Patients who were lost to follow-up were censored at their last contact. Mortality status was confirmed using EMRs and obituary searches.
Exploratory outcome
Severe postoperative complications were assessed up to 30 days after surgery using EMRs and defined as grade ≥ 3 complications per the Clavien Dindo classification of surgical complications system [21].
Statistical analysis
Study data were summarized using the mean and standard deviation or frequencies and proportions where appropriate. The intra-rater reliability for assessing the repeatability of VBD and SMI measurements was evaluated in a random subset of 24 patients (~ 10% of the cohort) using the intraclass correlation coefficient (ICC3,1) based on a two-way mixed-effects model with absolute agreement. The correlation between SMI and VBD was assessed using Pearson’s correlation. The Kaplan-Meier plot was used to assess the probability of overall mortality based on VBD and SMI status categories. Multivariable Cox regression was used to determine the associations between radiographic osteosarcopenia and overall mortality. The adjusted analysis for overall mortality included variables with p ≤ 0.1 from univariate analysis. To reduce threshold dependence and further characterize the associations between CT-based measures and overall mortality, VBD and SMI were also examined as continuous predictors in separate multivariable Cox regression that included the same covariates as in the main model. The HRs are presented per 5-unit decrease for SMI and VBD. All analyses were completed using IBM SPSS for Windows, Version 29.0. Armonk, NY, USA: IBM Corp.
Sensitivity analyses
Given the limited number of events and concerns regarding bias or overfitting, a sensitivity analysis was conducted to examine whether the associations between radiographic osteosarcopenia and overall mortality persisted in more parsimonious models. To improve the event per variable (EPV) ratio, three multivariable Cox regression models were developed. The first model included age, AJCC stage, in addition to VBD and SMI status. The second model included the same variables in addition to comorbidities given their prognostic value [22, 23], while the third and final model retained the variables of the second model but was also adjusted for severe postoperative complications.
An additional sensitivity analysis was conducted to test whether the associations between radiographic osteosarcopenia and overall mortality differ by adjuvant treatment status, as the number of patients who received adjuvant treatment varied among groups. To improve model estimates, patients with low VBD alone and low SMI alone were merged.
Exploratory analysis
Logistic regression was used to explore the associations between radiographic osteosarcopenia and the occurrence of severe postoperative complications. Given the small number of events for severe postoperative complications, covariates in multivariable logistic regression included age and comorbidities to prevent model overfitting and due to their clinical relevance [24]. Additionally, in the exploratory analysis for severe postoperative complications, patients were collapsed into two categories based on the presence or absence of radiographic osteosarcopenia due to the small number of events in the entire cohort and within each VBD and SMI category.
Results
Characteristics of study participants
A total of 235 older patients (mean age: 71.8 years) were included in the analysis, of whom 126 (53.6%) were females. Regarding preoperative VBD and SMI status, 90 (38.3%) patients had normal VBD and SMI, 28 (11.9%) had low VBD only, 75 (31.9%) had low SMI only, and 42 (17.9%) were classified as having radiographic osteosarcopenia (Table 1). The ICCs for intra-rater reliability in measuring VBD and SMI were 0.97 (95%CI: 0.93–0.98) and 0.99 (95%CI: 0.98–0.99), respectively. Patients with radiographic osteosarcopenia were older (mean age: 78.2 years) but had comparable comorbidities and clinical characteristics compared to patients in the other categories. Notably, older patients with normal VBD and SMI status were more socially vulnerable per the VVI compared to other groups (Table 1). Of the 98 patients with AJCC stage III disease, 55 (56.1%) received adjuvant treatment in line with previous work among older patients with stage III colon cancer [25]. A weak positive correlation was found between SMI (cm2/m2) and VBD (HU) (r= 0.335, p < 0.001).
Table 1.
Characteristics of study participants
| Characteristic | All participants (n = 235) | Normal VBD and SMI (n = 90) | Low VBD (n = 28) | Low SMI (n = 75) | Radiographic osteosarcopenia (n = 42) | p |
|---|---|---|---|---|---|---|
| Age (years), mean SD | 71.8 (8.4) | 68.2 (6.7) | 72.4 (7.6) | 72.3 (8.0) | 78.2 (9.1) | < 0.001 |
| BMI (kg/m2), mean, SD | 27.8 (6.7) | 30.3 (7.8) | 28.4 (4.7) | 25.8 (5.0) | 25.3 (5.8) | < 0.001 |
| Sex (females), n (%) | 126 (53.6) | 39 (43.3) | 19 (67.9) | 37 (49.3) | 31 (73.8) | 0.004 |
| Race, n (%) | 0.10 | |||||
| White | 159 (67.7) | 54 (60.0) | 22 (78.6) | 50 (66.7) | 33 (78.6) | |
| Black | 76 (32.3) | 36 (40.0) | 6 (21.4) | 25 (33.3) | 9 (21.4) | |
| CCI, mean (SD) | 3.2 (1.7) | 3.3 (1.9) | 3.4 (1.7) | 3.0 (1.7) | 3.3 (1.6) | 0.62 |
| Cancer site, n (%) | 0.64 | |||||
| Colon | 189 (80.4) | 69 (76.7) | 22 (78.6) | 63 (84.0) | 35 (83.3) | |
| Rectal | 46 (19.6) | 21 (23.3) | 6 (21.4) | 12 (16.0) | 7 (16.7) | |
| Neoadjuvant treatment (yes), n (%) | 23 (9.8) | 10 (11.1) | 3 (10.7) | 8 (10.7) | 2 (4.8) | 0.69 |
| Adjuvant treatment (yes), n (%) | 69 (29.4) | 28 (31.1) | 6 (21.4) | 28 (37.3) | 7 (16.7) | 0.08 |
| AJCC stage, n (%) | 0.80 | |||||
| I | 54 (23.0) | 24 (26.7) | 9 (32.1) | 13 (17.3) | 8 (18.0) | |
| II | 83 (35.3) | 31 (34.4) | 8 (28.6) | 30 (40.0) | 14 (33.3) | |
| III | 98 (41.7) | 35 (38.9) | 11 (39.3) | 32 (42.7) | 20 (47.6) | |
| Type of surgery, n (%) | 0.19 | |||||
| Open | 53 (22.6) | 20 (22.2) | 2 (7.1) | 18 (24.0) | 13 (31.0) | |
| Laparoscopic | 93 (39.6) | 32 (35.6) | 13 (46.4) | 29 (38.7) | 19 (45.2) | |
| Robotic-assisted | 89 (37.9) | 38 (42.2) | 13 (46.4) | 28 (37.3) | 10 (23.8) | |
| Skeletal muscle index (cm2/m2) | 45.4 (10.3) | 53.6 (9.3) | 47.4 (6.1) | 40.3 (6.8) | 35.7 (4.9) | < 0.001 |
| Vertebral bone density (HU) | 129.5 (36.1) | 150.7 (23.9) | 86.8 (17.9) | 144.4 (24.5) | 85.8 (17.6) | < 0.001 |
| Vizient Vulnerability Index™ | 0.9 (0.9) | 1.2 (1.0) | 0.7 (0.6) | 0.9 (0.8) | 0.7 (0.7) | 0.018 |
AJCC= American Joint Committee on Cancer; BMI= body mass index; CCI= Charlson Comorbidity Index; HU= Hounsfield units
Note: n = 1 patient had missing information on the Vizient Vulnerability Index™. There were no missing values in the remaining variables
Associations between radiographic osteosarcopenia and overall mortality
Over a median follow up of 31.5 months, 51 (21.7%) patients died, of whom 14 (27.5%) had normal VBD and SMI status, 2 (3.9%) had low VBD alone, 14 (27.5%) had low SMI alone, while 21 (41.2%) had radiographic osteosarcopenia. Figure 2 illustrates the probability of overall mortality based on preoperative VBD and SMI status. Patients with radiographic osteosarcopenia had a significantly higher risk of death from any cause according to the log-rank test (p < 0.001). In univariate analysis, significant predictors of overall mortality were age, CCI, radiographic osteosarcopenia, American Joint Committee on Cancer (AJCC) stage, and type of surgery (Table 2). In univariate analysis, radiographic osteosarcopenia was a significant predictor of all-cause mortality compared to normal SMI and VBD status (hazard ratio (HR): 3.93, 95% confidence interval (CI): 1.99–7.75, p < 0.001). These findings persisted in the multivariable analysis, where patients with radiographic osteosarcopenia had a significantly higher risk of overall mortality compared to patients with normal VBD and SMI status (hazard ratio (HR): 3.43, 95%CI: 1.42–8.23, p = 0.006). Low VBD alone (HR: 0.47, 95%CI: 0.10–2.16, p = 0.33) or low SMI alone (HR: 1.51, 95%CI: 0.67–3.41, p = 0.32) were not significantly associated with a higher risk of overall mortality compared to normal SMI and VBD status (Table 2). Additional predictors of overall mortality in the multivariable analysis included age (HR: 1.06, 95%CI: 1.02–1.10, p = 0.004), a higher CCI (HR: 1.34, 95%CI: 1.17–1.53, p < 0.001), AJCC stage III disease (HR: 2.71, 95%CI: 1.48–4.93, p = 0.001), and higher social vulnerability per the VVI (HR: 1.52, 95%CI: 1.13–2.03, p = 0.005). An interaction term between VBD and SMI status and VVI was introduced to the multivariable model to evaluate potential moderation by social vulnerability. However, the interaction between VBD and SMI status and VVI was not statistically significant (p = 0.66) suggesting that the associations between of radiographic osteosarcopenia and overall mortality do not vary across levels of social vulnerability.
Fig. 2.
Probability of overall mortality based on VBD and SMI status (n = 235)
Table 2.
Univariate and multivariable Cox regression of the association between radiographic osteosarcopenia and overall mortality
| Variable | Univariate HR (95%CI) | p | Multivariable HRs (95%CI) (n = 234) | p |
|---|---|---|---|---|
| Age per year | 1.08 (1.04–1.11) | < 0.001 | 1.06 (1.02–1.10) | 0.004 |
| Sex (females) | 1.01 (0.58–1.76) | 0.97 | ||
| BMI per kg/m2 | 0.99 (0.94–1.03) | 0.53 | ||
| Race (Black) | ||||
| White | ref. | |||
| Black | 0.99 (0.56–1.78) | 0.99 | ||
| CCI per unit | 1.23 (1.09–1.38) | < 0.001 | 1.34 (1.17–1.53) | < 0.001 |
| CT-based VBD and SMI status | ||||
| Normal VBD and SMI | ref. | ref. | ||
| Low VBD | 0.44 (0.09–1.92) | 0.27 | 0.47 (0.10–2.16) | 0.33 |
| Low SMI | 1.26 (0.60–2.64) | 0.54 | 1.51 (0.67–3.41) | 0.32 |
| Radiographic osteosarcopenia | 3.93 (1.99–7.75) | < 0.001 | 3.43 (1.42–8.23) | 0.006 |
| Cancer site | 0.58 (0.25–1.37) | 0.21 | ||
| AJCC stage | ||||
| I-II | ref. | ref. | ||
| III | 2.12 (1.22–3.69) | 0.008 | 2.71 (1.48–4.93) | 0.001 |
| Neoadjuvant therapy (yes) | 0.93 (0.33–2.57) | 0.88 | ||
| Type of surgery | ||||
| Robotic-assisted | ref. | ref. | ||
| Laparoscopic | 2.37 (1.14–4.94) | 0.021 | 1.41 (0.66–3.01) | 0.37 |
| Open | 2.67 (1.21–5.89) | 0.015 | 1.66 (0.74–3.74) | 0.22 |
| Adjuvant therapy (yes) | 0.59 (0.31–1.16) | 0.13 | ||
| Vizient Vulnerability Index™ | 1.27 (0.95–1.68) | 0.10 | 1.52 (1.13–2.03) | 0.005 |
AJCC= American Joint Committee on Cancer; BMI= body mass index; CCI= Charlson Comorbidity Index; CT= computed tomography; HR= hazard ratio; SMI= skeletal muscle index; VBD= vertebral bone density
Note: n = 1 was missing information on the Vizient Vulnerability Index™. There were no missing values in the remaining variables
Skeletal muscle index and vertebral bone density as continuous predictors of overall mortality
In the univariate analysis, a 5-unit lower SMI was significantly associated with overall mortality (HR: 1.26, 95%CI: 1.08–1.47, p = 0.004). A significant association was also observed between a 5-unit lower VBD and overall mortality (HR: 1.06, 95%CI 1.02–1.09, p = 0.004). Table 3. illustrates the associations between SMI, VBD, and overall mortality. A 5-unit lower SMI was associated with a 21% higher risk of overall mortality (HR: 1.21, 95%CI: 1.02–1.43, p = 0.026). However, VBD was not associated with overall mortality (HR: 1.02, 95%CI: 0.97–1.06, p = 0.45) (Table 3). In line with the main model, older age, a higher CCI, AJCC stage III disease, and a higher VVI were significantly associated with overall mortality (Table 3). An interaction term between SMI and VBD was forced into the multivariable model, but it was not statistically significant (p = 0.26).
Table 3.
Multivariable Cox regression of the associations between continuous CT-based measures and overall mortality
| Variable | Multivariable HRs (95%CI) (n = 234) | p |
|---|---|---|
| Age per year | 1.07 (1.03–1.11) | < 0.001 |
| CCI per unit | 1.34 (1.17–1.53) | < 0.001 |
| SMI per − 5 cm2/m2 | 1.21 (1.02–1.43) | 0.026 |
| VBD per − 5 HU | 1.02 (0.97–1.06) | 0.45 |
| AJCC stage | ||
| I-II | ref. | |
| III | 3.05 (1.67–5.55) | < 0.001 |
| Type of surgery | ||
| Robotic-assisted | ref. | |
| Laparoscopic | 1.68 (0.79–3.55) | 0.18 |
| Open | 1.71 (0.76–3.88) | 0.19 |
| Vizient Vulnerability Index™ | 1.45 (1.09–1.92) | 0.011 |
AJCC= American Joint Committee on Cancer; CCI= Charlson Comorbidity Index; HR= hazard ratio; SMI= skeletal muscle index; VBD= vertebral bone density
Note: n = 1 was missing information on the Vizient Vulnerability Index™. There were no missing values in the remaining variables
Sensitivity analyses of the associations between radiographic osteosarcopenia and overall mortality
Supplementary Table 1 illustrates the sensitivity analyses of the associations between radiographic osteosarcopenia and overall mortality. Three multivariable models were developed. In the first multivariable model (EPV ratio: 10.2) that was adjusted for age and AJCC stage, patients with radiographic osteosarcopenia had a significantly higher risk of overall mortality compared to those with normal VBD and SMI (HR: 2.21, 95%CI: 1.02–4.81, p = 0.045). The addition of comorbidities to the second multivariable model (EPV ratio: 8.5) strengthened the association between radiographic osteosarcopenia and overall mortality (HR: 2.76, 95%CI: 1.22–6.26, p = 0.015). A similar association between radiographic osteosarcopenia and overall mortality (HR: 2.69, 95%CI: 1.15–6.28, p = 0.022) was observed in the third and final multivariable model (EPV ratio: 6.9) (Supplementary Table 1). Older age, higher comorbidities per the CCI, and AJCC stage III disease were consistent predictors of overall mortality in sensitivity analyses. Similarly, severe postoperative complications were significantly associated with a higher risk of overall mortality (HR: 2.49, 95%CI: 1.25–5.01, p = 0.010) (Supplementary Table 1).
Sensitivity analysis stratified by adjuvant treatment status
Supplementary Table 2 illustrates the stratified analysis by adjuvant treatment status. The HR for patients with radiographic osteosarcopenia who received adjuvant treatment was HR: 2.62, 95%CI: 0.48–14.41, p = 0.27. Patients with radiographic osteosarcopenia who did not receive adjuvant treatment had a HR of 3.95, 95%CI: 1.83–8.49, p < 0.001 (Supplementary Table 2).
Exploratory analysis of the associations between radiographic osteosarcopenia and severe postoperative complications
Severe postoperative complications were examined in 231 of the 235 patients. Four patients were excluded from the analysis as the outcome could not be assessed due to unavailable clinical notes up to 30 days after surgery. A total of 32 (13.9%) participants experienced at least one severe postoperative complication, of whom 13 (40.6%) had normal SMI and VBD, 2 (6.3%) had low VBD alone, 6 (18.8%) had low SMI alone, while 11 (34.4%) had radiographic osteosarcopenia. Due to the small number of events, particularly among patients with low VBD alone or low SMI alone, groups were collapsed, and patients were dichotomized into those with and without radiographic osteosarcopenia (Supplementary Table 3). Radiographic osteosarcopenia was a significant predictor of severe postoperative complications in the univariate (OR: 3.07, 95%CI: 1.34–7.04, p = 0.008) and multivariable (OR: 2.79, 95%CI: 1.12–6.99, p = 0.028) analyses (Supplementary Table 3).
Discussion
This retrospective cohort study examined the associations between preoperative radiographic osteosarcopenia and overall mortality among older patients undergoing CRC resection. The prevalence of preoperative radiographic osteosarcopenia in our study (17.9%) is comparable to previous work in patients with CRC cancer, where radiographic osteosarcopenia was present in 16.5%-25.8% of the sample [8, 10].
Our results demonstrate that patients with radiographic osteosarcopenia were approximately 3.4 times more likely to die of any cause compared to patients with normal VBD and SMI status. An increased risk of overall mortality in the presence of preoperative radiographic osteosarcopenia has also been observed in other studies among patients with CRC and gastric cancer [8, 9, 12]. Nonetheless, these studies assigned participants into two categories (osteosacopenic vs. non-osteosarcopenic based on CT) [8, 9, 12]. In contrast, our study included four categories based on the patients’ SMI and VBD status to further characterize the associations between radiographic osteosarcopenia and overall mortality. The prognostic value of radiographic osteosarcopenia may also be relevant to patients undergoing non-oncologic surgeries. For example, Solla-Suarez et al., who assigned participants to four categories based on their psoas muscle area (PMA) and VBD status, found a significant association between preoperative radiographic osteosarcopenia and overall mortality among older adults undergoing transcatheter aortic valve replacement [16]. In that study [16], low VBD alone, or low PMA alone, were not significantly associated with overall mortality compared to normal VBD and PMA status before surgery. The lack of a significant association between low SMI and overall mortality in our study is a surprising finding, given previous meta-analytic data that demonstrate a higher risk of overall mortality among patients with low SMI [26]. Additionally, patients with low VBD alone exhibited very few deaths (n = 2) resulting in wide confidence intervals. Therefore, cautious interpretation is advised due to sparse data bias in this group.
In further analysis, we found that lower SMI per 5 units was significantly associated with a 21% higher risk of overall mortality in this cohort of older patients. Our findings further the understanding of the association between SMI and overall mortality, as most oncology studies have used specific cutoffs to examine it. This cutoff-based approach relies on the assumption that patients assigned to categories based on their SMI value have the same risk which may not be accurate [27]. Our findings are in line with previous work among patients with CRC [28] and other solid tumors [29, 30]. Although lower VBD per 5 units was significantly associated with a 6% higher risk overall mortality in the univariate analysis, this association was attenuated after adjusting for covariates in the multivariable analysis and was no longer statistically significant.
An important consideration regarding our primary analysis is the low EPV ratio which raises the concern of model overfitting. Sensitivity analyses were conducted to address this concern by creating three multivariable Cox regression models with fewer predictors, resulting in improved EPV ratios. Radiographic osteosarcopenia remained a significant predictor of overall mortality in sensitivity analyses.
Although adjuvant treatment status did not meet our criteria for inclusion in the main multivariable model, we performed a stratified analysis to test whether the associations between radiographic osteosarcopenia and overall mortality differ by adjuvant treatment status. Our results indicate that radiographic osteosarcopenia may be associated with a higher risk of overall mortality among those who do not receive adjuvant treatment. Regarding the cohort that received adjuvant treatment, the small sample and associated wide confidence intervals preclude from assessing whether radiographic osteosarcopenia is associated with overall mortality in response to adjuvant treatment, underscoring the need for additional studies with larger samples.
An attempt to elucidate the mechanisms behind the associations between radiographic osteosarcopenia and overall mortality among older patients with CRC is challenging due to the retrospective nature of this study. However, radiographic osteosarcopenia may co-exist with frailty as demonstrated by a prospective cohort study of community dwelling older adults (mean age: 63.9 years) [31]. Several studies suggest that older cancer survivors who are frail have a significantly higher risk of overall mortality compared to their non-frail counterparts [32–34].
In addition to radiographic osteosarcopenia, age. a higher CCI, AJCC stage, and social vulnerability via the VVI were independently associated with overall mortality in this cohort. Regarding social vulnerability, each unit increase in the VVI was associated with a 52% higher risk of overall mortality in the primary model, which is in line with previous research among patients with gastrointestinal cancer [35]. However, a worse VBD and/or SMI status prior to surgery was not associated with a higher VVI, which was an unexpected finding. A worse VBD and SMI status may be indicative of frailty, which is associated with higher social vulnerability among older adults [36]. Nonetheless, we cannot conclusively determine whether individuals with radiographic osteosarcopenia in our cohort were truly frail solely based on imaging-based techniques and without information on physical function or other relevant variables. Others have shown that social vulnerability may not always explain declines in indices of frailty [37], which is a counterintuitive finding. However, as noted by the authors of that study, geographic-based social vulnerability may not entirely capture exposure to social vulnerability [37], which may be plausible in our study. It may also be that those with normal VBD and SMI appear to be more socially vulnerable due to lack of transportation and/or exposure to low-wage, physically demanding work that may preserve VBD and SMI. Future studies are warranted to characterize the associations between social vulnerability and body composition measures among older patients with cancer.
In an exploratory analysis, radiographic osteosarcopenia was also a significant predictor of 30-day severe postoperative complications. These findings are in line with previous literature among patients with CRC and gastric cancer [8, 12]. However, cautious interpretation is advised as patients were dichotomized based on the presence/absence of radiographic osteosarcopenia due to the small number of events and to improve model estimates.
This study has several strengths. First, the use of four categories based on the patients’ VBD and SMI status furthers the understanding of the associations between preoperative radiographic osteosarcopenia and overall mortality among older patients with CRC. Second, the inclusion of the VVI in the multivariable analysis is another strength, as most studies do not report on social vulnerability status despite its prognostic value. Several limitations should be considered when interpreting the findings of this study. First, our analysis did not include measures of muscle strength and function, which have been shown to predict overall mortality among older adults with cancer [38]. Therefore, we cannot conclusively determine the presence of osteosarcopenia in our cohort merely based on imaging-based VBD and SMI. To avoid potential misinterpretation, the term radiographic osteosarcopenia was used to accurately reflect our methodology and risk exposure for the group that exhibited CT-based low VBD and low SMI combined. Second, our analysis focused only on muscle quantity based on CT-defined SMI, but not skeletal muscle density which has been shown to be predictive of overall mortality among older adults with cancer [39, 40]. Additionally, the low EPV ratio in our primary analysis is a limitation as it can increase the risk of bias and model overfitting. Sensitivity analyses, however, demonstrated that the associations between radiographic osteosarcopenia and overall mortality persisted in more parsimonious models. Moreover, our exploratory analysis on the associations between radiographic osteosarcopenia and the occurrence of severe postoperative complications did not include our initial four VBD and SMI categories. Instead, patients were dichotomized based on the presence of radiographic sarcopenia, an analytical approach that was selected due to the small number of events within each category. Further studies with larger sample sizes and sufficient number of events are warranted to examine whether low VBD and low SMI alone or combined predict severe postoperative complications following CRC surgery. Furthermore, information on the cause of death or data on disease-free survival (DFS) or cancer-specific survival (CSS) were not available, which has several implications for clinical interpretation. For example, radiographic osteosarcopenia may reflect higher vulnerability which is often characterized by metabolic dysregulation and reduced physical function, thereby increasing the risk of adverse outcomes, such as postoperative complications falls, unplanned hospitalizations, and non-cancer related deaths [41, 42]. The extent to which radiographic osteosarcopenia can contribute to mortality due to disease-related factors (e.g., treatment failure, disease progression) cannot be determined given the retrospective nature of this study and the available information. It is also important to note that 47.6% of patients with radiographic osteosarcopenia in our study had stage III disease, which was a significant predictor of overall mortality. Further research is warranted to describe the associations between radiographic osteosarcopenia and additional outcomes (e.g., PFS and CSS) along with associated biological mechanisms. Additional study limitations include the lack of physical activity and nutritional data. Physical activity has been associated with a lower risk of overall- and cancer-specific mortality among older adults [43] while recent evidence from a phase III randomized controlled trial demonstrated prolonged DFS among colon cancer patients who followed a structured exercise program compared to those receiving health-education alone (median age: 61 years) following adjuvant chemotherapy [44]. In addition to physical activity and exercise, adequate caloric and protein intake may positively influence muscle mass and function while reducing hospitalizations and treatment complications among patients with cancer [45, 46]. Collectively, improvements in these outcomes may influence overall mortality. Given the lack of information on physical function, physical activity, and nutritional status, the possibility of residual confounding should be considered when interpreting our findings.
Our findings are clinically relevant and underscore the importance of targeted interventions for older patients to improve muscle mass and bone mineral density, starting as early as possible after diagnosis and prior to cancer treatment [47]. Exercise recommendations for improving muscle mass and bone mineral density in older adults are provided elsewhere [48]. In brief, the Intrinsic Capacity of Frailty and Sarcopenia Research (ICFSR) recommends resistance and power training, along with balance and gait exercises for geriatric syndromes such as sarcopenia and frailty [48]. To improve bone mineral density and balance, the ICFSR recommends high-impact activities, in addition to resistance training and balance exercises [48]. However, pre-exercise health screening is necessary to inform exercise prescription as certain conditions may contraindicate high-impact training or power training. For example, the presence of osteoarthritis or tendinopathies may preclude the use of power training or high-impact exercises [48]. Therefore, careful selection of exercises tailored to the unique needs and abilities of the patient is critical to minimize the risk of injuries while improving health outcomes.
Conclusion
Radiographic osteosarcopenia is associated with an increased risk of overall mortality among older patients with CRC. Targeted interventions aimed at increasing muscle mass and bone mineral density may improve patient care and long-term outcomes in older patients with CRC.
Supplementary Information
Below is the link to the electronic supplementary material.
Author contributions
Conceptualization and methodology: Efthymios Papadopoulos. Investigation: All authors. Data management and analysis: Efthymios Papadopoulos. Data analysis and interpretation of the data: All authors. Preparation of manuscript: Efthymios Papadopoulos. Manuscript review: All authors.
Funding
No funding was received to assist with the preparation of this manuscript.
Data availability
The data of this study are available from the corresponding author (EP) upon reasonable request.
Declarations
Competing interests
The authors declare no competing interests.
Ethics Approval
All study procedures were approved by the Institutional Research Ethics Board at the Louisiana State University Health New Orleans (ID: 7224).
Footnotes
Publisher’s Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
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Associated Data
This section collects any data citations, data availability statements, or supplementary materials included in this article.
Supplementary Materials
Data Availability Statement
The data of this study are available from the corresponding author (EP) upon reasonable request.