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. 2023 Dec 1;35(12):817–824. doi: 10.1589/jpts.35.817

Addition of the nutrition factor enhances the cancer prehabilitation program design for colorectal cancer patients: a multi-center cohort study

Tsuyoshi Hara 1,*, Eisuke Kogure 2, Shinno Iijima 3, Yasuhisa Fukawa 4, Akira Kubo 5, Wataru Kakuda 6
PMCID: PMC10698313  PMID: 38075511

Abstract

[Purpose] The purpose of this study was to investigate the interrelationship between different baseline functional capacity items, and their relationship with postoperative course in colorectal cancer patients. [Participants and Methods] This was a three-institution cohort study that included 127 patients scheduled for elective colorectal cancer surgery. Baseline functional capacity was evaluated using skeletal muscle index (SMI), six-minute walk test (6MWT), serum-albumin (Alb), vitality, and mental health before surgery. Postoperative findings, including C-reactive protein (CRP) levels 3 days post-operation, frequency of postoperative complications, and length of hospital stay (LOS), were evaluated based on the medical records. [Results] CRP was positively related to SMI, but negatively related to Alb level. LOS was negatively related to vitality. The 6MWT results and mental health-related findings were not significantly related to the postoperative course, but were directly and indirectly related to vitality, respectively. Alb level was also indirectly related to vitality through the 6MWT and mental health-related findings. The final constructed model demonstrated an acceptable fit to the data (goodness-of-fit index=0.958, adjusted goodness-of-fit index=0.930, comparative fit index=1.000, root mean square error of approximation=0.000). [Conclusion] Nutrition status, as measured by Alb level before surgery, may positively affect both the postoperative course and other functional capacity parameters.

Keywords: Colorectal surgery, Exercise, Postoperative course

INTRODUCTION

In cancer medicine, surgery is a cornerstone in the curative treatment of colorectal cancer (CRC); however, it will cause pain, and fatigue which negatively impact physical function, limiting activities of daily living1, 2). Additionally, if postoperative complications develop in patients with CRC, not only will the physical and mental burdens of patients worsen, but reductions in quality of life and lifespan can occur3, 4). As such, cancer prehabilitation has attracted worldwide attention as a multidisciplinary preoperative intervention aimed at preventing complications and improving postoperative outcomes5). Cancer prehabilitation determines the baseline functional capacity from the assessment of physical, nutritional, and psychological status and intervenes to improve a cancer patient’s preoperative functional reserve before surgery6). Because functional impairment in oncology patients is multi-factorial, cancer prehabilitation employs a multimodal treatment approach by combining various evaluations and interventions5). Additionally, it considers the synergistic effect of combining interventions7).

Recently, cancer prehabilitation for patients with CRC was reported in a systematic review8). However, previous studies have mostly used unimodal interventions, such as only physical exercise or nutrition, and few have investigated multimodal cancer prehabilitation9,10,11,12). Additionally, the effects of cancer prehabilitation were relatively insignificant, and evidence-based outcomes were limited8). Thus, no consensus exists on the design and contents of an ideal cancer prehabilitation program or what cancer patients would benefit from the most. Therefore, there is a need for not only a randomized control trial of multimodal interventions, but also for a factor analysis to clarify the relationship between each component and enhance the rationale for the program design.

The purpose of this study was to provide a comprehensive evaluation of baseline functional capacity factors, including the physical, nutritional, and psychological status of patients with CRC, to investigate how they relate to each other and how they influence the outcome of the postoperative course to enhance the rationale of the program design.

PARTICIPANTS AND METHODS

This study was approved by the Research Ethics Board of the International University of Health and Welfare, Otawara-shi, Tochigi, Japan, and the study procedures were performed by ethical standards (Registration no. 17-Io-202-2). All participants provided oral and written informed consent, and the study was conducted by the principles of the Declaration of Helsinki.

The participants were scheduled to undergo elective surgery for CRC at the International University of Health and Welfare Mita Hospital, the International University of Health and Welfare Hospital, or the International University of Health and Welfare Ichikawa Hospital. These hospitals are accredited as designated cancer hospitals and cancer treatment hospitals. The exclusion criteria included having received neoadjuvant therapy or a diagnosis of a non-malignant tumor after surgery. Data on patient demographics and characteristics, age at baseline, gender, clinical stage of cancer, diagnosis, type of surgery, surgery duration, and amount of blood loss were collected.

This study was designed as a three-institution cohort study. The study period was between March 1, 2016, and March 31, 2020. Functional capacity based on cancer prehabilitation was evaluated at baseline and 1–2 days before surgery. Additionally, data on the parameters of the postoperative course were prospectively collected from medical records. Each participant’s perioperative care was managed by a surgeon who specialized in colorectal surgery; the care provided was based on the clinical pathway for CRC surgery provided by each acute care medical institution. All patients underwent medical examination performed by a rehabilitation physician and postoperative physical therapy performed by a physical therapist.

For the baseline functional capacity, skeletal muscle index (SMI), 6-minute walk test (6MWT), serum albumin (Alb), vitality (VT), and mental health (MH) parameters were assessed based on the cancer prehabilitation components (i.e., exercise, nutrition, and mental care) (Fig. 1)8). The SMI was evaluated based on computed tomography (CT) images at the 3rd lumbar vertebra (L3) using thresholds of −29 to +150 Hounsfield units (HU: water was defined as 0 HU, air as 1,000 HU)13). The SMI was normalized using the sum of the cross-sectional areas of multiple muscles, including the psoas, erector spinae, quadratus lumborum, transversus abdominis, external and internal oblique abdominals, and rectus abdominis muscles, divided by the square of the height. SMI analyses were performed using ImageJ (version 1.51; NIH, Bethesda, MD, USA; Java 1.8.0_112). The 6MWT was performed based on the guidelines of the American Thoracic Society14). Patients were instructed to walk back and forth along a 30-m hallway for 6 minutes at a pace that required maximum effort by the end of the walk. The total distance covered within 6 minutes was recorded. Data on Alb levels were collected using the laboratory data obtained upon admission based on medical records. The VT and MH were evaluated using the Japanese 36-Item Short-Form Health Survey (SF-36), version 2, acute form15,16,17). The SF-36 is a self-administered questionnaire that includes 8 subscales including VT and MH. The VT and MH scores were calculated using the SF-36 version 2 scoring program recommended by iHope International. In this study, VT and MH scores ranged from 0 to 100 points, with higher scores indicating better psychological status. Additionally, patients followed the instructions of the rehabilitation staff to complete the SF-36 questionnaire.

Fig. 1.

Fig. 1.

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Conceptual model of the relationship between cancer prehabilitation and clinical outcomes in patients with colorectal cancer.

For postoperative course parameters, the C-reactive protein (CRP) on postoperative day 3, frequency of postoperative complications (PCs), and length of hospital stay (LOS) were adopted based on the clinical outcomes of cancer prehabilitation, or outcomes that influence the postoperative course and contribution to health care systems (Fig. 1)8). Data on CRP levels were obtained from medical records obtained on postoperative day 3, as this reflects the postoperative immune response associated with surgery and strongly relates to PCs18). The frequency of PCs was graded using the Clavien–Dindo classification19) based on medical records from the patient’s hospital stay. In this study, complications classified as grade II or higher according to the Clavien–Dindo system were defined as PCs20). Data on LOS, defined as the period of hospital stay from admission to discharge, were collected from medical records.

The relationship between baseline functional capacity and postoperative course parameters was first analyzed using the Pearson’s product-moment correlation coefficient and Spearman’s rank correlation coefficient. The final model was analyzed using the structural equation modeling path analysis, based on the conceptual model of cancer prehabilitation (Fig. 1). The following parameters were included in the final model based on the temporal relationship of the postoperative course: the CRP level on postoperative day 3 was directly related to the frequency of PCs; further, the frequency of PCs was directly related to LOS. The interrelationship of baseline functional capacity parameters and the relationship between baseline functional capacity and postoperative course parameters were examined as direct and/or indirect associations with each other. Second, age at baseline and sex, which were significantly related to the baseline functional capacity based on the Pearson’s product-moment correlation coefficient or Spearman’s rank correlation coefficient, were examined for their direct association with the baseline functional capacity.

A final model was derived by excluding the relationship of non-significant variables. The goodness-of-fit of final models were evaluated using the following parameters of goodness-of-fit indices (GFI; values >0.90 indicate good model fit)21): the adjusted GFI (AGFI; values >0.90 indicate good model fit)21), the comparative fit index (CFI; values >0.90 indicate good model fit)22), and the root mean square error of approximation (RMSEA; values <0.07 indicate good model fit)23). All statistical analyses were performed using SPSS Statistics version 28.0 and SPSS Amos version 28.0 (SPSS Inc., Chicago, IL, USA). Statistical significance was set at p<0.05.

RESULTS

In total, 232 patients were approached for consent; 20 patients declined to participate and 85 patients were excluded (three according to the exclusion criteria and 82 due to incomplete data). Ultimately, a total of 127 patients were enrolled in the study. All the study participants were of Japanese descent. The patient demographics and characteristics are shown in Table 1. The mean age at baseline was 63.8 ± 11.5 years, and 63% were male. The diagnosis was colon cancer in 53% of cases, and laparoscopic surgery was performed in 91% of cases. The baseline functional capacity and postoperative course parameters are also shown in Table 1. The frequency of PCs, based on the Clavien–Dindo classification, observed in the complication group was as follows: Grade I, 25%; grade II, 20%; grade III, 8%; grade IIIa, 6%; and grade IIIb, 2%. The most common PCs were infection in nine cases (7%), followed by ileus in six cases (5%). The mean LOS was 18.9 ± 11.1 days.

Table 1. Patient demographics and clinical characteristics.

Patients with colorectal cancer
n=127
Age (years) 63.8 ± 11.5
Gender Female 47 (37)
Male 80 (63)
Clinical stage of cancer I 42 (33)
II 43 (34)
III 35 (28)
IV 7 (5)
Diagnosis Colon cancer 67 (53)
Rectal cancer 60 (47)
Type of surgery Open 8 (7)
Laparoscopic 116 (91)
Robot-assisted 3 (2)
Surgery duration (min) 265.0 ± 109.1
Blood loss (mL) 136.5 ± 421.8
Baseline functional capacity Skeletal muscle index (cm2/m2) 37.2 ± 8.7
6-minute walk test (meters) 514.8 ± 96.0
Serum-albumin (mg/dL) 4.2 ± 0.5
Vitality 65.8 ± 19.7
Mental health 68.2 ± 21.5
Postoperative course parameters C-reactive protein on postoperative day 3 (mg/dL) 9.8 ± 6.2
Clavien–Dindo classification*
Grade I 32 (25)
Grade II 25 (20)
Grade III 10 (8)
Grade IIIa 7 (6)
Grade IIIb 3 (2)
Grade IV 0
Grade IVa 0
Grade IVb 0
Grade V 0
Postoperative complications (grade II or higher)*
Infection 9 (7)
Ileus 6 (5)
Anastomotic leakage 5 (4)
Anastomotic stenosis 1 (1)
Lymphatic fistula 1 (1)
Other 10 (8)
Cases corresponding to Clavien–Dindo classification grade II or higher 33 (26)
Length of hospital stay (days) 18.9 ± 11.1
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Values are number (percentage for total patients) or mean ± standard deviation.

*Includes duplicate cases.

The correlations between baseline functional capacity and postoperative course parameters are shown in Table 2. In terms of the relationship between baseline functional capacity variables, the SMI was significantly and positively correlated with the 6MWT findings (r=0.195). The 6MWT findings were significantly correlated with the Alb level (r=0.484) and MH-related findings (r=0.188). Further, VT was significantly and positively correlated with the MH-related findings (r=0.652). In terms of the relationship between postoperative course parameters, the CRP on postoperative day 3 was significantly correlated with the PCs (r=0.300) and LOS (r=0.267). Additionally, the PCs were significantly and positively correlated with the LOS (r=0.466). Finally, in terms of the relationship between baseline functional capacity and postoperative course parameters, the SMI on postoperative day 3 was significantly and positively correlated with the CRP (r=0.372). The 6MWT findings on postoperative day 3 was significantly and negatively correlated with the CRP (r=−0.197) and LOS (r=−0.242). In addition, the Alb level on postoperative day 3 was significantly and negatively correlated with the CRP (r=−0.220) and LOS (r=−0.300). In the sub-analysis of the relationship between baseline functional capacity and demographics, the age at baseline was significantly correlated with the SMI (r=−0.204), 6MWT findings (r=−0.469), and Alb level (r=−0.374). Additionally, sex was significantly correlated with the SMI (r=0.640) (Table 2).

Table 2. Correlations between baseline functional capacity and postoperative course parameters.

6MWT Alb VT MH CRP PCs LOS Age Sex
Skeletal muscle index (SMI) 0.195* 0.136 0.012 −0.011 0.372* 0.079 −0.023 −0.204* 0.640†
6-minute walk test (6MWT) 0.484* 0.163 0.188* −0.197* −0.158 −0.242† −0.469* 0.103
Serum-albumin (Alb) 0.117 0.039 −0.220* −0.076 −0.300† −0.374* 0.002
Vitality (VT) 0.652* −0.076 −0.011 −0.166 −0.015 0.091
Mental health (MH) −0.077 −0.001 −0.167 0.045 0.079
C-reactive protein on postoperative day 3 (CRP) 0.300† 0.267† 0.171 0.291†
Cases corresponding to Clavien–Dindoclassification grade II or higher (PCs) 0.466† 0.129 0.119
Length of hospital stay (LOS) 0.109 0.017
Age 0.076
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* Significant difference for Pearson’s product-moment correlation coefficient.

† Significant difference for Spearman’s rank correlation coefficient.

In terms of the total effect of baseline functional capacity on postoperative course parameters, the SMI (standardized β=0.411, p<0.05) and Alb level (standardized β=−0.273, p<0.05) were significantly and directly related to the CRP on postoperative day 3. VT was significantly and directly related to LOS (standardized β=−0.158, p<0.05). The 6MWT findings were negatively and indirectly related to LOS through the MH and VT findings (standardized β=−0.019, p<0.05), whereas the MH-related findings were negatively and indirectly related to LOS through VT (standardized β=−0.103, p<0.05) (Table 3).

Table 3. Standardized total effect of cancer prehabilitation items with postoperative course items in the final model.

SMI 6MWT Alb VT MH
C-reactive protein on postoperative day 3 0.411 −0.273
Frequency of postoperative complications 0.110 −0.073
Length of hospital stay 0.051 −0.019 −0.041 −0.158 −0.103
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Complications classified as grade II or higher according to the Clavien–Dindo system were defined as postoperative complications.

SMI: Skeletal muscle index; 6MWT: 6-minute walk test; Alb: Serum-albumin; VT: Vitality; MH: Mental health.

The postoperative course parameters in the final model showed that the CRP on postoperative day 3 was significantly and directly related to the frequency of PCs (standardized β=0.268, p<0.05), and that the frequency of PCs was significantly and directly related to LOS (standardized β=0.463, p<0.05). In terms of the interrelationship of baseline functional capacity parameters, the Alb level was positively and directly related to 6MWT findings (standardized β=0.359, p<0.05), whereas the 6MWT findings were positively and directly related to MH (standardized β=0.188, p<0.05). Additionally, MH was significantly and directly related to VT (standardized β=0.652, p<0.05). In the final model, the age at baseline was negatively and directly related to the SMI (standardized β=−0.243, p<0.05), 6MWT findings (standardized β=−0.334, p<0.05), and Alb level (standardized β=−0.374, p<0.05). Additionally, sex (male: 1, female: 0) was negatively and directly related to the SMI (standardized β=0.609, p<0.05). The fit parameters of the final model were as follows: χ2=28.548, df=33, GFI=0.958, AGFI=0.930, CFI=1.000, and RMSEA=0.000 (Fig. 2).

Fig. 2.

Fig. 2.

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The final model of cancer prehabilitation items leading to the postoperative course in patients with colorectal cancer.

*p<0.05.

Model fit: goodness-of-fit index (GFI)=0.958, adjusted goodness-of-fit index (AGFI)=0.930, comparative fit index (CFI)=1.000, root mean square error of approximation (RMSEA)=0.000.

DISCUSSION

We found that the C-reactive protein (CRP) level on postoperative day 3 in patients with colorectal cancer (CRC) was significantly and positively correlated with the skeletal muscle index (SMI), whereas it was significantly and negatively correlated with the serum albumin (Alb) level. Additionally, the length of hospital stay (LOS) of patients with CRC was significantly and negatively correlated with vitality (VT). In terms of the interrelationship of baseline functional capacity parameters, 6-minute walk test (6MWT) findings were significantly and positively correlated with mental health (MH) and the latter was significantly and positively correlated with VT. Particularly among the baseline functional capacity parameters, Alb level was not only related to the postoperative course, but also significantly and positively related to the 6MWT findings. Therefore, for a good postoperative course in patients with CRC, it may be necessary to improve the baseline functional capacity using multimodal cancer prehabilitation.

Increased postoperative CRP levels reflect postoperative inflammatory responses, which may be due to tissue repair and infection prevention24). Similarly, postoperative CRP levels are associated with decreased T-lymphocyte function and development of hyperglycemia with protein catabolism24, 25). Therefore, the CRP level after surgery is a useful laboratory parameter for monitoring inflammatory reactions to surgical stress26), reaching the maximum value at 48 hours and fluctuating for the first 120 hours after surgery27). In a previous study, the postoperative day 3 CRP level was reported to be useful in predicting PCs in patients with CRC18). In consensus with the previous study18), the postoperative day 3 CRP level was significantly and positively correlated with PCs in patients with CRC in our study.

Protein is the energy source that normally drives the postoperative inflammatory response in the skeletal muscle and internal organs28). In previous studies, SMI and Alb, a protein in skeletal muscles and internal organs, have been reported as predictors of PCs in patients with CRC29, 30). As mentioned previously, preoperative SMI and Alb level were also significantly associated with postoperative day 3 CRP level in our study. Additionally, compared to those in healthy adults, the SMI and Alb level tend to decline in patients with CRC due to tumor metabolism31). Thus, cancer prehabilitation for patients with CRC should aim to improve or maintain the skeletal muscle mass and Nutrition status as expressed by Alb level before surgery by employing exercise and nutrition approaches in order to achieve a good postoperative course.

Importantly, the Alb level in patients with CRC was significantly and directly associated with the 6MWT findings and indirectly with VT and MH through the 6MWT findings. In a previous study, preoperative malnutrition in patients with CRC was associated not only with PCs29), but also physical and psychological function before surgery32). Malnutrition is an adaptive mechanism that leads to reduction of the basal metabolic rate and decrease in physical performance in an attempt to conserve nutrient reserves33). Additionally, in this study, walking capacity and the mental component summary of the SF-36 before surgery were related to the patient’s Nutrition status as expressed by Alb level and are important factors leading to a decreased health-related quality of life after discharge34, 35) and survival36) in patients with gastrointestinal cancer. Therefore, the preoperative Nutrition status as expressed by Alb level of patients with CRC should be cared for first to improve the preoperative physical and psychological status with cancer prehabilitation.

In previous studies, increasing the preoperative psychological function of patients with CRC through education significantly reduced LOS37, 38). As mentioned before, providing information related to CRC treatments before surgery may help increase VT related to inpatient treatment and reduce LOS. In this study, preoperative VT in patients with CRC was significantly and negatively correlated with LOS. Increasing preoperative VT in patients with CRC may lead to reduced LOS, similar to that seen in previous studies37, 38). Moreover, VT was influenced by the 6MWT findings, in addition to Alb levels. In a previous study, participation in a preoperative exercise program increased the SF-36 scores including those for VT before surgery in patients with CRC39). Therefore, to increase the VT in patients with CRC using cancer prehabilitation, programs should combine exercise and nutrition along with mental care.

This study has some limitations. First, the factor structure model of this study was based on the influence of baseline clinical characteristics. Although a wide range of patients with CRC were recruited in this three-institution cohort study, selection bias, especially for clinical stage IV of cancer, is conceivable. In future studies, the factor structure model of cancer prehabilitation should be reanalyzed using a propensity score calculated based on baseline demographics and clinical data. Second, a good postoperative course in patients with CRC is characterized by various factors showing a complex relationship. This study only collected data on CRP levels on postoperative day 3 as a representative parameter for the early postoperative immune response; however, a more detailed analysis of the perioperative care should be performed in the future. Third, this study did not perform cancer prehabilitation targeting patients with CRC. The true synergy and influence of each component, such as exercise, nutrition, and mental care, in cancer prehabilitation should be examined using randomized controlled trials and causal analysis.

In conclusion, this study provides a factor structure model needed for program design based on baseline functional capacity parameters, which can be evaluated before patients with CRC undergo cancer prehabilitation. Nutrition status as expressed by Alb level was the most important factor influencing the postoperative outcome and other baseline functional capacity parameters. This study provides a basis for designing a cancer prehabilitation program for patients with CRC in the future. However, this study did not include demographics and clinical data, except for age and sex. Due to the lack of rationale for the cancer prehabilitation program design among patients with CRC, this intervention must be considered from various perspectives in the future.

Funding

This study was funded by Grants-in-Aid for Scientific Research (Grant no. 19K19880) from the Japan Society for the Promotion of Science.

Conflict of interest

The authors declare that there is no conflict of interest regarding the publication of this article.

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