Fit for Surgery-feasibility of short-course multimodal individualized prehabilitation in high-risk frail colon cancer patients prior to surgery

R D Bojesen, L B Jørgensen, C Grube, S T Skou, C Johansen, S O Dalton, I Gögenur, R D Bojesen, L B Jørgensen, C Grube, S T Skou, C Johansen, S O Dalton, I Gögenur

Abstract

Background: Prehabilitation is a promising modality for improving patient-related outcomes after major surgery; however, very little research has been done for those who may need it the most: the elderly and the frail. This study aimed to investigate the feasibility of a short course multimodal prehabilitation prior to primary surgery in high-risk, frail patients with colorectal cancer and WHO performance status I and II.

Methods: The study was conducted as a single-center, prospective one-arm feasibility study of eight patients with colon cancer between October 4, 2018, and January 14, 2019. The intervention consisted of a physical training program tailored to the patients with both high-intensity interval training and resistance training three times a week in sessions of approximately 1 h in length, for a duration of at least 4 weeks, nutritional support with protein and vitamins, a consultation with a dietician, and medical optimization prior to surgery. Feasibility was evaluated regarding recruitment, retention, compliance and adherence, acceptability, and safety. Retention was evaluated as the number of patients that completed the intervention, with a feasibility goal of 75% completing the intervention. Compliance with the high-intensity training was evaluated as the number of sessions in which the patient achieved a minimum of 4 min > 90% of their maximum heart rate and adherence as the attended out of the offered training sessions.

Results: During the study period, 64 patients were screened for eligibility, and out of nine eligible patients, eight patients were included and seven completed the intervention (mean age 80, range 66-88). Compliance to the high-intensity interval training using 90% of maximum heart rate as the monitor of intensity was difficult to measure in several patients; however, adherence to the training sessions was 87%. Compliance with nutritional support was 57%. Half the patients felt somewhat overwhelmed by the multiple appointments and six out of seven reported difficulties with the dosage of protein.

Conclusions: This one-arm feasibility study indicates that multimodal prehabilitation including high-intensity interval training can be performed by patients with colorectal cancer and WHO performance status I and II.

Trial registration: Clinicaltrials.gov : the study current feasibility study was conducted prior to the initiation of a full ongoing randomized trial registered by NCT04167436; date of registration: November 18, 2019. Retrospectively registered. No separate prospectively registration of the feasibility trial was conducted but outlined by the approved study protocol (Danish Scientific Ethical Committee SJ-607).

Keywords: Colorectal cancer; Elderly; Frail; High-intensity training; Prehabilitation.

Conflict of interest statement

The authors report no conflict of interest and are alone responsible for the content of the paper.

© 2022. The Author(s).

Figures

Fig. 1
Fig. 1
Outline of the course of testing and intervention. Single asterisk indicates the following: all testing consisted of baseline questionnaires (G8 and fried frailty), nutritional screening (PG-SGA) and anthropometric measurement, blood work, cardiopulmonary exercise test (CPET), handgrip strength, leg extension strength test, 6-min walk test, sit to stand test (30 s), and stair climb test (30 s), in that exact chronological order. Double asterisk indicates the following: the intervention consisted of individual training three times a week with a minimum of 10 sessions. Nutritional counseling within the first week of inclusion (1.5 h), 0.4 g/kg bodyweight protein supplement two times a day, and medical optimization. Medical optimization was performed on the same day of baseline testing. Triple asterisk indicates the following: discharge managed through standardized discharge criteria. Adherence to Enhanced Recovery After Surgery (ERAS) was recorded each day during admission
Fig. 2
Fig. 2
CONSORT diagram of the inclusion process. APR, abdominoperineal resection. CRC, colorectal cancer. WHO, World Health Organization
Fig. 3
Fig. 3
a, b Examples of different issues within training sessions based on maximum heart rate. a Examples of training sessions with continuous measurement of heart rate and Borg’s RPE for three different patients. Horizontal lines represent the time within the interval spent above 90% of maximum heart rate (HR) within each interval. Patient 1 (red) represents the expected course of the HR during a training session. Patient 2 (blue) shows a training session where the HR did not decrease between high-intensity intervals. Patient 3 (orange) shows a patient with known paroxysmal atrial fibrillation, which is suspected to have atrial fibrillation during the training. HR was above 100% of the maximum HR completely during the session. HR during the last 4 min of training was not registered. b Illustrative example of a high-intensity interval training bout of a frail patient with colonic cancer without an expected decrease in heart rate between high intensive interval bouts. Similar to patient two (blue) in Fig. 2 a. The example was produced on Lode Corival rehab ergometer bike (Lode B.V., Groningen NL) on a patient not included in the feasibility study, in order to show the missing decrease in HR in correlation to intervals on a similar patient. The measure of Watt (green line), revolutions per minute (RPM (blue line)), heart rate (beats per minute, BPM (red line)), by time in minutes (x-axis). Oxygen saturation (SpO2) was not measured. The resting pulse of 75, increased rapidly after the start of the bout, even on 30% of maximum wattage defined by CPET, and reached maximum pulse within the first minute of exercise. The pulse did not decrease in low-intensity phases. CPET, cardiopulmonary exercise test. RPE, Borg’s Rating of Perceived exertion (RPE) 6-20 scale
Fig. 4
Fig. 4
Changes in VO2 peak, workload, and 6-min walk test at baseline, preoperative, and 4 weeks after surgery for each patient

References

    1. Ingeholm P, Iversen L, Krarup P-M, Roikjær O, Nielsen SE, Hagemann-Madsen RH, et al. DCCG Årsrapport. 2015:2015 Available from: .
    1. JL van V. Improving the outcomes in oncological colorectal surgery. World J Gastroenterol. 2014;20:12445.
    1. Manfredi S, Jooste V, Gay C, Faivre J, Drouillard A, Bouvier A-M. Time trends in colorectal cancer early postoperative mortality. A French 25-year population-based study. Int J Colorectal Dis. 2017;32:1725–1731.
    1. Hamaker ME, Prins MC, Schiphorst AH, van Tuyl SAC, Pronk A, van den Bos F. Long-term changes in physical capacity after colorectal cancer treatment. J Geriatr Oncol. 2015;6:153–164.
    1. Fagard K, Leonard S, Deschodt M, Devriendt E, Wolthuis A, Prenen H, et al. The impact of frailty on postoperative outcomes in individuals aged 65 and over undergoing elective surgery for colorectal cancer: a systematic review. J Geriatr Oncol. 2016;7:479–491.
    1. Mayo NE, Feldman L, Scott S, Zavorsky G, Kim DJ, Charlebois P, et al. Impact of preoperative change in physical function on postoperative recovery: argument supporting prehabilitation for colorectal surgery. Surgery. 2011;150:505–514.
    1. Hijazi Y, Gondal U, Aziz O. A systematic review of prehabilitation programs in abdominal cancer surgery. Int J Surg. 2017;39:156–162.
    1. Onerup A, Angenete E, Bonfre P, Börjesson M, Haglind E, Wessman C, et al. Self-assessed preoperative level of habitual physical activity predicted postoperative complications after colorectal cancer surgery: a prospective observational cohort study. Eur J Surg Oncol. 2019;45:2045–2051.
    1. Ommundsen N, Wyller TB, Nesbakken A, Bakka AO, Jordhøy MS, Skovlund E, et al. Preoperative geriatric assessment and tailored interventions in frail older patients with colorectal cancer: a randomized controlled trial. Color Dis. 2018;20:16–25.
    1. Partridge J, Sbai M, Dhesi J. Proactive care of older people undergoing surgery. Aging Clin Exp Res. 2018;30:253–257.
    1. Fowler AJ, Ahmad T, Phull MK, Allard S, Gillies MA, Pearse RM. Meta-analysis of the association between preoperative anaemia and mortality after surgery. Br J Surg. 2015;102:1314–1324.
    1. Mislang AR, Di Donato S, Hubbard J, Krishna L, Mottino G, Bozzetti F, et al. Nutritional management of older adults with gastrointestinal cancers: an International Society of Geriatric Oncology (SIOG) review paper. J Geriatr Oncol. 2018;9:382–392.
    1. van Rooijen S, Carli F, Dalton S, Thomas G, Bojesen R, Le Guen M, et al. Multimodal prehabilitation in colorectal cancer patients to improve functional capacity and reduce postoperative complications: the first international randomized controlled trial for multimodal prehabilitation. BMC Cancer. 2019;19:98.
    1. Hughes MJ, Hackney RJ, Lamb PJ, Wigmore SJ, Christopher Deans DA, Skipworth RJE. Prehabilitation before major abdominal surgery: a systematic review and meta-analysis. World J Surg. 2019;43:1661–1668.
    1. Bruns ERJ, van den Heuvel B, Buskens CJ, van Duijvendijk P, Festen S, Wassenaar EB, et al. The effects of physical prehabilitation in elderly patients undergoing colorectal surgery: a systematic review. Colorectal Dis. 2016;18:O267–O277.
    1. Daniels SL, Lee MJ, George J, Kerr K, Moug S, Wilson TR, et al. Prehabilitation in elective abdominal cancer surgery in older patients: systematic review and meta-analysis. BJS Open. 2020;4:1022–1041.
    1. Minnella EM, Bousquet-Dion G, Awasthi R, Scheede-Bergdahl C, Carli F. Multimodal prehabilitation improves functional capacity before and after colorectal surgery for cancer: a five-year research experience. Acta Oncol (Madr). 2017;56:295–300.
    1. Northgraves MJ, Arunachalam L, Madden LA, Marshall P, Hartley JE, MacFie J, et al. Feasibility of a novel exercise prehabilitation programme in patients scheduled for elective colorectal surgery: a feasibility randomised controlled trial. Support Care Cancer. 2020;28:3197–3206.
    1. Gillis C, Buhler K, Bresee L, Carli F, Gramlich L, Culos-Reed N, et al. Effects of nutritional prehabilitation, with and without exercise, on outcomes of patients who undergo colorectal surgery: a systematic review and meta-analysis. Gastroenterology. 2018;155:391–410.e4.
    1. Moran J, Wilson F, Guinan E, McCormick P, Hussey J, Moriarty J. Role of cardiopulmonary exercise testing as a risk-assessment method in patients undergoing intra-abdominal surgery: a systematic review. Br J Anaesth. 2016;116:177–191.
    1. Steffens D, Ismail H, Denehy L, Beckenkamp PR, Solomon M, Koh C, et al. Preoperative cardiopulmonary exercise test associated with postoperative outcomes in patients undergoing cancer surgery: a systematic review and meta-analyses. Ann Surg Oncol. 2021;28:7120–7146.
    1. Ito S, Mizoguchi T, Saeki T. Review of high-intensity interval training in cardiac rehabilitation. Intern Med. 2016;55:2329–2336.
    1. Milanović Z, Sporiš G, Weston M. Effectiveness of high-intensity interval training (HIT) and continuous endurance training for VO2max improvements: a systematic review and meta-analysis of controlled trials. Sport Med. 2015;45:1469–1481.
    1. Carli F, Bousquet-Dion G, Awasthi R, Elsherbini N, Liberman S, Boutros M, et al. Effect of multimodal prehabilitation vs postoperative rehabilitation on 30-day postoperative complications for frail patients undergoing resection of colorectal cancer. JAMA Surg. 2020;155:233.
    1. Scott MJ, Baldini G, Fearon KCH, Feldheiser A, Feldman LS, Gan TJ, et al. Enhanced Recovery After Surgery (ERAS) for gastrointestinal surgery, part 1: pathophysiological considerations. Acta Anaesthesiol Scand. 2015;59:1212–1231.
    1. Feldheiser A, Aziz O, Baldini G, Cox BPBW, Fearon KCH, Feldman LS, et al. Enhanced Recovery After Surgery (ERAS) for gastrointestinal surgery, part 2: consensus statement for anaesthesia practice. Acta Anaesthesiol Scand. 2016;60:289–334.
    1. Crum RM. Population-based norms for the mini-mental state examination by age and educational level. JAMA J Am Med Assoc. 1993;269:2386.
    1. Taylor AE, Olver IN, Sivanthan T, Chi M, Purnell C. Observer error in grading performance status in cancer patients. Support Care Cancer. 1999;7:332–335.
    1. Blagden SP, Charman SC, Sharples LD, Magee LRA, Gilligan D. Performance status score: do patients and their oncologists agree? Br J Cancer. 2003;89:1022–1027.
    1. Bojesen RD, Degett TH, Dalton SO, Gögenur I. High World Health Organization performance status is associated with short- and long-term outcomes after colorectal cancer surgery: a nationwide population-based study. Dis Colon Rectum. 2021;64:851–860.
    1. Scherr J, Wolfarth B, Christle JW, Pressler A, Wagenpfeil S, Halle M. Associations between Borg’s rating of perceived exertion and physiological measures of exercise intensity. Eur J Appl Physiol. 2013;113:147–155.
    1. Taylor JD, Fletcher JP. Reliability of the 8-repetition maximum test in men and women. J Sci Med Sport. 2012;15:69–73.
    1. Frankenfield DC, Muth ER, Rowe WA. The Harris-Benedict studies of human basal metabolism. J Am Diet Assoc. 1998;98:439–445.
    1. Slade SC, Dionne CE, Underwood M, Buchbinder R. Consensus on exercise reporting template (CERT): explanation and elaboration statement. Br J Sports Med. 2016;50:1428–1437.
    1. Kollock RO, Onate JA, Van Lunen B. The reliability of portable fixed dynamometry during hip and knee strength assessments. J Athl Train. 2010;45:349–356.
    1. Bohannon RW, Bubela DJ, Magasi SR, Wang Y-C, Gershon RC. Sit-to-stand test: performance and determinants across the age-span. Isokinet Exerc Sci. 2010;18:235–240.
    1. Jones CJ, Rikli RE, Beam WC. A 30-s chair-stand test as a measure of lower body strength in community-residing older adults. Res Q Exerc Sport. 1999;70:113–119.
    1. Brzycki M. Strength testing—predicting a one-rep max from reps-to-fatigue. J Phys Educ Recreat Danc. 1993;64:88–90.
    1. Bauer J, Capra S, Ferguson M. Use of the scored Patient-Generated Subjective Global Assessment (PG-SGA) as a nutrition assessment tool in patients with cancer. Eur J Clin Nutr. 2002;56:779–785.
    1. Fried LP, Tangen CM, Walston J, Newman AB, Hirsch C, Gottdiener J, et al. Frailty in older adults: evidence for a phenotype. J Gerontol Ser A Biol Sci Med Sci. 2001;56:M146–M157.
    1. Charlson ME, Pompei P, Ales KL, MacKenzie CR. A new method of classifying prognostic comorbidity in longitudinal studies: development and validation. J Chronic Dis. 1987;40:373–383.
    1. Xue Q-L. The frailty syndrome: definition and natural history. Clin Geriatr Med. 2011;27:1–15.
    1. Takahashi M, Takahashi M, Komine K, Yamada H, Kasahara Y, Chikamatsu S, et al. The G8 screening tool enhances prognostic value to ECOG performance status in elderly cancer patients: a retrospective, single institutional study. PLoS One. 2017;12:e0179694.
    1. Rose GA, Davies RG, Davison GW, Adams RA, Williams IM, Lewis MH, et al. The cardiopulmonary exercise test grey zone; optimising fitness stratification by application of critical difference. Br J Anaesth. 2018;120:1187–1194.
    1. Dindo D, Demartines N, Clavien P-A. Classification of surgical complications: a new proposal with evaluation in a cohort of 6336 patients and results of a survey. Ann Surg. 2004;240:205–213.
    1. Slankamenac K, Nederlof N, Pessaux P, de Jonge J, Wijnhoven BPL, Breitenstein S, et al. The Comprehensive Complication Index: a novel and more sensitive endpoint for assessing outcome and reducing sample size in randomized controlled trials. Ann Surg. 2014;260:757–763.
    1. Bell M, Eriksson LI, Svensson T, Hallqvist L, Granath F, Reilly J, et al. Days at home after surgery: an integrated and efficient outcome measure for clinical trials and quality assurance. EClinicalMedicine. 2019;11:18–26.
    1. Eldridge SM, Chan CL, Campbell MJ, Bond CM, Hopewell S, Thabane L, et al. CONSORT 2010 statement: extension to randomised pilot and feasibility trials. BMJ. 2016;355:i5239.
    1. Ellingsen Ø, Halle M, Conraads V, Støylen A, Dalen H, Delagardelle C, et al. High-intensity interval training in patients with heart failure with reduced ejection fraction. Circulation. 2017;135:839–849.
    1. Støren Ø, Helgerud J, Sæbø M, Støa EM, Bratland-Sanda S, Unhjem RJ, et al. The effect of age on the V˙O2max response to high-intensity interval training. Med Sci Sport Exerc. 2017;49:78–85.
    1. Licker M, Karenovics W, Diaper J, Frésard I, Triponez F, Ellenberger C, et al. Short-term preoperative high-intensity interval training in patients awaiting lung cancer surgery: a randomized controlled trial. J Thorac Oncol. 2017;12:323–333.
    1. Jones LW, Peddle CJ, Eves ND, Haykowsky MJ, Courneya KS, Mackey JR, et al. Effects of presurgical exercise training on cardiorespiratory fitness among patients undergoing thoracic surgery for malignant lung lesions. Cancer. 2007;110:590–598.
    1. Boereboom CL, Phillips BE, Williams JP, Lund JN. A 31-day time to surgery compliant exercise training programme improves aerobic health in the elderly. Tech Coloproctol. 2016;20:375–382.

Source: PubMed

3
订阅