Effects of a yoga-based stress reduction intervention on stress, psychological outcomes and cardiometabolic biomarkers in cancer caregivers: A randomized controlled trial

Lena J Lee, Robert Shamburek, Hyojin Son, Gwenyth R Wallen, Robert Cox, Sharon Flynn, Li Yang, Margaret Bevans, Leslie Wehrlen, Alyson Ross, Lena J Lee, Robert Shamburek, Hyojin Son, Gwenyth R Wallen, Robert Cox, Sharon Flynn, Li Yang, Margaret Bevans, Leslie Wehrlen, Alyson Ross

Abstract

Caregiving stress is a risk factor for cardiometabolic disease. Therefore, integrating cardiometabolic biomarkers into caregiving research provides a more comprehensive assessment of an individual's health and response to an intervention. The objective of this study was to examine the effects of a yoga-based stress reduction intervention on stress, psychological outcomes, and cardiometabolic biomarkers in cancer caregivers. This prospective randomized controlled trial enrolled family caregivers of adult patients who underwent an allogeneic HSCT at the National Institutes of Health (NIH) Clinical Center. All subjects received usual care education. Participants in the intervention group received an Iyengar yoga intervention self-administered over six weeks using an audio recording file. The primary outcome was perceived stress (measured using the NIH toolbox Perceived Stress). The secondary outcomes were psychological factors (depression and anxiety measured using PROMIS® Depression and Anxiety), and cardiometabolic biomarkers measured by nuclear magnetic resonance spectroscopy. A total of 50 family caregivers (mean [SD] age, 44.9 [15.2] years; 42 [84.0%] women) were randomized, 25 to the intervention group and 25 to the control group. No group differences were noted in stress, depression, and anxiety. Significant interaction effects between group and time were found in large TRL-P (F(1,43) = 10.16, p = 0.003) and LP-IR (F(1,42) = 4.28, p = 0.045). Post-hoc analyses revealed that the levels of large TRL-P (mean difference = 1.68, CI = [0.86, 2.51], p< .001) and LP-IR (mean difference = 5.67, CI = [1.15, 10.18], p = 0.015) significantly increased over time in the control group but while remained stable in the intervention group (mean difference = -0.15, CI = [-0.96, 0.66], p = 0.718; mean difference = -0.81, CI = [-5.22, 3.61], p = 0.714, respectively). Even when perceptions of psychological distress remain unchanged, incorporating gentle yoga poses and breathing exercises may reduce the risk of cardiometabolic disease in caregivers by inhibiting the development of insulin resistance. Standard lipids of cardiometabolic risk do not appear to be robust enough to detect short-term early changes of cardiometabolic risk in caregivers. Trial registration: ClinicalTrials.gov Identifier: NCT02257853.

Conflict of interest statement

The authors have declared that no competing interests exist.

Copyright: This is an open access article, free of all copyright, and may be freely reproduced, distributed, transmitted, modified, built upon, or otherwise used by anyone for any lawful purpose. The work is made available under the Creative Commons CC0 public domain dedication.

Figures

Fig 1. Consolidate Standards of Reporting Trials…
Fig 1. Consolidate Standards of Reporting Trials (CONSORT) flow diagram.
Fig 2. Mean cardiometabolic biomarkers levels over…
Fig 2. Mean cardiometabolic biomarkers levels over time for the intervention and control groups.
a. Predicted large TRL-p overtime. Post-hoc analyses showed significant differences between baseline and 6 weeks for control group only (p < 0.001). b. Predicted LP-IR over time. Post-hoc analyses showed significant differences between baseline and 6 weeks for control group only (p = 0.015).

References

    1. National Alliance for Caregiving. Caregiving in the U.S. 2020. .
    1. National Alliance for Caregiving. Cancer Caregiving in the U.S.: An intense, episodic, and challenging care experience.
    1. Arnaout K, Patel N, Jain M, El-Amm J, Amro F, Tabbara IA. Complications of allogeneic hematopoietic stem cell transplantation. Cancer Invest. 2014;32: 349–362. doi: 10.3109/07357907.2014.919301
    1. Applebaum AJ, Bevans M, Son T, Evans K, Hernandez M, Giralt S, et al.. A scoping review of caregiver burden during allogeneic HSCT: lessons learned and future directions. Bone Marrow Transplant. 2016;51(11): 1416–1422. doi: 10.1038/bmt.2016.164
    1. Xie L, Shen C, Shi Y, Li H. Caregiver burden among primary family caregivers of patients undergoing HSCT: a cross-sectional study from Suzhou, China. Cancer Nurs. 2021;44(6): E556–E566.
    1. Gupta V, Raj M, Hoodin F, Yahng L, Braun T, Choi SW. Electronic health record portal use by family caregivers of patients undergoing HSCT: United States national survey study. JMIR Cancer. 2021;7(1): e26509.
    1. Ravyts SG, Sannes TS, Dzierzewski JM, Zhou ES, Brewer BW, Natvig C, et al.. Check your sleep before you start: a secondary analysis of a stress management intervention for caregivers of stem cell transplant patients. Psychooncology. 2021;30(6): 936–945. doi: 10.1002/pon.5680
    1. Ahn S, Esquivel JH, Davis EM, Logan JG, Chung ML. Cardiovascular disease incidence and risk in family caregivers of adults with chronic conditions: a systematic review. J Cardiovasc Nurs. 2022;37(3): E47–E60. doi: 10.1097/JCN.0000000000000816
    1. Kim Y, Carver CS, Shaffer KM, Gansler T, Cannady RS. Cancer caregiving predicts physical impairments: roles of earlier caregiving stress and being a spousal caregiver. Cancer. 2015;121(2): 302–310. doi: 10.1002/cncr.29040
    1. Lee LJ, Kim Y, Shamburek R, Ross A, Yang L, Bevans MF. Caregiving stress and burden associated with cardiometabolic risk in family caregivers of individuals with cancer. Stress. 2022;25(1): 258–266. doi: 10.1080/10253890.2022.2037548
    1. Steel JL, Cheng H, Pathak R, Wang Y, Miceli J, Hecht CL, et al.. Psychosocial and behavioral pathways of metabolic syndrome in cancer caregivers. Psychooncology. 2019;28(8): 1735–1742. doi: 10.1002/pon.5147
    1. Johns SA, Beck-Coon K, Stutz PV, Talib TL, Chinh K, Cottingham AH, et al.. Mindfulness training supports quality of life and advance care planning in adults with metastatic cancer and their caregivers: results of a pilot study. Am J Hosp Palliat Care. 2020;37(2): 88–99. doi: 10.1177/1049909119862254
    1. Schellekens MPJ, van den Hurk DGM, Prins JB, Donders ART, Molema J, Dekhuijzen R, et al.. Mindfulness-based stress reduction added to care as usual for lung cancer patients and/or their partners: a multicentre randomized controlled trial. Psychooncology. 2017;26(12): 2118–2126. doi: 10.1002/pon.4430
    1. Milbury K, Li J, Weathers S-P, Mallaiah S, Armstrong T, Li Y, et al.. Pilot randomized, controlled trial of a dyadic yoga program for glioma patients undergoing radiotherapy and their family caregivers. Neurooncol Pract. 2019;6(4): 311–320. doi: 10.1093/nop/npy052
    1. Vinci C, Pidala J, Lau P, Reblin M, Jim H. A mindfulness-based intervention for caregivers of allogeneic hematopoietic stem cell transplant patients: pilot results. Psychooncology. 2020;29(5): 934–937. doi: 10.1002/pon.5353
    1. Park J, Ross A, Klagholz SD, Bevans MF. The role of biomarkers in research on caregivers of cancer patients: a scoping review. Biol Res Nurs. 2018;20(3): 300–311.
    1. Franke DDH, Connelly MA. Chapter 11—Nuclear magnetic resonance technology and clinical applications. In: Clarke W, Marzinke MA, editors. Contemporary practice in clinical chemistry. 4th ed. Academic Press; 2020. pp. 187–200.
    1. Otvos JD, Mora S, Shalaurova I, Greenland P, Mackey RH, Goff DC Jr. Clinical implications of discordance between low-density lipoprotein cholesterol and particle number. J Clin Lipidol. 2011;5(2): 105–113. doi: 10.1016/j.jacl.2011.02.001
    1. Matyus SP, Braun PJ, Wolak-Dinsmore J, Jeyarajah EJ, Shalaurova I, Xu Y, et al.. NMR measurement of LDL particle using the Vantera Clinical Analyzer. Clin Biochem. 2014;47(16–17): 203–210.
    1. Urbina EM, McCoy CE, Gao Z, Khoury PR, Shah AS, Dolan LM, et al.. Lipoprotein particle number and size predict vascular structure and function better than traditional lipids in adolescent and young adults. J Clin Lipidol, 2017;11(4): 1023–1031.
    1. Ross A, Shamburek R, Wehrlen L, Klagholz SD, Yang L, Stoops E, et al.. Cardiometabolic risk factors and health behaviors in family caregivers. PLoS One. 2017;12(5): e0176408. doi: 10.1371/journal.pone.0176408
    1. Ross A, Lee LJ, Wehrlen L, Cox R, Yang L, Perez A, et al.. Factors that influence health-promoting behaviors in cancer caregivers. Oncol Nurs Forum, 2020;47(6): 692–702. doi: 10.1188/20.ONF.692-702
    1. Mochari-Greenberger H, Mosca L. Caregiver burden and nonachievement of health lifestyle behaviors among family caregivers of cardiovascular disease patients. Am J Health Promot. 2012;27(2): 84–89.
    1. Sisk RJ. Caregiver burden and health promotion. Int J Nurs Stud. 2000;37(1): 37–43. doi: 10.1016/s0020-7489(99)00053-x
    1. Cramer H, Ward L, Saper R, Fishbein D, Dobos G, Lauche R. The safety of yoga: a systematic review and meta-analysis of randomized controlled trials. Am J Epidemiol. 2015;182(4): 281–293. doi: 10.1093/aje/kwv071
    1. Cohen S, Janicki‐Deverts D. Who’s stressed? Distributions of psychological stress in the United States in probability samples from 1983, 2006, and 2009. J Appl Soc Psychol. 2012;42(6): 1320–1334.
    1. Gershon RC, Wagster MV, Hendrie HC, Fox NA, Cook KF, Nowinski CJ. NIH toolbox for assessment of neurological and behavioral function. Neurology. 2013;80(11 Suppl 3):S2–S6. doi: 10.1212/WNL.0b013e3182872e5f
    1. Cella D, Riley W, Stone A, Rothrock N, Reeve B, Yount S, et al.. The Patient-Reported Outcomes Measurement Information System (PROMIS) developed and tested its first wave of adult self-reported health outcome item banks: 2005–2008. J Clin Epidemiol. 2010;63(11): 1179–1194. doi: 10.1016/j.jclinepi.2010.04.011
    1. Bevans MF, Ross A, Wehrlen L, Klagholz SD, Yang L, Childs R, et al.. Documenting stress in caregivers of transplantation patients: initial evidence of HPA dysregulation. 2016;19(2): 175–184.
    1. Fitzmaurice GM, Laird NM, Ware JH. Applied longitudinal analysis. 2nd Edition. John Wiley & Sons; 2011. Chapter 20, Sample size and power for longitudinal studies; p. 581–609.
    1. Bernardi MLD, Amorim MHC, Salaroli LB, Zandonade E. Effects of Hatha Yoga on caregivers of children and adolescents with cancer: a randomized controlled trial. Esc Anna Nery. 2019;24(1): e20190133.
    1. Cheung DSK, Kor PPK, Jones C, Davies N, Moyle W, Chien WT, et al.. The use of modified mindfulness-based stress reduction and mindfulness-based cognitive therapy program for family caregivers of people living with dementia: a feasibility study. Asian Nurs Res (Korean Soc Nurs Sci). 2020;14(4): 221–230. doi: 10.1016/j.anr.2020.08.009
    1. Danucalov MAD, Kozasa EH, Ribas KT, Galduróz JCF, Garcia MC, Verreschi ITN, et al.. A yoga and compassion meditation program reduces stress in familial caregivers of Alzheimer’s disease patients. Evid Based Complement Alternat Med. 2013;2013: 513149. doi: 10.1155/2013/513149
    1. Varambally S, Vidyendaran S, Sajjanar M, Thirthalli J, Hamza A, Nagendra HR, et al.. Yoga-based intervention for caregivers of outpatients with psychosis: a randomized controlled pilot study. Asian J Psychiatr. 2013;6(2): 141–145. doi: 10.1016/j.ajp.2012.09.017
    1. Butzer B, LoRusso A, Shin SH, Khalsa SBS. Evaluation of yoga for preventing adolescent substance use risk factors in a middle school setting: a preliminary group-randomized controlled trial. J Youth Adolesc. 2017;46(3): 603–632. doi: 10.1007/s10964-016-0513-3
    1. Chong CSM, Tsunaka M, Tsang HWH, Chan EP, Cheung WM. Effects of yoga on stress management in healthy adults: a systematic review. Altern Ther Health Med. 2011;17(1): 32–38.
    1. Wang F, Szabo A. Effects of yoga on stress among healthy adults: a systematic review. Altern Ther Health Med. 2020;26(4): AT6214.
    1. Adeva-Andany MM, Martínez-Rodríguez J, González-Lucán M, Fernández-Fernández C, Castro-Quintela E. Insulin resistance is a cardiovascular risk factor in humans. Diabetes Metab Syndr. 2019;13(2): 1449–1455. doi: 10.1016/j.dsx.2019.02.023
    1. Schmiegelow MD, Hedlin H, Stefanick ML, Mackey RH, Allison M, Martin LW, et al.. Insulin resistance and risk of cardiovascular disease in postmenopausal women: a cohort study from the Women’s Health Initiative. Circ Cardiovasc Qual Outcomes. 2015;8(3): 309–316. doi: 10.1161/CIRCOUTCOMES.114.001563
    1. Thacker EL, Psaty BM, McKnight B, Heckbert SR, Longstreth WT Jr, Mukamal KJ, et al.. Fasting and post-glucose load measures of insulin resistance and risk of ischemic stroke in older adults. Stroke. 2011;42(12): 3347–3351. doi: 10.1161/STROKEAHA.111.620773
    1. Garvey WT, Kwon S, Zheng D, Shaughnessy S, Wallace P, Hutto A, et al.. Effects of insulin resistance and type 2 diabetes on lipoprotein subclass particle size and concentration determined by nuclear magnetic resonance. Diabetes. 2003;52(2): 453–462. doi: 10.2337/diabetes.52.2.453
    1. Goff DC Jr, D’Agostino RB Jr, Haffner SM, Otvos JD. Insulin resistance and adiposity influence lipoprotein size and subclass concentrations. Results from the Insulin Resistance Atherosclerosis Study. Metabolism. 2005;54(2): 264–270. doi: 10.1016/j.metabol.2004.09.002
    1. Goldberg IJ. Clinical review 124: Diabetic dyslipidemia: causes and consequences. J Clin Endocrinol Metab. 2001;86(3): 965–971. doi: 10.1210/jcem.86.3.7304
    1. Peckett AJ, Wright DC, Riddell MC. The effects of glucocorticoids on adipose tissue lipid metabolism. Metabolism. 2011;60(11): 1500–1510. doi: 10.1016/j.metabol.2011.06.012
    1. Harada PHN, Demler OV, Dugani SB, Akinkuolie AO, Moorthy MV, Ridker PM, et al.. Lipoprotein insulin resistance score and risk of incident diabetes during extended follow-up of 20 years: The Women’s Health Study. J Clin Lipidol. 2017;11(5): 1257–1267. doi: 10.1016/j.jacl.2017.06.008
    1. Flores-Guerrero JL, Connelly MA, Shalaurova I, Gruppen EG, Kieneker LM, Dullaart RPF, et al.. Lipoprotein insulin resistance index, a high-throughput measure of insulin resistance, is associated with incident type II diabetes mellitus in the Prevention of Renal and Vascular End-Stage Disease study. J Clin Lipidol. 2019;13(1): 129–137.e1. doi: 10.1016/j.jacl.2018.11.009
    1. Flores-Guerrero JL, Gruppen EG, Connelly MA, Shalaurova I, Otvos JD, Garcia E, et al.. A newly developed diabetes risk index, based on lipoprotein subfractions and branched chain amino acids, is associated with incident type 2 diabetes mellitus in the PREVEND Cohort. J Clin Med. 2020;9(9): 2781. doi: 10.3390/jcm9092781
    1. Ellsworth DL, Costantino NS, Blackburn HL, Engler RJM, Kashani M, Vernalis MN. Lifestyle modification interventions differing in intensity and dietary stringency improve insulin resistance through changes in lipoprotein profiles. Obes Sci Pract. 2016;2(3): 282–292. doi: 10.1002/osp4.54
    1. Ross LM, Slentz CA, Zidek AM, Huffman KM, Shalaurova I, Otvos JD, et al.. Effects of amount, intensity, and mode of exercise training on insulin resistance and type 2 diabetes risk in the STRRIDE randomized trials. Front Physiol. 2021;12: 626142. doi: 10.3389/fphys.2021.626142

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