Abstract
Background
We aimed to study adherence to cardiac screening in long-term childhood cancer survivors (CCS) at high risk of cardiomyopathy.
Methods
This study involved 976 5-year CCS at high risk for cardiomyopathy from the French Childhood Cancer Survivor Study. Determinants of adherence to recommended surveillance were studied using multivariable logistic regression models. Association of attendance to a long-term follow-up (LTFU) visit with completion of an echocardiogram was estimated using a Cox regression model.
Results
Among participants, 32% had an echocardiogram within the 5 previous years. Males (adjusted RR [aRR] 0.71, 95% CI 0.58–0.86), survivors aged 36–49 (aRR 0.79, 95% CI 0.64–0.98), Neuroblastoma (aRR 0.53, 95% CI 0.30–0.91) and CNS tumour survivors (aRR 0.43, 95% CI 0.21–0.89) were less likely to adhere to recommended surveillance. Attendance to an LTFU visit was associated with completion of an echocardiogram in patients who were not previously adherent to recommendations (HR 8.20, 95% CI 5.64–11.93).
Conclusions
The majority of long-term survivors at high risk of cardiomyopathy did not adhere to the recommended surveillance. Attendance to an LTFU visit greatly enhanced the completion of echocardiograms, but further interventions need to be developed to reach more survivors.
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Data availability
The datasets used and/or analyzed during the current study are available from the corresponding author on reasonable request.
References
Kaatsch P. Epidemiology of childhood cancer. Cancer Treat Rev. 2010;36:277–85.
Hudson MM, Ness KK, Gurney JG, Mulrooney DA, Chemaitilly W, Krull KR, et al. Clinical ascertainment of health outcomes among adults treated for childhood cancer. J Am Med Assoc. 2013;309:2371–81.
Tukenova M, Guibout C, Oberlin O, Doyon F, Mousannif A, Haddy N, et al. Role of cancer treatment in long-term overall and cardiovascular mortality after childhood cancer. J Clin Oncol. 2010;28:1308–15.
Lipshultz SE, Adams MJ, Colan SD, Constine LS, Herman EH, Hsu DT, et al. Long-term cardiovascular toxicity in children, adolescents, and young adults who receive cancer therapy: pathophysiology, course, monitoring, management, prevention, and research directions: a scientific statement from the American Heart Association. Circulation. 2013;128:1927–95.
Cardinale D, Colombo A, Lamantia G, Colombo N, Civelli M, De Giacomi G, et al. Anthracycline-induced cardiomyopathy: clinical relevance and response to pharmacologic therapy. J Am Coll Cardiol. 2010;55:213–20.
Yeh ETH, Tong AT, Lenihan DJ, Yusuf SW, Swafford J, Champion C, et al. Cardiovascular complications of cancer therapy: diagnosis, pathogenesis, and management. Circulation. 2004;109:3122–31.
Mansouri I, Allodji RS, Hill C, El-Fayech C, Pein F, Diallo S, et al. The role of irradiated heart and left ventricular volumes in heart failure occurrence after childhood cancer. Eur J Heart Fail. 2019;21:509–18.
Armenian SH, Hudson MM, Mulder RL, Chen MH, Constine LS, Dwyer M, et al. Recommendations for cardiomyopathy surveillance for survivors of childhood cancer: a report from the International Late Effects of Childhood Cancer Guideline Harmonization Group. Lancet Oncol. 2015;16:e123–136.
Children’s Oncology Group [Internet]. [cited 2021 Jul 13]. Available from: http://www.survivorshipguidelines.org/.
Sieswerda E, Postma A, van Dalen EC, van der Pal HJ, Tissing WJ, Rammeloo LA, et al. The Dutch Childhood Oncology Group guideline for follow-up of asymptomatic cardiac dysfunction in childhood cancer survivors. Ann Oncol. 2012;23:2191–8.
Wallace WHB, Thompson L, Anderson RA. Long term follow-up of survivors of childhood cancer: summary of updated SIGN guidance. BMJ. 2013;346:f1190.
Nathan PC, Greenberg ML, Ness KK, Hudson MM, Mertens AC, Mahoney MC, et al. Medical care in long-term survivors of childhood cancer: a report from the childhood cancer survivor study. J Clin Oncol. 2008;26:4401–9.
Marr KC, Agha M, Sutradhar R, Pole JD, Hodgson D, Guttmann A, et al. Specialized survivor clinic attendance increases adherence to cardiomyopathy screening guidelines in adult survivors of childhood cancer. J Cancer Surviv Res Pract. 2017;11:614–23.
Hawkins M, Bhatia S, Henderson TO, Nathan PC, Yan A, Teepen JC, et al. Subsequent primary neoplasms: risks, risk factors, surveillance, and future research. Pediatr Clin North Am. 2020;67:1135–54.
Zabih V, Kahane A, O’Neill NE, Ivers N, Nathan PC. Interventions to improve adherence to surveillance guidelines in survivors of childhood cancer: a systematic review. J Cancer Surviv Res Pract. 2019;13:713–29.
Hudson MM, Leisenring W, Stratton KK, Tinner N, Steen BD, Ogg S, et al. Increasing cardiomyopathy screening in at-risk adult survivors of pediatric malignancies: a randomized controlled trial. J Clin Oncol. 2014;32:3974–81.
Demoor-Goldschmidt C, Allodji RS, Journy N, Rubino C, Zrafi WS, Debiche G, et al. Risk factors for small adult height in childhood cancer survivors. J Clin Oncol. 2020;38:1785–96.
Bezin J, Duong M, Lassalle R, Droz C, Pariente A, Blin P, et al. The national healthcare system claims databases in France, SNIIRAM and EGB: powerful tools for pharmacoepidemiology. Pharmacoepidemiol Drug Saf. 2017;26:954–62.
Rey G, Jougla E, Fouillet A, Hémon D. Ecological association between a deprivation index and mortality in France over the period 1997 - 2001: variations with spatial scale, degree of urbanicity, age, gender and cause of death. BMC Public Health. 2009;9:33.
Zou G. A modified Poisson regression approach to prospective binary data. Am J Epidemiol. 2004;159:702–6.
Knol MJ, Le Cessie S, Algra A, Vandenbroucke JP, Groenwold RHH. Overestimation of risk ratios by odds ratios in trials and cohort studies: alternatives to logistic regression. Can Med Assoc J. 2012;184:895–9.
Cox CL, Hudson MM, Mertens A, Oeffinger K, Whitton J, Montgomery M, et al. Medical screening participation among childhood cancer survivors. Arch Intern Med. 2009;169:454–62.
Steele JR, Wall M, Salkowski N, Mitby P, Kawashima T, Yeazel MW, et al. Predictors of risk-based medical follow-up: a report from the childhood cancer survivor study. J Cancer Surviv Res Pract. 2013;7:379–91.
Dumas A. Gender inequalities in health over the life course. Attitudes towards III-health in men and women treated for childhood cancer. Swiss J Sociol. 2018;44:281–300.
Courtenay WH. Constructions of masculinity and their influence on men’s well-being: a theory of gender and health. Soc Sci Med. 2000;50:1385–401.
Laverdière C, Liu Q, Yasui Y, Nathan PC, Gurney JG, Stovall M, et al. Long-term outcomes in survivors of neuroblastoma: a report from the Childhood Cancer Survivor Study. J Natl Cancer Inst. 2009;101:1131–40.
Gunn ME, Lähdesmäki T, Malila N, Arola M, Grönroos M, Matomäki J, et al. Late morbidity in long-term survivors of childhood brain tumors: a nationwide registry-based study in Finland. Neuro-Oncol. 2015;17:747–56.
Zebrack BJ, Eshelman DA, Hudson MM, Mertens AC, Cotter KL, Foster BM, et al. Health care for childhood cancer survivors: insights and perspectives from a Delphi panel of young adult survivors of childhood cancer. Cancer. 2004;100:843–50.
Howard AF, Goddard K, Tan de Bibiana J, Pritchard S, Olson R, Kazanjian A. Adult childhood cancer survivors’ narratives of managing their health: the unexpected and the unresolved. J Cancer Surviv Res Pract. 2016;10:711–25.
Baxstrom K, Peterson BA, Lee C, Vogel RI, Blaes AH. A pilot investigation on impact of participation in a long-term follow-up clinic (LTFU) on breast cancer and cardiovascular screening among women who received chest radiation for Hodgkin lymphoma. Support Care Cancer. 2018;26:2361–8.
Dumas A, Milcent K, Bougas N, Bejarano-Quisoboni D, El Fayech C, Charreire H, et al. Predictive factors of long-term follow-up attendance in very long-term childhood cancer survivors. Cancer. 2023;
Jabson JM. Treatment summaries, follow-up care instructions, and patient navigation: could they be combined to improve cancer survivor’s receipt of follow-up care? J Cancer Surviv Res Pract. 2015;9:692–8.
Edgar AB, Borthwick S, Duffin K, Marciniak-Stepak P, Wallace WHB. Survivors of childhood cancer lost to follow-up can be re-engaged into active long-term follow-up by a postal health questionnaire intervention. Eur J Cancer. 2012;48:1066–73.
Oeffinger KC, Hudson MM, Mertens AC, Smith SM, Mitby PA, Eshelman-Kent DA, et al. Increasing rates of breast cancer and cardiac surveillance among high risk survivors of childhood Hodgkin lymphoma following a mailed, one-page survivorship care plan. Pediatr Blood Cancer. 2011;56:818–24.
Kadan-Lottick NS, Ross WL, Mitchell HR, Rotatori J, Gross CP, Ma X. Randomized trial of the impact of empowering childhood cancer survivors with survivorship care plans. J Natl Cancer Inst. 2018;110:1352–9.
Landier W, Bhatia S. Cancer survivorship: a pediatric perspective. The Oncologist. 2008;13:1181–92.
Nathan PC, Daugherty CK, Wroblewski KE, Kigin ML, Stewart TV, Hlubocky FJ, et al. Family physician preferences and knowledge gaps regarding the care of adolescent and young adult survivors of childhood cancer. J Cancer Surviv Res Pract. 2013;7:275–82.
Klosky JL, Cash DK, Buscemi J, Lensing S, Garces-Webb DM, Zhao W, et al. Factors influencing long-term follow-up clinic attendance among survivors of childhood cancer. J Cancer Surviv Res Pract. 2008;2:225–32.
Oeffinger KC, Ford JS, Moskowitz CS, Diller LR, Hudson MM, Chou JF, et al. Breast cancer surveillance practices among women previously treated with chest radiation for a childhood cancer. J Am Med Assoc. 2009;301:404–14.
Austin PC, Stuart EA. Moving towards best practice when using inverse probability of treatment weighting (IPTW) using the propensity score to estimate causal treatment effects in observational studies. Stat Med. 2015;34:3661–79.
Acknowledgements
We thank the patients and all the clinicians and research staff who participated in the study. We are grateful to Carole Rubino, Odile Oberlin, Amel Boumaraf, Amel Belhout and Isao Kobayashi for their contribution to this work.
Funding
This work was supported by the INCa/ARC foundation (CHART project). The FCCSS cohort is supported and funded by the French Society of Cancer in Children and Adolescents (SFCE), the Gustave Roussy Foundation (Pediatric Program “Guérir le Cancer de l’Enfant”), the Foundation ARC (POPHarC program) and The French National Research Agency (ANR, HOPE-EPI project), the ‘Ligue Nationale Contre le Cancer’, and the ‘Programme Hospitalier de Recherche Clinique’. The funders had no role in the conduct of the research.
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AD, RSA, BF, NH, NB and FDV designed the study. All authors participated to the collection and assembly of data. NB performed the statistical analysis and drafted the manuscript with the help of AD, BF, RSA and FDV. All authors revised the work, approved its final version and agreed to be accountable for all its aspects.
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The FCCSS study was approved by the INSERM Institutional review board (CEEI N°12-077) and the French National Agency regulating Data Protection (CNIL N°902287). Patients, parents, or guardians’ consent was obtained according to national research ethics requirements. The study was performed in accordance with the Declaration of Helsinki.
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Bougas, N., Allodji, R.S., Fayech, C. et al. Surveillance after childhood cancer: are survivors with an increased risk for cardiomyopathy regularly followed-up?. Br J Cancer 129, 1298–1305 (2023). https://doi.org/10.1038/s41416-023-02400-0
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DOI: https://doi.org/10.1038/s41416-023-02400-0
