Technology-enabled activation of skin cancer screening for hematopoietic cell transplantation survivors and their primary care providers (TEACH)

Saro H Armenian, Lanie Lindenfeld, Aleksi Iukuridze, Meagan Echevarria, Samantha Bebel, Catherine Coleman, Ryotaro Nakamura, Farah Abdullah, Badri Modi, Kevin C Oeffinger, Karen M Emmons, Ashfaq A Marghoob, Alan C Geller, Saro H Armenian, Lanie Lindenfeld, Aleksi Iukuridze, Meagan Echevarria, Samantha Bebel, Catherine Coleman, Ryotaro Nakamura, Farah Abdullah, Badri Modi, Kevin C Oeffinger, Karen M Emmons, Ashfaq A Marghoob, Alan C Geller

Abstract

Background: Hematopoietic cell transplantation (HCT) is a curative option for a growing number of patients with hematologic diseases and malignancies. However, HCT-related factors, such as total body irradiation used for conditioning, graft-versus-host disease, and prolonged exposure to immunosuppressive therapy, result in very high risk for melanoma and non-melanoma skin cancer (NMSC). In fact, skin cancer is the most common subsequent neoplasm in HCT survivors, tending to develop at a time when survivors' follow-up care has largely transitioned to the primary care setting. The goal of this study is to increase skin cancer screening rates among HCT survivors through patient-directed activation alone or in combination with physician-directed activation. The proposed intervention will identify facilitators of and barriers to risk-based screening in this population and help reduce the burden of cancer-related morbidity after HCT.

Methods/design: 720 HCT survivors will be enrolled in this 12-month randomized controlled trial. This study uses a comparative effectiveness design comparing (1) patient activation and education (PAE, N = 360) including text messaging and print materials to encourage and motivate skin examinations; (2) PAE plus primary care physician activation (PAE + Phys, N = 360) adding print materials for the physician on the HCT survivors' increased risk of skin cancer and importance of conducting a full-body skin exam. Patients on the PAE + Phys arm will be further randomized 1:1 to the teledermoscopy (PAE + Phys+TD) adding physician receipt of a portable dermatoscope to upload images of suspect lesions for review by the study dermatologist and an online course with descriptions of dermoscopic images for skin cancers.

Discussion: When completed, this study will provide much-needed information regarding strategies to improve skin cancer detection in other high-risk (e.g. radiation-exposed) cancer survivor populations, and to facilitate screening and management of other late effects (e.g. cardiovascular, endocrine) in HCT survivors.

Trial registration: ClinicalTrials.gov, NCT04358276 . Registered 24 April 2020.

Keywords: Dermoscopy; Early detection; Hematopoietic cell transplantation; Patient activation; Skin cancer; Skin self-examination; Survivors.

Conflict of interest statement

There is no competing interest to declare on the part of any named author.

Figures

Fig. 1
Fig. 1
DermLite Dermatoscope. DermLite (www.dermlite.com) works with virtually any smartphone and tablet
Fig. 2
Fig. 2
Study Schema for different arms. PAE: Patient Activation/Education (educational materials and text messages). PAE + Phys: Patient Activation/Education (educational materials and text messages) + physician activation/educational materials targeted to identified primary care providers (PCPs). PAE + Phys+TD: Phys: Patient Activation/Education (print materials and text messages) + physician activation/education + teledermoscopy (PCPs receive a dermatoscope to upload images of suspicious skin lesions to the remote study dermatologist)

References

    1. The Skin Cancer Foundation. . Accessed 19 June 2019.
    1. Guy GP, Jr, Machlin SR, Ekwueme DU, et al. Prevalence and costs of skin cancer treatment in the U.S., 2002-2006 and 2007-2011. Am J Prev Med. 2015;48:183–187.
    1. The Surgeon General’s Call to Action to Prevent Skin Cancer 2014. . Accessed 19 June 2019.
    1. Wernli KJ, Henrikson NB, Morrison CC, et al. Screening for skin Cancer in adults: updated evidence report and systematic review for the US preventive services task force. JAMA. 2016;316:436–447.
    1. Majhail NS, Tao L, Bredeson C, et al. Prevalence of hematopoietic cell transplant survivors in theUnited states. Biol Blood Marrow Transplant. 2013;19:1498–1501.
    1. Bhatia S, Armenian SH, Landier W. How I monitor long-term and late effects after blood or marrow transplantation. Blood. 2017;130:1302–1314.
    1. Majhail NS. Long-term complications after hematopoietic cell transplantation. Hematol Oncol Stem Cell Ther. 2017;10:220–227.
    1. Danylesko I, Shimoni A. Second malignancies after hematopoietic stem cell transplantation. Curr Treat Options in Oncol. 2018;19:9.
    1. Sun CL, Kersey JH, Francisco L, et al. Burden of morbidity in 10+ year survivors of hematopoietic cell transplantation: report from the bone marrow transplantation survivor study. Biol Blood Marrow Transplant. 2013;19:1073–1080.
    1. Brown JR, Yeckes H, Friedberg JW, et al. Increasing incidence of late second malignancies after conditioning with cyclophosphamide and total-body irradiation and autologous bone marrow transplantation for non-Hodgkin's lymphoma. J Clin Oncol. 2005;23:2208–2214.
    1. Leisenring W, Friedman DL, Flowers ME, et al. Nonmelanoma skin and mucosal cancers after hematopoietic cell transplantation. J Clin Oncol. 2006;24:1119–1126.
    1. DePry JL, Vyas R, Lazarus HM, et al. Cutaneous malignant neoplasms in hematopoietic cell transplant recipients: a systematic review. JAMA Dermatol. 2015;151:775–782.
    1. Kuklinski LF, Li S, Karagas MR, et al. Effect of voriconazole on risk of nonmelanoma skin cancer after hematopoietic cell transplantation. J Am Acad Dermatol. 2017;77:706–712.
    1. Rambhia PH, Conic RZ, Atanaskova-Mesinkovska N, et al. Role of graft-versus-host disease in the development of secondary skin cancers in hematopoietic stem cell transplant recipients: A meta-analysis. J Am Acad Dermatol. 2018;79:378–380.
    1. Sloand EM, Pfannes L, Ling C, et al. Graft-versus-host disease: role of inflammation in the development of chromosomal abnormalities of keratinocytes. Biol Blood Marrow Transplant. 2010;16:1665–1673.
    1. Omland SH, Gniadecki R, Haedersdal M, et al. Skin Cancer risk in hematopoietic stem-cell transplant recipients compared with background population and renal transplant recipients: a population-based cohort study. JAMA Dermatol. 2016;152:177–183.
    1. Hasegawa W, Pond GR, Rifkind JT, et al. Long-term follow-up of secondary malignancies in adults after allogeneic bone marrow transplantation. Bone Marrow Transplant. 2005;35:51–55.
    1. Curtis RE, Metayer C, Rizzo JD, et al. Impact of chronic GVHD therapy on the development of squamous-cell cancers after hematopoietic stem-cell transplantation: an international case-control study. Blood. 2005;105:3802–3811.
    1. Rigel DS, Russak J, Friedman R. The evolution of melanoma diagnosis: 25 years beyond the ABCDs. CA Cancer J Clin. 2010;60:301–316.
    1. Berwick M, Begg CB, Fine JA, et al. Screening for cutaneous melanoma by skin self-examination. J Natl Cancer Inst. 1996;88:17–23.
    1. Aitken JF, Elwood M, Baade PD, et al. Clinical whole-body skin examination reduces the incidence of thick melanomas. Int J Cancer. 2010;126:450–458.
    1. Katalinic A, Waldmann A, Weinstock MA, et al. Does skin cancer screening save lives?: an observational study comparing trends in melanoma mortality in regions with and without screening. Cancer. 2012;118:5395–5402.
    1. Hahn T, Paplham P, Austin-Ketch T, et al. Ascertainment of unmet needs and participation in health maintenance and screening of adult hematopoietic cell transplantation survivors followed in a formal survivorship program. Biol Blood Marrow Transplant. 2017;23:1968–1973.
    1. Majhail NS, Rizzo JD, Lee SJ, et al. Recommended screening and preventive practices for long-term survivors after hematopoietic cell transplantation. Biol Blood Marrow Transplant. 2012;18:348–371.
    1. Morton LM, Saber W, Baker KS, et al. National Institutes of Health hematopoietic cell transplantation late effects initiative: the subsequent neoplasms working group report. Biol Blood Marrow Transplant. 2017;23:367–378.
    1. Shankar SM, Carter A, Sun CL, et al. Health care utilization by adult long-term survivors of hematopoietic cell transplant: report from the bone marrow transplant survivor study. Cancer Epidemiol Biomark Prev. 2007;16:834–839.
    1. Prasad PK, Sun CL, Baker KS, et al. Health care utilization by adult Hispanic long-term survivors of hematopoietic stem cell transplantation: report from the bone marrow transplant survivor study. Cancer. 2008;113:2724–33.
    1. Weinstock MA, Ferris LK, Saul MI, et al. Downstream consequences of melanoma screening in a community practice setting: first results. Cancer. 2016;122:3152–3156.
    1. Koh HK, Miller DR, Geller AC, et al. Who discovers melanoma? Patterns from a population-based survey. J Am Acad Dermatol. 1992;26:914–919.
    1. Geller AC, Emmons K, Brooks DR, et al. Skin cancer prevention and detection practices among siblings of patients with melanoma. J Am Acad Dermatol. 2003;49:631–638.
    1. Daniel CL, Armstrong GT, Keske RR, et al. Advancing Survivors' knowledge (ASK) about skin cancer study: study protocol for a randomized controlled trial. Trials. 2015;16:109.
    1. Bruce AF, Mallow JA, Theeke LA. The use of teledermoscopy in the accurate identification of cancerous skin lesions in the adult population: a systematic review. J Telemed Telecare. 2018;24:75–83.
    1. Pew Internet and Technology. 2018. . Accessed 19 June 2019.
    1. Pena-Robichaux V, Kvedar JC, Watson AJ. Text messages as a reminder aid and educational tool in adults and adolescents with atopic dermatitis: a pilot study. Dermatol Res Pract. 2010;2010.
    1. Youl PH, Soyer HP, Baade PD, et al. Can skin cancer prevention and early detection be improved via mobile phone text messaging? A randomised, attention control trial. Prev Med. 2015;71:50–56.
    1. Armstrong AW, Watson AJ, Makredes M, et al. Text-message reminders to improve sunscreen use: a randomized, controlled trial using electronic monitoring. Arch Dermatol. 2009;145:1230–1236.
    1. Oeffinger KC, McCabe MS. Models for delivering survivorship care. J Clin Oncol. 2006;24:5117–5124.
    1. Susong JR, Ahrns HT, Daugherty A, et al. Evaluation of a virtual dermatology curriculum for dermoscopy using the triage amalgamated Dermoscopic algorithm (TADA) for novice dermoscopists. J Am Acad Dermatol. 2019; (In Press).
    1. Shaikh WR, Geller A, Alexander G, et al. Developing an interactive web-based learning program on skin cancer: the learning experiences of clinical educators. J Cancer Educ. 2012;27:709–716.
    1. Hibbard JH, Stockard J, Mahoney ER, et al. Development of the patient activation measure (PAM): conceptualizing and measuring activation in patients and consumers. Health Serv Res. 2004;39:1005–1026.
    1. Hibbard JH, Mahoney E. Toward a theory of patient and consumer activation. Patient Educ Couns. 2010;78:377–381.
    1. Mehrotra A, Hussey PS, Milstein A, et al. Consumers' and providers' responses to public cost reports, and how to raise the likelihood of achieving desired results. Health Aff (Millwood) 2012;31:843–851.
    1. Rask KJ, Ziemer DC, Kohler SA, et al. Patient activation is associated with healthy behaviors and ease in managing diabetes in an indigent population. Diabetes Educ. 2009;35:622–630.
    1. Cooper LA, Roter DL, Carson KA, et al. A randomized trial to improve patient-centered care and hypertension control in underserved primary care patients. J Gen Intern Med. 2011;26:1297–1304.
    1. Holman H, Lorig K. Patient self-management: a key to effectiveness and efficiency in care of chronic disease. Public Health Rep. 2004;119:239–243.
    1. Geller AC, O'Riordan DL, Oliveria SA, et al. Overcoming obstacles to skin cancer examinations and prevention counseling for high-risk patients: results of a national survey of primary care physicians. J Am Board Fam Pract. 2004;17:416–423.
    1. Hibbard J, Lorig K. The dos and don'ts of patient engagement in busy office practices. J Ambul Care Manage. 2012;35:129–132.
    1. Renders CM, Valk GD, de Sonnaville JJ, et al. Quality of care for patients with type 2 diabetes mellitus--a long-term comparison of two quality improvement programmes in the Netherlands. Diabet Med. 2003;20:846–852.
    1. Jones C, Roderick P, Harris S, et al. An evaluation of a shared primary and secondary care nephrology service for managing patients with moderate to advanced CKD. Am J Kidney Dis. 2006;47:103–114.
    1. Holm T, Lassen JF, Husted SE, et al. A randomized controlled trial of shared care versus routine care for patients receiving oral anticoagulant therapy. J Intern Med. 2002;252:322–331.
    1. Tsang MW, Resneck JS., Jr Even patients with changing moles face long dermatology appointment wait-times: a study of simulated patient calls to dermatologists. J Am Acad Dermatol. 2006;55:54–58.
    1. Reiter O, Mimouni I, Gdalevich M, et al. The diagnostic accuracy of dermoscopy for basal cell carcinoma: a systematic review and meta-analysis. J Am Acad Dermatol. 2019;80:1380–1388.
    1. Yim KM, Florek AG, Oh DH, McKoy K, Armstrong AW. Teledermatology in the United States: An Update in a Dynamic Era. Telemed J E Health. 2018;24:691–7.
    1. Weinstock MA, Martin RA, Risica PM, et al. Thorough skin examination for the early detection of melanoma. Am J Prev Med. 1999;17:169–175.
    1. Weinstock MA, Risica PM, Martin RA, et al. Melanoma early detection with thorough skin self-examination: the "check it out" randomized trial. Am J Prev Med. 2007;32:517–524.
    1. Weinstock MA, Risica PM, Martin RA, et al. Reliability of assessment and circumstances of performance of thorough skin self-examination for the early detection of melanoma in the check-it-out project. Prev Med. 2004;38:761–765.
    1. Swetter SM, Chang J, Shaub AR, et al. Primary care-based skin Cancer screening in a veterans affairs health care system. JAMA Dermatol. 2017;153:797–801.
    1. Gellar, Alan C. "Advancing Survivors' Knowledge (ASK) about skin cancer study: study protocol for a randomized controlled trial." Presentation, 2018 Emerging Technology in Childhood Cancer Survivorship Research Conference. Houston; 2018.
    1. Solomon JA, Oswalt M, Nodzenski M, et al. Assessing skin biopsy rates for histologic findings indicative of nonpathological cutaneous disease. Dermatol Surg. 2019;45:640–649.
    1. Stang A, Jockel KH, Heidinger O. Skin cancer rates in North Rhine-Westphalia, Germany before and after the introduction of the nationwide skin cancer screening program (2000-2015) Eur J Epidemiol. 2018;33:303–312.
    1. Hsiao WC, Braun P, Dunn DL, et al. An overview of the development and refinement of the resource-based relative value scale. The foundation for reform of U.S. physician payment. Med Care. 1992;30:NS1–N12.
    1. Drummond MF, Sculpher MJ, Torrance GW, et al. Methods for the Economic Evaluation of Health Care Programmes. (ed 3) New York: Oxford University Press; 2005.

Source: PubMed

Подписаться