Total body irradiation for hematopoietic stem cell transplantation during early childhood is associated with the risk for diabetes mellitus

go back to reference T. Mori, A. Manabe, M. Tsuchida, R. Hanada, H. Yabe, A. Ohara, T. Saito, S. Nakazawa, Allogeneic bone marrow transplantation in first remission rescues children with Philadelphia chromosome-positive acute lymphoblastic leukemia. Tokyo Children’s Cancer Study Group (TCCSG) studies L89-12 and L92-13. Med. Pediatr. Oncol. 37(5), 426–431 (2001)CrossRefPubMed T. Mori, A. Manabe, M. Tsuchida, R. Hanada, H. Yabe, A. Ohara, T. Saito, S. Nakazawa, Allogeneic bone marrow transplantation in first remission rescues children with Philadelphia chromosome-positive acute lymphoblastic leukemia. Tokyo Children’s Cancer Study Group (TCCSG) studies L89-12 and L92-13. Med. Pediatr. Oncol. 37(5), 426–431 (2001)CrossRefPubMed

go back to reference J.E. Sanders, Growth and development after hematopoietic cell transplant in children. Bone Marrow Transplant. 41(2), 223–227 (2008)CrossRefPubMed J.E. Sanders, Growth and development after hematopoietic cell transplant in children. Bone Marrow Transplant. 41(2), 223–227 (2008)CrossRefPubMed

go back to reference S.H. Armenian, C.-L. Sun, T. Kawashima, M. Arora, W. Leisenring, C.A. Sklar, K.S. Baker, L. Francisco, J.B. The, G. Mills, F.L. Wong, J. Rosenthal, L.R. Diller, M.M. Hudson, K.C. Oeffinger, S.J. Forman, L.L. Robison, S. Bhatia, Long-term health-related outcomes in survivors of childhood cancer treated with HSCT versus conventional therapy: a report from the Bone Marrow Transplant Survivor Study (BMTSS) and Childhood Cancer Survivor Study (CCSS). Blood 118(5), 1413–1420 (2011)CrossRefPubMedPubMedCentral S.H. Armenian, C.-L. Sun, T. Kawashima, M. Arora, W. Leisenring, C.A. Sklar, K.S. Baker, L. Francisco, J.B. The, G. Mills, F.L. Wong, J. Rosenthal, L.R. Diller, M.M. Hudson, K.C. Oeffinger, S.J. Forman, L.L. Robison, S. Bhatia, Long-term health-related outcomes in survivors of childhood cancer treated with HSCT versus conventional therapy: a report from the Bone Marrow Transplant Survivor Study (BMTSS) and Childhood Cancer Survivor Study (CCSS). Blood 118(5), 1413–1420 (2011)CrossRefPubMedPubMedCentral

go back to reference J.L. Perkins, A.S. Kunin-Batson, N.M. Youngren, K.K. Ness, K.J. Ulrich, M.J. Hansen, A. Petryk, J. Steinberger, F.S. Anderson, K.S. Baker, Long-term follow-up of children who underwent hematopoeitic cell transplant (HCT) for AML or ALL at less than 3 years of age. Pediatr. Blood Cancer 49(7), 958–963 (2007)CrossRefPubMed J.L. Perkins, A.S. Kunin-Batson, N.M. Youngren, K.K. Ness, K.J. Ulrich, M.J. Hansen, A. Petryk, J. Steinberger, F.S. Anderson, K.S. Baker, Long-term follow-up of children who underwent hematopoeitic cell transplant (HCT) for AML or ALL at less than 3 years of age. Pediatr. Blood Cancer 49(7), 958–963 (2007)CrossRefPubMed

go back to reference E.J. Chow, L. Anderson, K.S. Baker, S. Bhatia, G.M.T. Guilcher, J. Huang, W. Pelletier, J.L. Perkins, L.S. Rivard, T. Schechter, Late effects surveillance recommendations among survivors of childhood hematopoietic cell transplantation: a children’s oncology group report. Biol. Blood Marrow Transplant. 22(5), 782–795 (2016)CrossRefPubMedPubMedCentral E.J. Chow, L. Anderson, K.S. Baker, S. Bhatia, G.M.T. Guilcher, J. Huang, W. Pelletier, J.L. Perkins, L.S. Rivard, T. Schechter, Late effects surveillance recommendations among survivors of childhood hematopoietic cell transplantation: a children’s oncology group report. Biol. Blood Marrow Transplant. 22(5), 782–795 (2016)CrossRefPubMedPubMedCentral

go back to reference A.R. Hartman, S.F. Williams, J.J. Dillon, Survival, disease-free survival and adverse effects of conditioning for allogeneic bone marrow transplantation with busulfan/cyclophosphamide vs total body irradiation: a meta-analysis. Bone Marrow Transplant. 22(5), 439–443 (1998)CrossRefPubMed A.R. Hartman, S.F. Williams, J.J. Dillon, Survival, disease-free survival and adverse effects of conditioning for allogeneic bone marrow transplantation with busulfan/cyclophosphamide vs total body irradiation: a meta-analysis. Bone Marrow Transplant. 22(5), 439–443 (1998)CrossRefPubMed

go back to reference Z. DeFilipp, R.F. Duarte, J.A. Snowden, N.S. Majhail, D.M. Greenfield, J.L. Miranda, M. Arat, K.S. Baker, L.J. Burns, C.N. Duncan, M. Gilleece, G.A. Hale, M. Hamadani, B.K. Hamilton, W.J. Hogan, J.W. Hsu, Y. Inamoto, R.T. Kamble, M.T. Lupo-Stanghellini, A.K. Malone, P. McCarthy, M. Mohty, M. Norkin, P. Paplham, M. Ramanathan, J.M. Richart, N. Salooja, H.C. Schouten, H. Schoemans, A. Seber, A. Steinberg, B.M. Wirk, W.A. Wood, M. Battiwalla, M.E.D. Flowers, B.N. Savani, B.E. Shaw, Metabolic syndrome and cardiovascular disease following hematopoietic cell transplantation: screening and preventive practice recommendations from CIBMTR and EBMT. Bone Marrow Transplant. 52(2), 173–182 (2017)CrossRefPubMed Z. DeFilipp, R.F. Duarte, J.A. Snowden, N.S. Majhail, D.M. Greenfield, J.L. Miranda, M. Arat, K.S. Baker, L.J. Burns, C.N. Duncan, M. Gilleece, G.A. Hale, M. Hamadani, B.K. Hamilton, W.J. Hogan, J.W. Hsu, Y. Inamoto, R.T. Kamble, M.T. Lupo-Stanghellini, A.K. Malone, P. McCarthy, M. Mohty, M. Norkin, P. Paplham, M. Ramanathan, J.M. Richart, N. Salooja, H.C. Schouten, H. Schoemans, A. Seber, A. Steinberg, B.M. Wirk, W.A. Wood, M. Battiwalla, M.E.D. Flowers, B.N. Savani, B.E. Shaw, Metabolic syndrome and cardiovascular disease following hematopoietic cell transplantation: screening and preventive practice recommendations from CIBMTR and EBMT. Bone Marrow Transplant. 52(2), 173–182 (2017)CrossRefPubMed

go back to reference C. Bizzarri, R.M. Pinto, S. Ciccone, L. Brescia, F. Locatelli, C. Marco, Early and progressive insulin resistance in young, non-obese cancer survivors treated with hematopoietic stem cell transplantation. Pediatr. Blood Cancer 62(9), 1650–1655 (2015)CrossRefPubMed C. Bizzarri, R.M. Pinto, S. Ciccone, L. Brescia, F. Locatelli, C. Marco, Early and progressive insulin resistance in young, non-obese cancer survivors treated with hematopoietic stem cell transplantation. Pediatr. Blood Cancer 62(9), 1650–1655 (2015)CrossRefPubMed

go back to reference K.S. Baker, K.K. Ness, J. Steinberger, A. Carter, L. Francisco, L.J. Burns, C. Sklar, S. Forman, D. Weisdorf, J.G. Gurney, S. Bhatia, Diabetes, hypertension, and cardiovascular events in survivors of hematopoietic cell transplantation: a report from the bone marrow transplantation survivor study. Blood 109(4), 1765–1772 (2007)CrossRefPubMed K.S. Baker, K.K. Ness, J. Steinberger, A. Carter, L. Francisco, L.J. Burns, C. Sklar, S. Forman, D. Weisdorf, J.G. Gurney, S. Bhatia, Diabetes, hypertension, and cardiovascular events in survivors of hematopoietic cell transplantation: a report from the bone marrow transplantation survivor study. Blood 109(4), 1765–1772 (2007)CrossRefPubMed

go back to reference M. Taskinen, U.M. Saarinen-Pihkala, L. Hovi, M. Lipsanen-Nyman, Impaired glucose tolerance and dyslipidaemia as late effects after bone-marrow transplantation in childhood. Lancet 356(9234), 993–997 (2000)CrossRefPubMed M. Taskinen, U.M. Saarinen-Pihkala, L. Hovi, M. Lipsanen-Nyman, Impaired glucose tolerance and dyslipidaemia as late effects after bone-marrow transplantation in childhood. Lancet 356(9234), 993–997 (2000)CrossRefPubMed

go back to reference C. Oudin, M.-C. Simeoni, N. Sirvent, A. Contet, C.A. Begu-Le, P. Bordigoni, C. Curtillet, M. Poirée, I. Thuret, B. Play, M.C. Massot, P. Chastagner, H. Chambost, P. Auquier, G. Michel, Prevalence and risk factors of the metabolic syndrome in adult survivors of childhood leukemia. Blood 117(17), 4442–4448 (2011)CrossRefPubMed C. Oudin, M.-C. Simeoni, N. Sirvent, A. Contet, C.A. Begu-Le, P. Bordigoni, C. Curtillet, M. Poirée, I. Thuret, B. Play, M.C. Massot, P. Chastagner, H. Chambost, P. Auquier, G. Michel, Prevalence and risk factors of the metabolic syndrome in adult survivors of childhood leukemia. Blood 117(17), 4442–4448 (2011)CrossRefPubMed

go back to reference W. Chemaitilly, F. Boulad, K.C. Oeffinger, C.A. Sklar, Disorders of glucose homeostasis in young adults treated with total body irradiation during childhood: a pilot study. Bone Marrow Transplant. 44(6), 339–343 (2009)CrossRefPubMed W. Chemaitilly, F. Boulad, K.C. Oeffinger, C.A. Sklar, Disorders of glucose homeostasis in young adults treated with total body irradiation during childhood: a pilot study. Bone Marrow Transplant. 44(6), 339–343 (2009)CrossRefPubMed

go back to reference K.A. Neville, R.J. Cohn, K.S. Steinbeck, K. Johnston, J.L. Walker, Hyperinsulinemia, impaired glucose tolerance, and diabetes mellitus in survivors of childhood cancer: prevalence and risk factors. J. Clin. Endocrinol. Metab. 91(11), 4401–4407 (2006)CrossRefPubMed K.A. Neville, R.J. Cohn, K.S. Steinbeck, K. Johnston, J.L. Walker, Hyperinsulinemia, impaired glucose tolerance, and diabetes mellitus in survivors of childhood cancer: prevalence and risk factors. J. Clin. Endocrinol. Metab. 91(11), 4401–4407 (2006)CrossRefPubMed

go back to reference L.R. Meacham, C.A. Sklar, S. Li, Q. Liu, N. Gimpel, Y. Yasui, J.A. Whitton, M. Stovall, L.L. Robison, K.C. Oeffinger, Diabetes mellitus in long-term survivors of childhood cancer. Increased risk associated with radiation therapy: a report for the childhood cancer survivor study. Arch. Intern Med. 169(15), 1381–1388 (2009)CrossRefPubMedPubMedCentral L.R. Meacham, C.A. Sklar, S. Li, Q. Liu, N. Gimpel, Y. Yasui, J.A. Whitton, M. Stovall, L.L. Robison, K.C. Oeffinger, Diabetes mellitus in long-term survivors of childhood cancer. Increased risk associated with radiation therapy: a report for the childhood cancer survivor study. Arch. Intern Med. 169(15), 1381–1388 (2009)CrossRefPubMedPubMedCentral

go back to reference S. Shalitin, M. Phillip, J. Stein, Y. Goshen, D. Carmi, I. Yaniv, Endocrine dysfunction and parameters of the metabolic syndrome after bone marrow transplantation during childhood and adolescence. Bone Marrow Transplant. 37(12), 1109–1117 (2006)CrossRefPubMed S. Shalitin, M. Phillip, J. Stein, Y. Goshen, D. Carmi, I. Yaniv, Endocrine dysfunction and parameters of the metabolic syndrome after bone marrow transplantation during childhood and adolescence. Bone Marrow Transplant. 37(12), 1109–1117 (2006)CrossRefPubMed

go back to reference C. Annaloro, P. Usardi, L. Airaghi, V. Giunta, S. Forti, A. Orsatti, M. Baldini, A. Delle Volpe, G. Lambertenghi Deliliers, Prevalence of metabolic syndrome in long-term survivors of hematopoietic stem cell transplantation. Bone Marrow Transplant. 41(9), 797–804 (2008)CrossRefPubMed C. Annaloro, P. Usardi, L. Airaghi, V. Giunta, S. Forti, A. Orsatti, M. Baldini, A. Delle Volpe, G. Lambertenghi Deliliers, Prevalence of metabolic syndrome in long-term survivors of hematopoietic stem cell transplantation. Bone Marrow Transplant. 41(9), 797–804 (2008)CrossRefPubMed

go back to reference C. Wei, R. Unsworth, N. Davis, R. Cox, K. Bradley, M. Stevens, E. Crowne, Survivors of childhood leukaemia treated with haematopoietic stem cell transplantation and total body irradiation should undergo screening for diabetes by oral glucose tolerance tests. Diabet. Med. J. Br. Diabet. Assoc. 33(10), 1347–1351 (2016)CrossRef C. Wei, R. Unsworth, N. Davis, R. Cox, K. Bradley, M. Stevens, E. Crowne, Survivors of childhood leukaemia treated with haematopoietic stem cell transplantation and total body irradiation should undergo screening for diabetes by oral glucose tolerance tests. Diabet. Med. J. Br. Diabet. Assoc. 33(10), 1347–1351 (2016)CrossRef

go back to reference L.M. Turcotte, A. Yingst, M.R. Verneris, Metabolic syndrome after hematopoietic cell transplantation: at the intersection of treatment toxicity and immune dysfunction. Biol. Blood Marrow Transplant. 22(7), 1159–1166 (2016)CrossRefPubMedPubMedCentral L.M. Turcotte, A. Yingst, M.R. Verneris, Metabolic syndrome after hematopoietic cell transplantation: at the intersection of treatment toxicity and immune dysfunction. Biol. Blood Marrow Transplant. 22(7), 1159–1166 (2016)CrossRefPubMedPubMedCentral

go back to reference C. Oudin, P. Auquier, Y. Bertrand, A. Contet, J. Kanold, N. Sirvent, S. Thouvenin, M.D. Tabone, P. Lutz, S. Ducassou, D. Plantaz, J.H. Dalle, V. Gandemer, S. Beliard, J. Berbis, C. Vercasson, V. Barlogis, A. Baruchel, G. Leverger, G. Michel, Metabolic syndrome in adults who received hematopoietic stem cell transplantation for acute childhood leukemia: an LEA study. Bone Marrow Transplant. 50(11), 1438–1444 (2015)CrossRefPubMed C. Oudin, P. Auquier, Y. Bertrand, A. Contet, J. Kanold, N. Sirvent, S. Thouvenin, M.D. Tabone, P. Lutz, S. Ducassou, D. Plantaz, J.H. Dalle, V. Gandemer, S. Beliard, J. Berbis, C. Vercasson, V. Barlogis, A. Baruchel, G. Leverger, G. Michel, Metabolic syndrome in adults who received hematopoietic stem cell transplantation for acute childhood leukemia: an LEA study. Bone Marrow Transplant. 50(11), 1438–1444 (2015)CrossRefPubMed

go back to reference American Diabetes Association, 2. Classification and Diagnosis of Diabetes: Standards of Medical Care in Diabetes-2018. Diabetes Care. 41(Suppl 1), S13–S27 (2018) American Diabetes Association, 2. Classification and Diagnosis of Diabetes: Standards of Medical Care in Diabetes-2018. Diabetes Care. 41(Suppl 1), S13–S27 (2018)

go back to reference T. Okada, M. Murata, K. Yamauchi, K. Harada, New criteria of normal serum lipid levels in Japanese children: the nationwide study. Pediatr. Int. 44(6), 596–601 (2002)CrossRefPubMed T. Okada, M. Murata, K. Yamauchi, K. Harada, New criteria of normal serum lipid levels in Japanese children: the nationwide study. Pediatr. Int. 44(6), 596–601 (2002)CrossRefPubMed

go back to reference E. Erhardt, R. Foraita, I. Pigeot, G. Barba, T. Veidebaum, M. Tornaritis, N. Michels, G. Eiben, W. Ahrens, L.A. Moreno, E. Kovács, D. Molnár, IDEFICS consortium, Reference values for leptin and adiponectin in children below the age of 10 based on the IDEFICS cohort. Int J. Obes. 38(Suppl 2), S32–S38 (2014)CrossRef E. Erhardt, R. Foraita, I. Pigeot, G. Barba, T. Veidebaum, M. Tornaritis, N. Michels, G. Eiben, W. Ahrens, L.A. Moreno, E. Kovács, D. Molnár, IDEFICS consortium, Reference values for leptin and adiponectin in children below the age of 10 based on the IDEFICS cohort. Int J. Obes. 38(Suppl 2), S32–S38 (2014)CrossRef

go back to reference R.E. Ostlund, J.W. Yang, S. Klein, R. Gingerich, Relation between plasma leptin concentration and body fat, gender, diet, age, and metabolic covariates. J. Clin. Endocrinol. Metab. 81(11), 3909–3913 (1996)PubMed R.E. Ostlund, J.W. Yang, S. Klein, R. Gingerich, Relation between plasma leptin concentration and body fat, gender, diet, age, and metabolic covariates. J. Clin. Endocrinol. Metab. 81(11), 3909–3913 (1996)PubMed

go back to reference K. Numakura, S. Satoh, N. Tsuchiya, Y. Horikawa, T. Inoue, H. Kakinuma, S. Matsuura, M. Saito, H. Tada, T. Suzuki, T. Habuchi, Clinical and genetic risk factors for posttransplant diabetes mellitus in adult renal transplant recipients treated with tacrolimus. Transplantation 80(10), 1419–1424 (2005)CrossRefPubMed K. Numakura, S. Satoh, N. Tsuchiya, Y. Horikawa, T. Inoue, H. Kakinuma, S. Matsuura, M. Saito, H. Tada, T. Suzuki, T. Habuchi, Clinical and genetic risk factors for posttransplant diabetes mellitus in adult renal transplant recipients treated with tacrolimus. Transplantation 80(10), 1419–1424 (2005)CrossRefPubMed

go back to reference N. Bunin, R. Aplenc, N. Kamani, K. Shaw, A. Cnaan, S. Simms, Randomized trial of busulfan vs total body irradiation containing conditioning regimens for children with acute lymphoblastic leukemia: a Pediatric Blood and Marrow Transplant Consortium study. Bone Marrow Transplant. 32(6), 543–548 (2003)CrossRefPubMed N. Bunin, R. Aplenc, N. Kamani, K. Shaw, A. Cnaan, S. Simms, Randomized trial of busulfan vs total body irradiation containing conditioning regimens for children with acute lymphoblastic leukemia: a Pediatric Blood and Marrow Transplant Consortium study. Bone Marrow Transplant. 32(6), 543–548 (2003)CrossRefPubMed

go back to reference J. Hartmann, M. Schüßler-Lenz, A. Bondanza, C.J. Buchholz, Clinical development of CAR T cells—challenges and opportunities in translating innovative treatment concepts. EMBO Mol. Med. 9(9), 1183–1197 (2017)CrossRefPubMedPubMedCentral J. Hartmann, M. Schüßler-Lenz, A. Bondanza, C.J. Buchholz, Clinical development of CAR T cells—challenges and opportunities in translating innovative treatment concepts. EMBO Mol. Med. 9(9), 1183–1197 (2017)CrossRefPubMedPubMedCentral

go back to reference K. Kavanagh, M.D. Dendinger, A.T. Davis, T.C. Register, R. Debo, G. Dugan, J.M. Cline, Type 2 diabetes is a delayed late effect of whole-body irradiation in nonhuman primates. Radiat. Res. 183(4), 398–406 (2015)CrossRefPubMedPubMedCentral K. Kavanagh, M.D. Dendinger, A.T. Davis, T.C. Register, R. Debo, G. Dugan, J.M. Cline, Type 2 diabetes is a delayed late effect of whole-body irradiation in nonhuman primates. Radiat. Res. 183(4), 398–406 (2015)CrossRefPubMedPubMedCentral

go back to reference M. Adachi, Y. Asakura, K. Muroya, H. Goto, H. Kigasawa, Abnormal adipose tissue distribution with unfavorable metabolic profile in five children following hematopoietic stem cell transplantation: a new etiology for acquired partial lipodystrophy. Clin. Pediatr. Endocrinol. 22(4), 53–64 (2013)CrossRefPubMedPubMedCentral M. Adachi, Y. Asakura, K. Muroya, H. Goto, H. Kigasawa, Abnormal adipose tissue distribution with unfavorable metabolic profile in five children following hematopoietic stem cell transplantation: a new etiology for acquired partial lipodystrophy. Clin. Pediatr. Endocrinol. 22(4), 53–64 (2013)CrossRefPubMedPubMedCentral

go back to reference C. Wei, M.S. Thyagiarajan, L.P. Hunt, J.P.H. Shield, M.C.G. Stevens, E.C. Crowne, Reduced insulin sensitivity in childhood survivors of haematopoietic stem cell transplantation is associated with lipodystropic and sarcopenic phenotypes. Pediatr. Blood Cancer 62(11), 1992–1999 (2015)CrossRefPubMed C. Wei, M.S. Thyagiarajan, L.P. Hunt, J.P.H. Shield, M.C.G. Stevens, E.C. Crowne, Reduced insulin sensitivity in childhood survivors of haematopoietic stem cell transplantation is associated with lipodystropic and sarcopenic phenotypes. Pediatr. Blood Cancer 62(11), 1992–1999 (2015)CrossRefPubMed

go back to reference E.T. Parlevliet, J.E. de Leeuw van Weenen, J.A. Romijn, H. Pijl, GLP-1 treatment reduces endogenous insulin resistance via activation of central GLP-1 receptors in mice fed a high-fat diet. Am. J. Physiol. Endocrinol. Metab. 299(2), E318–E324 (2010)CrossRefPubMed E.T. Parlevliet, J.E. de Leeuw van Weenen, J.A. Romijn, H. Pijl, GLP-1 treatment reduces endogenous insulin resistance via activation of central GLP-1 receptors in mice fed a high-fat diet. Am. J. Physiol. Endocrinol. Metab. 299(2), E318–E324 (2010)CrossRefPubMed

go back to reference H. Wu, C. Sui, H. Xu, F. Xia, H. Zhai, H. Zhang, P. Weng, B. Han, S. Du, Y. Lu, The GLP-1 analogue exenatide improves hepatic and muscle insulin sensitivity in diabetic rats: tracer studies in the basal state and during hyperinsulinemic-euglycemic clamp. J. Diabetes Res. 2014, 524517 (2014)PubMedPubMedCentral H. Wu, C. Sui, H. Xu, F. Xia, H. Zhai, H. Zhang, P. Weng, B. Han, S. Du, Y. Lu, The GLP-1 analogue exenatide improves hepatic and muscle insulin sensitivity in diabetic rats: tracer studies in the basal state and during hyperinsulinemic-euglycemic clamp. J. Diabetes Res. 2014, 524517 (2014)PubMedPubMedCentral

go back to reference J. Oliveira, E. Lau, D. Carvalho, P. Freitas, Glucagon-like peptide-1 analogues - an efficient therapeutic option for the severe insulin resistance of lipodystrophic syndromes: two case reports. J. Med. Case Rep. 11(1), 12 (2017)CrossRefPubMedPubMedCentral J. Oliveira, E. Lau, D. Carvalho, P. Freitas, Glucagon-like peptide-1 analogues - an efficient therapeutic option for the severe insulin resistance of lipodystrophic syndromes: two case reports. J. Med. Case Rep. 11(1), 12 (2017)CrossRefPubMedPubMedCentral