New-Onset Diabetes After Kidney Transplantation—Changes and Challenges

Despite substantial improvement in short-term results after kidney transplantation, increases in long-term graft survival have been modest. A significant impediment has been the morbidity and mortality attributable to cardiovascular disease (CVD). New-onset diabetes after transplantation (NODAT) is an independent predictor of cardiovascular events. This review examines recent literature surrounding diagnosis, outcomes and management of NODAT. Amongst otherwise heterogeneous studies, a common finding is the relative insensitivity of fasting blood glucose (FBG) as a screening test. Incorporating self-testing of afternoon capillary BG and glycohemoglobin (HbA1c) detects many cases that would otherwise remain undetected without the oral glucose tolerance test (OGTT). Assessing the impact of NODAT on patient and graft survival is complicated by changes to diagnostic criteria, evolution of immunosuppressive regimens and increasing attention to cardiovascular risk management. Although recent studies reinforce a link between NODAT and death with a functioning graft (DWFG), there seems to be little effect on death-censored graft loss. The significance of glycemic control and diabetes resolution for patient outcomes remain notably absent from NODAT literature and treatment is also a neglected area. This review examines new and old therapeutic options, emphasizing the need to assess β-cell pathology in customizing therapy. Finally, areas warranting further research are considered. Despite substantial improvement in short-term results after kidney transplantation, increases in long-term graft survival have been modest. A significant impediment has been the morbidity and mortality attributable to cardiovascular disease (CVD). New-onset diabetes after transplantation (NODAT) is an independent predictor of cardiovascular events. This review examines recent literature surrounding diagnosis, outcomes and management of NODAT. Amongst otherwise heterogeneous studies, a common finding is the relative insensitivity of fasting blood glucose (FBG) as a screening test. Incorporating self-testing of afternoon capillary BG and glycohemoglobin (HbA1c) detects many cases that would otherwise remain undetected without the oral glucose tolerance test (OGTT). Assessing the impact of NODAT on patient and graft survival is complicated by changes to diagnostic criteria, evolution of immunosuppressive regimens and increasing attention to cardiovascular risk management. Although recent studies reinforce a link between NODAT and death with a functioning graft (DWFG), there seems to be little effect on death-censored graft loss. The significance of glycemic control and diabetes resolution for patient outcomes remain notably absent from NODAT literature and treatment is also a neglected area. This review examines new and old therapeutic options, emphasizing the need to assess β-cell pathology in customizing therapy. Finally, areas warranting further research are considered. As rates of acute rejection have fallen and short-term graft survival has improved, new challenges have emerged to limit the longevity of kidney transplant recipients. Death with a functioning graft accounts for at least half of late allograft failure, and Cosio et al. noted that cardiovascular disease (CVD) is responsible for 61% of deaths in recipients with preexisting diabetes and 26% in recipients without diabetes (1Cosio FG Hickson LJ Griffin MD Stegall MD Kudva Y Patient survival and cardiovascular risk after kidney transplantation: The challenge of diabetes.Am J Transplant. 2008; 8: 593-599Crossref PubMed Scopus (155) Google Scholar,2Young JB Neumayer HH Gordon RD Pretransplant cardiovascular evaluation and posttransplant cardiovascular risk.Kidney Int. 2010; 78: S1-S7Abstract Full Text Full Text PDF Scopus (30) Google Scholar). Renal transplantation is associated with other CVD risk factors including hypertension, dyslipidemia and obesity (2Young JB Neumayer HH Gordon RD Pretransplant cardiovascular evaluation and posttransplant cardiovascular risk.Kidney Int. 2010; 78: S1-S7Abstract Full Text Full Text PDF Scopus (30) Google Scholar), however, new-onset diabetes after transplantation (NODAT) has previously been linked to a 1.7-fold increase in cardiovascular events, 1.9-fold increase in mortality and 1.6-fold increase in graft failure (3Cosio FG Kudva Y van der Velde M Larson TS Textor SC Griffin MD et al.New onset hyperglycemia and diabetes are associated with increased cardiovascular risk after kidney transplantation.Kidney Int. 2005; 67: 2415-2421Abstract Full Text Full Text PDF PubMed Scopus (328) Google Scholar,4Kasiske BL Snyder JJ Gilbertson D Matas AJ Diabetes mellitus after kidney transplantation in the United States.Am J Transplant. 2003; 3: 178-185Crossref PubMed Scopus (1066) Google Scholar). In this review of the current status of NODAT, we address incidence, outcomes and diagnosis in the modern era and consider pathogenesis in assessing therapeutic approaches. Prior publications have highlighted deficiencies in historic diagnostic criteria for NODAT (e.g. the requirement of hypoglycemic agents for a minimum period posttransplantation). The diversity of glycemic thresholds employed is one of several factors contributing to the wide variation in the reported incidence of NODAT (Table 1; Refs. 4Kasiske BL Snyder JJ Gilbertson D Matas AJ Diabetes mellitus after kidney transplantation in the United States.Am J Transplant. 2003; 3: 178-185Crossref PubMed Scopus (1066) Google Scholar, 5Cosio FG Pesavento TE Osei K Henry ML Ferguson RM Post-transplant diabetes mellitus: Increasing incidence in renal allograft recipients transplanted in recent years.Kidney Int. 2001; 59: 732-737Abstract Full Text Full Text PDF PubMed Scopus (323) Google Scholar, 6Vincenti FFS Scheuermann E Rostaing L et al.DIRECT Investigators. Results of an international, randomized trial comparing glucose metabolism disorders and outcome with cyclosporine versus tacrolimus.Am J Transplant. 2008; 7: 1506-1514Crossref Scopus (493) Google Scholar, 7Luan FL Steffick DE Ojo AO New-Onset diabetes mellitus in kidney transplant recipients discharged on steroid-free immunosuppression.Transplantation. 2011; 91: 334-341Crossref PubMed Scopus (109) Google Scholar).Table 1:Studies using treatment based definitions of NODAT or registry dataStudyNDefinitionNODAT incidence (%)PopulationPrimary maintenance immunosuppressive regimenMonths postYears post161351015Cosio et al. (2001) (Ref. 5Cosio FG Pesavento TE Osei K Henry ML Ferguson RM Post-transplant diabetes mellitus: Increasing incidence in renal allograft recipients transplanted in recent years.Kidney Int. 2001; 59: 732-737Abstract Full Text Full Text PDF PubMed Scopus (323) Google Scholar)2078Treatment past day 30710132130White/African AmericanPred, CsA, Aza/MMFKasiske et al. (2003) (Ref. 4Kasiske BL Snyder JJ Gilbertson D Matas AJ Diabetes mellitus after kidney transplantation in the United States.Am J Transplant. 2003; 3: 178-185Crossref PubMed Scopus (1066) Google Scholar)11 659Medicare claim91624US Medicare beneficiariesPred, CsA, MMFVincenti et al. (2008) (Ref. 6Vincenti FFS Scheuermann E Rostaing L et al.DIRECT Investigators. Results of an international, randomized trial comparing glucose metabolism disorders and outcome with cyclosporine versus tacrolimus.Am J Transplant. 2008; 7: 1506-1514Crossref Scopus (493) Google Scholar)567Treatment past day 301359 centers, 16 countriesPred, CsA/Tac, MMFLuan et al. (2011) (Ref. 7Luan FL Steffick DE Ojo AO New-Onset diabetes mellitus in kidney transplant recipients discharged on steroid-free immunosuppression.Transplantation. 2011; 91: 334-341Crossref PubMed Scopus (109) Google Scholar)25 837Registry16White/African AmericanPred, Tac, MMF/MFA (27% steroid free)Pred = prednisone/prednisolone; CsA = cyclosporine A; Tac = tacrolimus; Aza = azathioprine; MMF = mycophenolate mofetil; MFA = mycophenolic acid; US = United States. Open table in a new tab Pred = prednisone/prednisolone; CsA = cyclosporine A; Tac = tacrolimus; Aza = azathioprine; MMF = mycophenolate mofetil; MFA = mycophenolic acid; US = United States. Cognizant of the need for greater uniformity, international consensus guidelines for NODAT were developed in 2003, with approval from the World Health Organization (WHO) and American Diabetes Association (ADA). These mirrored WHO guidelines for nontransplant diabetes (Table 2; Refs. 8Davidson J WA, Dantal J, Dotta F, et al. New-onset diabetes after transplantation: 2003 international consensus guidelines. In: Proceedings of an International Expert Panel Meeting; 2003; Feb. 19; Barcelona, Spain [ Transplantation 2003; 10 (suppl 75): S3–S24].Google Scholar, 9Hagen M Hjelmesaeth J Jenssen T Morkrid L Hartmann A A 6-year prospective study on new onset diabetes mellitus, and in renal transplant Transplant. 2003; PubMed Scopus Google Scholar, E et of glucose metabolism in the after renal transplantation in PubMed Scopus Google Scholar, et factors associated with the onset and of diabetes in renal allograft PubMed Scopus Google Scholar, E A et in in the after kidney transplantation: A prospective and 2008; PubMed Scopus Google Scholar, Jenssen T Hartmann A et glucose and in the screening for diabetes mellitus after renal PubMed Scopus Google Scholar, FL E Ojo A and new onset diabetes after transplantation in kidney transplant Transplant. 2010; PubMed Scopus Google Scholar).Table criteria for posttransplant diabetes mellitus and glucose for new-onset diabetes after transplantation mellitus one of of with a glucose minimum glucose test be on day in the of hyperglycemia by acute for posttransplant fasting glucose or glucose tolerance and further with glucose and diabetes screening after transplantation: for and after the Open table in a new tab In the of consensus criteria of kidney transplant recipients as NODAT by 10 Jenssen T Hartmann A et glucose and in the screening for diabetes mellitus after renal PubMed Scopus Google Scholar). of NODAT incidence the posttransplant period have been by study and immunosuppressive regimens (Table is the of fasting blood glucose (FBG) as a diagnostic oral glucose tolerance test that of of would have evaluation been to Hartmann A et diabetes in kidney transplant A J 2010; PubMed Scopus Google Scholar). an as this of with In to after transplantation, that to with fasting glucose of with NODAT Jenssen T Hartmann A et glucose and in the screening for diabetes mellitus after renal PubMed Scopus Google Scholar). transplantation, that with 61% or capillary BG in the or A et diagnosis of renal transplant diabetes mellitus in renal transplant 2005; PubMed Scopus Google Scholar). glucose were the the of L Full Text Full Text PDF PubMed Scopus Google Scholar).Table using definitions of incidence (%)PopulationPrimary maintenance immunosuppressive regimenMonths postYears et al. (2003) (Ref. 9Hagen M Hjelmesaeth J Jenssen T Morkrid L Hartmann A A 6-year prospective study on new onset diabetes mellitus, and in renal transplant Transplant. 2003; PubMed Scopus Google CsA, et al. (Ref. E et of glucose metabolism in the after renal transplantation in PubMed Scopus Google Tac, et al. (Ref. et factors associated with the onset and of diabetes in renal allograft PubMed Scopus Google CsA, et al. (2008) (Ref. E A et in in the after kidney transplantation: A prospective and 2008; PubMed Scopus Google Tac, et al. (Ref. Jenssen T Hartmann A et glucose and in the screening for diabetes mellitus after renal PubMed Scopus Google CsA, et al. (Ref. FL E Ojo A and new onset diabetes after transplantation in kidney transplant Transplant. 2010; PubMed Scopus Google AmericanPred, CsA, = prednisone/prednisolone; CsA = cyclosporine A; Tac = tacrolimus; Aza = azathioprine; MMF = mycophenolate Open table in a new tab Pred = prednisone/prednisolone; CsA = cyclosporine A; Tac = tacrolimus; Aza = azathioprine; MMF = mycophenolate changes to screening and diagnostic criteria for NODAT be to of including and capillary BG The is and after be by the of hyperglycemia to L Full Text Full Text PDF PubMed Scopus Google Scholar). This is a for of afternoon capillary BG as a screening in this posttransplant In the nontransplant the has an of for the diagnosis of be in a BG and with of in nontransplant In to has and greater E et on the of the in the diagnosis of PubMed Scopus Google Scholar). a of with and the impact of factors (e.g. blood and factors common and as as posttransplant after renal J PubMed Scopus Google Scholar). A study of with at 10 posttransplant that using to of with NODAT and of to an Jenssen T Hartmann A et glucose and in the screening for diabetes mellitus after renal PubMed Scopus Google Scholar). the using as a for a and of to The of and a of from of the posttransplant the in criteria for NODAT in the diagnosis on patient and graft an of this in the modern era is by variation in immunosuppressive the of cardiovascular risk management and of studies Snyder JJ BL disease after renal transplantation: Results from the patient outcomes in renal transplantation 2011; 91: PubMed Scopus Google Scholar). In one of the prospective studies the outcomes of with NODAT, et al. kidney recipients transplanted between and and the of an at 10 a of associated with death glucose tolerance linked to a greater with the attributable to and CVD mortality 1; T J Hartmann A et of glucose with long-term 2011; PubMed Scopus Google Scholar). This be by the in posttransplant in the current In the in the NODAT a increase in CVD mortality and a increase in et al. also an between NODAT and death with a functioning graft (DWFG), studies little impact on death-censored graft survival BL Snyder JJ Gilbertson D Matas AJ Diabetes mellitus after kidney transplantation in the United States.Am J Transplant. 2003; 3: 178-185Crossref PubMed Scopus (1066) Google of acute rejection and new-onset diabetes on long-term transplant graft and patient J 2008; 3: PubMed Scopus Google Scholar). A registry of the impact of preexisting acute NODAT and of diabetes mellitus, new-onset diabetes after and acute rejection with transplant of the and transplant for J 2010; Full Text Full Text PDF PubMed Scopus Google Scholar). This the between preexisting diabetes and patient A to death-censored graft survival in with preexisting diabetes a significant in the period of In this NODAT associated with effect on patient or graft however, the that would an between NODAT and The of hyperglycemia to the CVD mortality in with NODAT is with the that of glucose metabolism at greater risk of and This further the need for prospective studies assessing the impact of glycemic control on patient outcomes after Although the need for hypoglycemic as a for NODAT, the requirement for from a patient and to the of NODAT. The current impact of NODAT is and changes to diagnostic criteria and to an In the the et al. the United Renal for kidney recipients transplanted between and and that by posttransplant of NODAT an J et and of new onset diabetes mellitus US and transplanted renal allograft J Transplant. 2003; 3: PubMed Scopus Google Scholar). In this NODAT to a to be complicated in transplant of blood and that the recent outcome studies by et al. of death or graft in the is to a diagnosis of NODAT significant in this period by (e.g. rejection that to of that associated with Refs. T J Hartmann A et of glucose with long-term 2011; PubMed Scopus Google Scholar, of acute rejection and new-onset diabetes on long-term transplant graft and patient J 2008; 3: PubMed Scopus Google Scholar, of diabetes mellitus, new-onset diabetes after and acute rejection with transplant of the and transplant for J 2010; Full Text Full Text PDF PubMed Scopus Google Scholar). The attributable to NODAT in the blood hypoglycemic review and of diabetes with is reported resolution of of NODAT cases with in and et factors and of diabetes Transplant. 2010; PubMed Scopus Google Scholar). Although of glucose has been associated with an increase in cardiovascular NODAT has been linked to the cardiovascular outcomes associated with disease T J Hartmann A et of glucose with long-term 2011; PubMed Scopus Google et factors and of diabetes Transplant. 2010; PubMed Scopus Google Scholar). In one of the studies this with NODAT were for an of of NODAT and that of events, in the of with NODAT J Hartmann A T et impact of new-onset diabetes mellitus on survival and Int. Full Text Full Text PDF PubMed Scopus Google Scholar). glucose of and are reported risk factors common to NODAT and diabetes Refs. 4Kasiske BL Snyder JJ Gilbertson D Matas AJ Diabetes mellitus after kidney transplantation in the United States.Am J Transplant. 2003; 3: 178-185Crossref PubMed Scopus (1066) Google FG Pesavento TE Osei K Henry ML Ferguson RM Post-transplant diabetes mellitus: Increasing incidence in renal allograft recipients transplanted in recent years.Kidney Int. 2001; 59: 732-737Abstract Full Text Full Text PDF PubMed Scopus (323) Google Scholar). obesity is with of or at the of and a of posttransplant and that the risk of NODAT increased for and for T A E et factors for of new-onset diabetes mellitus after kidney PubMed Scopus Google Scholar). Although and are associated with to the greater significance of and is and in with have a significance with cardiovascular outcomes et of and other obesity as of cardiovascular disease risk in with A prospective study from J 2011; PubMed Scopus Google Scholar). In a prospective study of a predictor of mortality after A et and mortality in kidney transplant J Transplant. 2010; Full Text Full Text PDF PubMed Scopus Google Scholar). risk for NODAT is with recipients at the of transplantation the risk of NODAT BL Snyder JJ Gilbertson D Matas AJ Diabetes mellitus after kidney transplantation in the United States.Am J Transplant. 2003; 3: 178-185Crossref PubMed Scopus (1066) Google FG Pesavento TE Osei K Henry ML Ferguson RM Post-transplant diabetes mellitus: Increasing incidence in renal allograft recipients transplanted in recent years.Kidney Int. 2001; 59: 732-737Abstract Full Text Full Text PDF PubMed Scopus (323) Google Scholar). Although to in many NODAT is by the associated with in immunosuppressive onset in the posttransplant period FG Pesavento TE Osei K Henry ML Ferguson RM Post-transplant diabetes mellitus: Increasing incidence in renal allograft recipients transplanted in recent years.Kidney Int. 2001; 59: 732-737Abstract Full Text Full Text PDF PubMed Scopus (323) Google Scholar). NODAT increasing of β-cell has also been et and to of in J 2010; PubMed Scopus Google Scholar). increase and and dyslipidemia and glucose by and Although other immunosuppressive or steroid to NODAT the risk of and an increased incidence of renal allograft pathology BL for the of kidney transplant J Transplant. Full Text Full Text PDF Scopus Google J et trial comparing versus 2008; PubMed Scopus Google Scholar). in the randomized trial of steroid the incidence of NODAT there a to glycemic control and of in the J et trial comparing versus 2008; PubMed Scopus Google Scholar). is to β-cell and to NODAT a and with of and (Ref. JJ in the diabetes to new PubMed Scopus Google are in with mycophenolate and the risk for the of glucose metabolism or NODAT is in the of with and 26% with cyclosporine at FFS Scheuermann E Rostaing L et al.DIRECT Investigators. Results of an international, randomized trial comparing glucose metabolism disorders and outcome with cyclosporine versus tacrolimus.Am J Transplant. 2008; 7: 1506-1514Crossref Scopus (493) Google Scholar). with studies from that a review that treatment of kidney transplant recipients with of cyclosporine of and graft in an cases of diabetes A versus as for kidney transplant 2005; PubMed Google Scholar). NODAT risk for is increased by and with or the of in have the risk between the A kidney of comparing and cyclosporine based significant in the of NODAT and hypertension, associated with and rejection graft with and cyclosporine in renal transplantation: kidney PubMed Scopus Google Scholar). 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This has been in other studies, in studies with however, the has been associated with a NODAT risk T A E et factors for of new-onset diabetes mellitus after kidney PubMed Scopus Google Scholar). that in the incidence of with and of with have a significant in NODAT to cyclosporine based regimens Y J et regimens are associated with cardiovascular and risk factors with cyclosporine in kidney transplant recipients and 2011; 91: PubMed Scopus Google et and of regimens in kidney transplant results of a study J Transplant. 2011; Scholar). be for kidney disease and transplantation from have been associated with an increased risk for however, results further evaluation T A E et factors for of new-onset diabetes mellitus after kidney PubMed Scopus Google A onset diabetes (NODAT) after kidney transplantation in kidney disease A 2011; of Scholar). has also been associated with an increased risk of NODAT to of J Jenssen T Hartmann A there a link between and new-onset diabetes of Transplant. 2005; PubMed Scopus Google Scholar). A of glucose metabolism and other CVD risk factors is with an glucose metabolism is A J Dotta et for the treatment and management of new-onset diabetes after Transplant. 2005; PubMed Scopus Google Scholar). that NODAT developed in of with on and the of and we an be is Refs. Hartmann A et diabetes in kidney transplant A J 2010; PubMed Scopus Google L et and risk factors of glucose metabolism disorders in kidney transplant of screening by oral glucose tolerance 2011; 91: PubMed Scopus Google Scholar). hyperglycemia or after kidney transplant has in to of with a risk for NODAT Y et between hyperglycemia and treatment after kidney transplantation and new onset diabetes J 2010; PubMed Scopus Google K Y of glucose metabolism in renal allograft and of diabetes mellitus Transplant. 2008; PubMed Scopus Google Scholar). BG posttransplant screening for and at and by A J Dotta et for the treatment and management of new-onset diabetes after Transplant. 2005; PubMed Scopus Google Scholar). as afternoon capillary BG self-testing the increases the of NODAT L Full Text Full Text PDF PubMed Scopus Google Scholar). As the from transplantation factors of this test in of posttransplant glucose and risk are by an at and an be an to and to address In with NODAT or glucose metabolism an between and be of or the of of the NODAT in of and β-cell be from glucose and and that in at 10 a of of glucose tolerance by J M Hartmann A K T Jenssen T The impact of and on glucose after renal Transplant. PubMed Scopus Google Scholar). prospective studies with are to the of on is an of and on and remain the to from glucose metabolism to relative risk E et in the incidence of diabetes with or PubMed Scopus Google Scholar). of and control has a improvement in glucose versus a in A K of in renal transplant recipients with 2008; PubMed Scopus Google Scholar). Renal transplant recipients have and after transplantation T J et in a transplant with new onset diabetes mellitus associated with Transplant. 2008; PubMed Scopus Google in to kidney J 2008; Full Text Full Text PDF PubMed Scopus Google Scholar). the of in the and treatment of NODAT has been and an is the effect on the of immunosuppressive and other with or at risk of NODAT, and of have been associated with glucose however, this increases the risk of and allograft J J A or for kidney transplant Scholar). seems to BL for the of kidney transplant J Transplant. Full Text Full Text PDF Scopus Google Scholar). with and to The of that and kidney transplant recipients a for have an increased risk of rejection D and of 2005; PubMed Scopus Google Scholar). has that of be and and D and of 2005; PubMed Scopus Google Scholar). are to the in the need for the of and the therapeutic therapeutic studies be D and of 2005; PubMed Scopus Google Scholar). with NODAT or at risk for of the of immunosuppressive consider the risk of graft rejection and cardiovascular a greater risk of NODAT and cyclosporine associated with hypertension, dyslipidemia and renal long-term outcome studies are FFS Scheuermann E Rostaing L et al.DIRECT Investigators. Results of an international, randomized trial comparing glucose metabolism disorders and outcome with cyclosporine versus tacrolimus.Am J Transplant. 2008; 7: 1506-1514Crossref Scopus (493) Google Scholar). CVD mortality after transplantation has fallen in the a in as the in cardiovascular death after kidney 2010; PubMed Scopus Google Scholar). this improvement in CVD outcomes is attributable to improvement in CVD risk management is between and increased and increased and increased Snyder JJ BL disease after renal transplantation: Results from the patient outcomes in renal transplantation 2011; 91: PubMed Scopus Google Scholar). 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Although there is of NODAT and there is a need for prospective to the incidence of NODAT with current immunosuppressive regimens and to be is glycemic control outcomes and the of hypoglycemic is Assessing the relative of in patient to and treatment of with NODAT, be by a in morbidity and an improvement in