Treatment of young patients with HNF1A mutations (HNF1A MODY)
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1 Short Report: Genetics DOI: /dme Treatment of young patients with HNF1A mutations (HNF1A MODY) K. Raile 1, E. Schober 2, K. Konrad 3, A. Thon 4, J. Grulich-Henn 5, T. Meissner 6,J.W olfle 7, N. Scheuing 8 and R. W. Holl 8 for the DPV Initiative the German BMBF Competence Network Diabetes Mellitus 1 Experimental and Clinical Research Center, Charite, Berlin, Germany, 2 Department of Paediatrics, Medical University of Vienna, Austria, 3 Paediatric Endocrinology and Diabetes, Department of Paediatrics II, University Children s Hospital Essen, 4 University Children s Hospital, MHH, Hannover, 5 Children s Hospital, University of Heidelberg, 6 Department of General Paediatrics, Neonatology and Pediatric Cardiology, University Children s Hospital D usseldorf, 7 Paediatric Endocrinology Division, Children s Hospital, University of Bonn and 8 Institute of Epidemiology and Medical Biometry, University of Ulm, Germany Accepted 2 December 2014 Abstract Aim Children and adolescents with a molecular diagnosis of HNF1A MODY should be treated with oral sulfonylurea according to current International Society for Pediatric and Adolescent Diabetes (ISPAD) guidelines. Methods We surveyed the German Austrian DPV database of people and included 114 patients with a confirmed molecular genetic diagnosis of HNF1A mutation and diabetes onset at below age 18 years. We analysed hypoglycaemic episodes, metabolic control (HbA 1c ) and other clinical variables according to treatment groups. Results People with HNF1A MODY were included and analysed according to treatment with insulin alone (n = 34), sulfonylurea (n = 30), meglitinides (n = 22) or lifestyle (n = 28). In those receiving any drug treatment (n = 86), severe hypoglycaemia did not occur with meglitinide and was highest (at 3.6 events per 100 patient-years) with insulin. HbA 1c was highest with insulin treatment (insulin = 58 mmol/mol, 7.5%; sulfonylurea = 55 mmol/mol, 7.2%; meglitinides = 52 mmol/mol, 6.9%; P = 0.008), whereas weight (BMI SD score), serum lipids and blood pressure were not different. Conclusions Of note, 40% of people with HNF1A MODY and medical treatment were receiving insulin alone and thus were not being treated in line with up-to-date International Society for Pediatric and Adolescent Diabetes/ International Diabetes Federation guidelines, despite insulin treatment being associated with worse metabolic control and the risk of hypoglycaemia. The unlicensed use of oral drugs in patients below age 18 years and adherence by both doctors and patients to the initial insulin treatment might contribute to this finding. Diabet. Med. 32, (2015) Introduction HNF1A MODY (MIM #600496) is caused by a heterozygous gene defect of the transcription factor HNF1a, which leads to a progressive malfunction in glucose-dependent insulin secretion [1]. HNF1a belongs to a complex, islet-cell-specific regulatory circuit that is formed by the transcription factors HNF4a, HNF6 and HNF1b. However, this rare diabetes type explains only up to 4% of all cases in people aged < 18 years [2 4]. If left untreated, people with HNF1A MODY develop severe insulin deficiency and hyperglycaemia, with a high risk of micro- and macrovascular diabetic complications [5]. Because people with HNF1A Correspondence to: Klemens Raile. klemens.raile@charite.de mutations respond very well to low doses of sulfonylurea [6,7], changing their treatment from insulin to sulfonylurea has been suggested [8]. Recently, the prevalence of MODY gene variants has been systematically studied in people with non-immune diabetes followed in the large SEARCH for Diabetes in Youth cohort. HNF1A MODY was the most frequent gene defect in those aged younger than 20 years in the USA, and most of those with later proven MODY gene mutations had been misdiagnosed as having Type 1 diabetes and incorrectly treated with insulin [3]. In addition, meglitinide (nateglinide and repaglinide) leads to a rapid and transient increase in insulin secretion [9] and good performance in adolescents with HNF1A MODY has recently been suggested [10]. The International Society for Pediatric and Adolescent Diabetes/ 526
2 Research article DIABETICMedicine What s new? The current International Society for Pediatric and Adolescent Diabetes/International Diabetes Federation (ISPAD/IDF) guidelines published in 2009 suggest switching patients with profen HNF1A mutation (HNF1A MODY) from insulin to sulfonylurea. Despite this, 40% of HNF1A patients with paediatricand adolescent-onset diabetes continued to receive insulin treatment in Germany and Austria. Insulin treatment was associated with higher HbA 1c and a higher risk of hypoglycaemia. International Diabetes Federation (ISPAD/IDF) guidelines recommend changing drug treatment from insulin to sulfonylurea as soon as a molecular diagnosis of HNF1A mutation is confirmed [11]. Because none of these oral drugs is licensed for use in children and adolescents, we aimed to accrue further information on the utility of the oral antidiabetic drugs sulfonylurea or meglitinides compared with insulin in patients with HNF1A MODY and paediatric disease onset. Participants and methods Study design and study population We analysed the German and Austrian DPV database [12]. Members prospectively document treatment and outcome measures of routine diabetes care using DPV software. Twice a year, locally collected data are anonymized and transmitted for central plausibility checks and analyses. Inconsistent data are reported back to the referring centre for validation and correction. In total, 169 German and Austrian diabetes centres that regularly report on Mendelian diabetes diagnosis participated in this DPV database project. Data were analysed from the September 2012 data report, which includes people, with last follow up not earlier than If a specific genetic defect in HNF1A was found, the attending physician registered the patients as having HNF1A MODY. Centres who registered people with HNF1A MODY were contacted and requested to confirm the diagnosis. Known HNF1A polymorphisms that had been initially misdiagnosed as HNF1A MODY were eliminated [12] and all variants available from HNF1A patients are given in the Supporting Information (Table S1). We focused on patients with HNF1A MODY diagnosed before the age of 18 years. Along with genetic diagnosis, we analysed current age, age at diagnosis, metabolic control, islet autoantibodies, hypoglycaemia and the presence of complications (retinopathy and nephropathy) for all patients. Medical treatment was classified as: (1) insulin; (2) oral anti-diabetic medication (sulfonylurea, meglitinides and biguanides); and (3) lifestyle/dietary interventions. The study was approved by the ethics committee of the University of Ulm. Statistical analysis We used SAS statistical software 9.3 (SAS Institute Inc., Cary, NC, USA). Mean, interquartile range and standard deviation (SD) of variables was computed. Significant differences (P < 0.05) between treatment groups of patients with HNF1A MODY were analysed using Wilcoxon s test for quantitative variables and the chi-square test for nonparametric variables. Where appropriate, P-values were adjusted for multiple testing using the Bonferroni step-down method. Results We identified 114 people with HNF1A MODY and 42 different mutations in HNF1A were registered. Of those, 20 were novel and were predicted to have a disease-causing effect (Table S1); compared with known mutations, we found no difference in clinical features. Of 114 people in total, 86 were treated with glucose-lowering medication (Table 1); of these, 34 (30%) still had insulin injections, 30 (27%) received sulfonylurea and 22 (19%) meglitinide. Among those receiving oral drugs, 14 of 30 on sulfonyurea and 9 of 22 on meglitinides had additional insulin treatment. The remaining 28 (24%) still had good metabolic control with dietary intervention alone. The ISPAD/IDF guidelines recommend first-line use of oral sulfonylurea, but one third of patients were still being treated with insulin alone (Table 1). We analysed the impact of drug treatment and found overall higher HbA 1c in association with insulin treatment, whereas lipids, BMI and blood pressure were similar in all groups (data not shown). We included young people with diabetes of short duration and thus found no retinopathy or diabetic nephropathy in these patients (data not shown). Severe hypoglycaemia was defined as unconsciousness, convulsions or being unable to take glucose without help from others. We found no hypoglycaemia with unconsciousness in any patient, but episodes requiring help from others were highest in those receiving insulin alone or in combination with oral drugs; this complication did not occur in any of the patients treated with meglitinides or sulfonylurea alone. Finally, we also tested whether patients with HNF1A mutations and at least one positive autoantibody (GAD-A, IA-2-A, IAA or ICA) had different clinical features and therefore might represent a subgroup of less pathogenic HNF1A variants but Type 1 diabetes. Overall, we found no association with antibody positivity and metabolic control, treatment regimen or risk of having severe hypoglycaemia (Table 1 and data not shown). 527
3 Treatment in HNF1A MODY K. Raile et al. Table 1 Clinical and metabolic findings in young patients (diagnosis before 18 years of age) with HNF1A-MODY classified along with their medical treatment. Drug treatment (n = 86) Sulfonylurea (n = 30) Meglitinides (n = 22) Clinical parameters Insulin alone (n = 34) Alone (n = 16) + Insulin (n = 14) Alone (n = 13) + Insulin (n = 9) Lifestyle alone (n = 28) P* Demographic and clinical characteristics Female (%) Age at last visit (years) 17.9 ( ) 16.7 ( ) 15.5 ( ) 17.1 ( ) 17.4 ( ) 14.9 ( ) 0.21 Age at diagnosis (years) 12.1 ( ) 12.9 ( ) 12.3 ( ) 13.6 ( ) 12.8 ( ) 10.2 ( ) 0.45 Diabetes duration (years) 5.8 ( ) 3.8 ( ) 3.2 ( ) 3.4 ( ) 4.6 ( ) 4.7 ( ) 0.22 Diabetes autoantibodies One beta cell AB+ve 18% (6/34) 31% (5/16) 7% (1/14) 8% (1/13) 11% (1/9) 21% (6/28) Two beta cell AB+ve 0% (0/34) 6% (1/16) 7% (1/14) 8% (1/13) 0 0% (0/28) 0.65 GAD-A+ve 3% (1/34) 6% (1/16) 0% (0/14) 8% (1/13) 0% (0/9) 4% (1/28) n.d. IA-2-A+ve 0% (0/34) 12% (2/16) 7% (1/14) 0% (0/13) 11% (1/9) 4% (1/28) n.d IAA+ve 9% (3/34) 19% (3/16) 7% (1/14) 0% (0/13) 11% (1/9) 14% (4/28) n.d ICA+ve 6% (2/34) 0% (0/16) 0% (0/7) 8% (1/13) 0% 0% (0/28) n.d Metabolic control HbA 1c (mmol/mol; %) 58 (44 67); 7.5 ( ) 49 (40 57); 6.7 ( ) 63 (49 74); 7.9 ( ) 51 (41 55); 6.8 ( ) 55 (49 63); 7.2 ( ) 43 (32 49); 6.1 ( ) Weight BMI (SD score) 0.77 ( ) 0.63 ( ) 0.85 ( ) 0.67 ( ) 0.78 ( 0.10 to 1.6) 0.01 ( 0.7 to 1.2) 0.11 Severe hypoglycaemic event (1/100 patient-years) Help from others needed Unconsciousness All values are means and interquartile range or SD, where appropriate. *Significance values and corrected P for multiple testing (Bonferroni-step-down). 528
4 Research article DIABETICMedicine Discussion Any individual with either Type 1 or Type 2 diabetes that has a suggestive family history or atypical, clinical features should be suspected of having MODY. Recently, a systematic analysis of the SEARCH for Diabetes in Youth database showed that HNF1A MODY is the most frequent monogenic diabetes form among young people with nonimmune diabetes; most of had not been properly diagnosed [3]. In our survey, we were able to identify 42 HNF1A mutations, including 20 novel ones. Predicting diseasecausing probability using bioinformatic prediction methods (MutationTaster, PolyPhen2) indicated a high pathogenic probability in at least one model (Table S1). Furthermore, as soon as the molecular diagnosis of HNF1A MODY had been made, the majority of such patients could be successfully transferred to sulfonylureas without deterioration but improvement in glycaemic control [13,14]. Insulin therapy is not appropriate for patients carrying a HNF1A mutation and conversion from insulin to sulfonylurea is currently recommended [11]. Nevertheless, HNF1A MODY is rare and adherence to insulin therapy that patients and their diabetes care professionals believe to be a lifelong requirement might still be present in both those with HNF1A MODY and diabetes care professionals. Twenty-three of the 52 patients already receiving sulfonylurea or meglitinides had additional insulin treatment and thus ~45% of patients might not respond to oral drugs alone. Unfortunately, sulfonylureas and meglitinides are not approved for use in patients aged < 18 years and we were therefore particularly interested in how physicians in Germany and Austria manage these patients. We analysed meglitinides (nateglinide and repaglinide) independently, because these drugs exhibit an optimum effect on postprandial glucose levels and have a low risk of inducing hypoglycaemia. To date, only case reports are available to assess these compounds in children and adolescents [10] and we found that currently almost 20% of people with HNF1A MODY are receiving these drugs. Compared with insulin and similar to sulfonylurea, meglitinides resulted in good metabolic control without any risk of severe hypoglycaemia and unchanged profile of major risk factors for micro- and macrovascular complications. The DPV database was analysed 3 years earlier [10]. At that time, 44 patients with HNF1A MODY were identified, with a lower rate of drug treatment (43%). Interestingly, insulin, with or without other drugs was given to approximately one third, thus the proportion of patients treated with insulin alone has remained almost unchanged despite publication of the ISPAD guidelines in 2009 [12]. Furthermore, it has been stated, that HNF1A mutation carriers respond with an overshooting insulin secretion in response to sulfonylureas [6] and this state of affairs has resulted in cautionary advice [8]. Our current data also suggest that use of sulfonylurea and meglitinides is safe and has no relevant risk for severe hypoglycaemia, with single events being observed with insulin alone or in combination with sulfonylurea. Insulin secretagogues have different effects on insulin secretion, largely reflecting their pharmacokinetics and ability to bind to the ATP-dependent potassium channel. In people with Type 2 diabetes, repaglinide and the short-acting sulfonylurea glipizide stimulated early and rapid insulin secretion much stronger than glibenclamide [15]. Insulin secretion stimulated by these drugs was still glucose-sensitive and could adapt to individual meal size and fasting glucose. These responses are in strong contrast to subcutaneous insulin injections. How sulfonylurea and meglitinides stimulate insulin secretion by specific binding to the SUR1 subunit of the ATP-dependent potassium channel and whether this affects good performance of sulfonylurea or meglitinide in people with HNF1A MODY, remains unclear. Glibenclamide binds to both the A and B sites, whereas meglitinides bind more specifically to the B site (repaglinide) or the A site (nateglinide) of SUR1 [16]. In conclusion, we were able to demonstrate that oral drugs are more effective than insulin in patients with paediatric-onset HNF1A MODY. Considering the pharmacodynamics of sulfonylurea versus meglitinides, the latter might have lower risk of hypoglycaemia and postprandial hyperglycaemia. However, our current analysis indicates that 40% of patients with HNF1A MODY were still receiving insulin alone and thus were not treated in accordance with up-to-date ISPAD/IDF guidelines. Unlicensed use of oral drugs in patients aged below 18 years and the adherence of both doctors and patients to insulin treatment once initiated might contribute to this finding. Funding sources The Bundesministerium f ur Bildung und Forschung (BMBF) funded the study by supporting the Competence Network Diabetes (grant 01GI1106). The Dr B urger B using Stiftung, Kaiserslautern, Germany also supported the study. Klemens Raile was funded by the Experimental and Clinical Research Center, a joint collaboration of Charite and Max-Delbr uck-center for Molecular Medicine. Conflicting interests None declared. Acknowledgements Maolian Gong from the Experimental and Clinical Research Center evaluated pathogenicity of new HNF1A variants. We 529
5 Treatment in HNF1A MODY K. Raile et al. thank all physicians of the Austrian and German pediatric diabetes centres contributing to the DPV database. All contributing centres are listed in the Supporting Information. References 1 Yamagata K, Oda N, Kaisaki PJ, Menzel S, Furuta H, Vaxillaire M et al. Mutations in the hepatocyte nuclear factor 1alpha gene in maturity-onset diabetes of the young (MODY3). Nature 1996; 384: Schober E, Rami B, Grabert M, Thon A, Kapellen T, Reinehr T et al. Phenotypical aspects of maturity-onset diabetes of the young (MODY diabetes) in comparison with Type 2 diabetes mellitus (T2DM) in children and adolescents: experience from a large multicentre database. Diabet Med 2009; 26: Gilliam LK, Pihoker C, Ellard S, Hattersley AT, Dabelea D, Davis C et al. Prevalence, characteristics and clinical diagnosis of maturity onset diabetes of the young due to mutations in HNF1A, HNF4A, and glucokinase: results from the SEARCH for Diabetes in Youth. J Clin Endocrinol Metab 2013; 98: Fendler W, Borowiec M, Baranowska-Jazwiecka A, Szadkowska A, Skala-Zamorowska E, Deja G et al. Prevalence of monogenic diabetes amongst Polish children after a nationwide genetic screening campaign. Diabetologia 2012; 55: Isomaa B, Henricsson M, Lehto M, Forsblom C, Karanko S, Sarelin L et al. Chronic diabetic complications in patients with MODY3 diabetes. Diabetologia 1998; 41: Hansen T, Eiberg H, Rouard M, Vaxillaire M, Moller AM, Rasmussen SK et al. Novel MODY3 mutations in the hepatocyte nuclear factor 1alpha gene: evidence for a hyperexcitability of pancreatic beta-cells to intravenous secretagogues in a glucosetolerant carrier of a P447L mutation. Diabetes 1997; 46: Pearson ER, Liddell WG, Shepherd M, Corrall RJ, Hattersley AT. Sensitivity to sulphonylureas in patients with hepatocyte nuclear factor 1alpha gene mutations: evidence for pharmacogenetics in diabetes. Diabet Med 2000; 17: Hattersley A, Bruining J, Shield J, Njolstad P, Donaghue KC. The diagnosis and management of monogenic diabetes in children and adolescents. Pediatr Diabetes 2009; 10(Suppl 12): Cozma LS, Luzio SD, Dunseath GJ, Underwood PM, Owens DR. Beta-cell response during a meal test: a comparative study of incremental doses of repaglinide in type 2 diabetic patients. Diabetes Care 2005; 28: Becker M, Galler A, Raile K. Meglitinide analogues in adolescent patients with HNF1A MODY (MODY 3). Pediatrics 2014; 133: e775 e Hattersley A, Bruining J, Shield J, Njolstad P, Donaghue K. ISPAD Clinical Practice Consensus Guidelines The diagnosis and management of monogenic diabetes in children. Pediatr Diabetes 2006; 7: Awa WL, Thon A, Raile K, Grulich-Henn J, Meissner T, Schober E et al. Genetic and clinical characteristics of patients with HNF1A gene variations from the German-Austrian DPV database. Eur J Endocrinol 2011; 164: Shepherd M, Shields B, Ellard S, Rubio-Cabezas O, Hattersley AT. A genetic diagnosis of HNF1A diabetes alters treatment and improves glycaemic control in the majority of insulin-treated patients. Diabet Med 2009; 26: Shepherd M, Hattersley AT. I don t feel like a diabetic any more : the impact of stopping insulin in patients with maturity onset diabetes of the young following genetic testing. Clin Med 2004; 4: Cozma LS, Luzio SD, Dunseath GJ, Langendorg KW, Pieber T, Owens DR. Comparison of the effects of three insulinotropic drugs on plasma insulin levels after a standard meal. Diabetes Care 2002; 25: Winkler M, Stephan D, Bieger S, Kuhner P, Wolff F, Quast U. Testing the bipartite model of the sulfonylurea receptor binding site: binding of A-, B-, and A + B-site ligands. J Pharmacol Exp Ther 2007; 322: Supporting Information Additional Supporting Information may be found in the online version of this article: Table S1. HNF1A mutations documented in the DPV database. Document S1. The following diabetes centres contributed anonymized patient data for this project. 530
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