Insulin lispro is as effective as regular insulin in optimising metabolic control and preserving b-cell function at onset of type 1 diabetes mellitus
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1 Diabetes Research and Clinical Practice 60 (2003) 153/159 Insulin lispro is as effective as regular insulin in optimising metabolic control and preserving b-cell function at onset of type 1 diabetes mellitus Mònica Recasens a,eva Aguilera a, Rosa Morínigo a, Roser Casamitjana b, Ferdinando Nicoletti c, Ramon Gomis a, Ignacio Conget a * a Endocrinology and Diabetes Unit, Hospital Clínic i Universitari, Villarroel 170, Barcelona, Spain b Hormonal Unit, IDIBAPS (Institut d Investigacions Biomèdiques August Pi i Sunyer), Hospital Clínic i Universitari, Barcelona, Spain c Department of Biomedical Sciences, Università degli Studi di Catania, Catania, Italy Received 5 September 2002; received in revised form 28 January 2003; accepted 3 February 2003 Abstract The aim of the study was to examine the effects of intensive insulin therapy using lispro on metabolic control, immunogenicity and b-cell function of newly diagnosed type 1 diabetic subjects in comparison with intensive insulin therapy using regular insulin. An open study was conducted in 45 newly diagnosed type 1 diabetic subjects. Patients were randomly assigned to intensive insulin therapy using insulin lispro (lispro) (lispro, n/22; 22.8 years) or intensive insulin therapy using regular insulin (regular) (regular, n/23; 24.4 years): three to five injections of subcutaneous rapid-acting insulin before meals and Neutral Protamine Hagedorn (NPH) before dinner/bed-time. GAD, IA2, insulin antibodies, basal and stimulated plasma C-peptide and HbA 1c were measured initially and at months 1, 4, 8 and 12. Daily blood glucose profiles tended to be lower in the lispro group, particularly values after breakfast, without reaching statistical significance. There were no differences in terms of HbA 1c throughout the study. The proportion of subjects achieving an HbA 1c B/6% at the end of the study was similar in both groups (regular 73.9%, lispro 68.0%). The number of mild hypoglycemic episodes tended to be lower with lispro, but not significantly. b-cell function was not significantly different in both groups. During follow-up there were no differences in antibodies, including IAAb. In summary, insulin lispro used in intensive insulin therapy is as effective as regular insulin in optimizing metabolic control and preserving b- cell function at diagnosis of type 1 diabetes. # 2003 Elsevier Science Ireland Ltd. All rights reserved. Keywords: Newly diagnosed type 1 diabetes; Insulin lispro; Regular insulin 1. Introduction * Corresponding author. Tel.: / ; fax: / address: iconget@clinic.ub.es (I. Conget). Preservation of b-cell function after diagnosis should be considered as one of the therapeutic goals in the management of newly diagnosed type 1 diabetes mellitus [1]. There is evidence that /03/$ - see front matter # 2003 Elsevier Science Ireland Ltd. All rights reserved. doi: /s (03)
2 154 M. Recasens et al. / Diabetes Research and Clinical Practice 60 (2003) 153/159 residual b-cell function could be beneficial in order to obtain optimal metabolic control, as well as to reduce the risk of hypoglycemia [1 /3]. Among the different intervention trials aiming to preserve endogenous insulin secretion, intensive insulin therapy, per se, has demonstrated the capacity, although transient, to delay the loss of b-cell function [4]. In addition to this, any attempt of immunomodulation at onset of the disease has been backed usually by exogenous insulin administration in an intensive manner [5]. The beneficial effect of intensive insulin therapy has been related to two main actions: (i) a reduction of glucotoxicity; and (ii) the induction of b-cell rest maintaining insulin-producing cells less susceptible to autoimmune attack [4,6 /8]. Conversely to the concerns related to risk and benefits of trials on immunotherapy at the onset of type 1 diabetic, there is no doubt that the safe achievement of near normoglycemia is a cornerstone in the treatment of newly-diagnosed type 1 diabetic subjects. One of the reasons why intensive insulin therapy in type 1 diabetic patients does not achieve sustained euglycemia is probably because of lessthan-satisfactory pharmacokinetics of subcutaneous injected regular insulin, which usually leads to inadequate control of postprandial blood glucose. Rapid-acting analogs have been developed to overcome this problem [9]. Insulin lispro is an insulin analog with a faster onset and a shorter duration of action than regular insulin [10,11]. There are randomized clinical trials that demonstrate lispro s efficacy in reducing postprandial glucose excursions in type 1 diabetes, reducing the number of hypoglycemic events and offering greater quality of life during intensified insulin therapy when compared with regular insulin [12 / 17]. Although the benefits and disadvantages of lispro insulin in the management of type 1 diabetes have been carefully explored, there is a lack of studies evaluating its potential utility in intensive insulin therapy at the onset of type 1 diabetes. In view of these characteristics of the lispro action profile it could be argued that more effective release of the b-cell from stress produced by postprandial glycemic challenge could represent added value of intensive therapy using lispro instead of regular insulin in order to preserve as long as possible insulin secretion capacity. Our study aimed to examine the effects of intensive insulin therapy using lispro on metabolic control, immunogenicity and b-cell function of newly diagnosed type 1 diabetic subjects in comparison with intensive insulin therapy using regular insulin. 2. Material and methods A 12-month follow-up open study was conducted in 45 newly diagnosed type 1 diabetic subjects admitted in our Endocrinology and Diabetes Unit. The study protocol was approved by the Hospital Clínic i Universitari ethics committee and informed consent was obtained from all the patients. Type 1 diabetes was diagnosed according to the National Diabetes Data Group criteria [18]. Patients were consecutively included in the study and after the correction of initial metabolic disturbances they were randomly assigned to lispro (n/22) or regular (n /23) insulin, which consisted of three to five daily doses (injections) of subcutaneous insulin: lispro or regular insulin before meals and Neutral Protamine Hagedorn (NPH) insulin before dinner/bed-time. Patients were instructed to inject human regular insulin 30 min before each of the main meals and lispro insulin immediately before eating. An extra dose of NPH insulin was added before breakfast or lunch when necessary according to premeal glucose targets. All patients received a diet adjusted to their age and body mass index (BMI), and insulin doses were regulated in order to maintain preprandial glucose between 3.9 and 7.0 mmol/l and postprandial glucose B/10 mmol/l based on 4 /6 daily capillary blood glucose determinations. While in hospital all the subjects participated in a 5-day education program for subjects with newly diagnosed type 1 diabetes Antibody measurements Glutamic acid decarboxylase antibodies (GA- DAb), tyrosine phosphatase antibodies (IA2Ab) and insulin autoantibodies (IAAb) were measured.
3 M. Recasens et al. / Diabetes Research and Clinical Practice 60 (2003) 153/ GADAb were determined by radiobinding assay and were considered positive when above 2 U/ml. The assay for GADAb achieved 100% sensitivity and 100% specificity in the 2nd GAD proficiency test. IA2Ab titers were measured in a radioimmunoassay and considered positive when above 0.8 U/ml. The interassay and intrassay coefficient of variation of IA2Ab determination were 7 and 5%, respectively. The upper limits of normal values for GADAb and IA2Ab were defined by the 99th percentile of antibodies measured in 110 nondiabetic subjects without a family history of type 1 diabetes. IAAb were measured using a radiobinding method. The upper normal limit of 1% was defined after the analysis of 500 samples from healthy controls. The interassay coefficient of variation of IAAb was 12% Assessment of pancreatic b-cell function A glucagon test was performed in the absence of hypoglycemia in the previous 48 h and only when fasting blood glucose values were between 5.0 and 8.0 mmol/l. Plasma C-peptide measurements were performed basally and 2, 4, 6, 8 and 10 min after the intravenous injection of 1 mg of glucagon. C- Peptide was determined using a commercially available kit (Bick Santeg, Germany; limit of detection mmol/l; intrassay coefficient of variation 2.6%; interassay coefficient of variation 4.4%). Basal and maximal values of C-peptide during the glucagon test were used as b-cell function parameters. Preservation of b-cell function was assessed by measuring the difference between maximum C-peptide at 1 year of followup and maximum C-peptide at diagnosis of type 1 diabetes Hypoglycemic events In order to quantitate hypoglycemic episodes, these were classified as severe or mild and estimated from subject s diaries of self-capillary blood glucose monitoring. Mild hypoglycemic events were defined as symptoms or signs associated with hypoglycemia experienced by the patient and self-treated without the need of assistance from a third party or a blood glucose measurement of B/3.3 mmol/l. Severe hypoglycemic events were defined as those associated with neuroglycopenia severe enough to require treatment from a third party Follow-up Patients were visited by the same team every 2 weeks during the first 3 months, and monthly thereafter until 12 months of follow-up. At each visit weight glucose profiles, daily rapid acting/ NPH insulin doses, number of NPH insulin injections and hypoglycemic events were recorded. Patients were reinstructed concerning glucose goals, and self-monitoring glucose control when necessary. Glucagon test and antibody measurements were determined initially and at months 1, 4, 8 and 12. HbA 1c was determined by high performance liquid chromatography (HPLC, HA 8121, Menarini Diagnostici, Firenze, Italy) at the same intervals (normal range 3.4 /5.5%) Statistical analysis Results are presented as mean9/sd. An analysis of variance considering repeated measures, with time and treatment as covariates, was used for multiple comparisons. Comparisons between proportions were done with a x 2 -test. Changes from baseline values at the end of the study were analyzed in the regular and lispro groups and compared by Wilcoxon Signed-Rank test. A P value B/0.05 was considered statistically significant. All statistical calculations were performed by the Statistical Package for Social Science for personal computers. 3. Results Forty-five subjects, 23 randomised to regular and 22 to lispro were included. Clinical, metabolic and immunological characteristics of the two groups at baseline are shown in Table 1. There was no statistically significant difference in any parameter. Mean daily blood glucose profiles tended to be lower in the lispro group, particularly values after
4 156 M. Recasens et al. / Diabetes Research and Clinical Practice 60 (2003) 153/159 Table 1 Baseline characteristics of the study groups Regular Lispro Number of subjects Age (year) 22.89/ /5.7 Sex (M) BMI (kg/m 2 ) 20.69/ /0.9 HbA 1c (%) 11.49/ /2.4 Weeks from diagnosis 8.19/ /3.8 H/K/KA (n) 3/17/3 6/11/5 GADAb (/) IA2Ab (/) IAAb (/) 7 6 Data are shown as mean9/sd. Regular, intensive insulin therapy using regular insulin; Lispro, intensive insulin therapy using lispro insulin; BMI, body mass index; H/K/KA, Hyperglycaemia/ketosis/ketoacidosis. breakfast, without reaching statistical significance (Fig. 1). After 4 months (1.3 vs. 0.9 episodes/week in regular and lispro, respectively) and during the rest of the follow-up (12 months, 0.8 vs. 0.3 episodes/week in regular and lispro, respectively), the number of mild hypoglycemic episodes tended to be lower with lispro. No severe hypoglycemic episodes occurred in either group during the follow-up period. HbA 1c levels declined toward normal values shortly after treatment was initiated in both group (Fig. 2). There were no significant differences throughout the study between regular and lispro groups (Fig. 2). The proportion of Fig. 2. HbA 1c during the follow-up period. Regular, intensive insulin therapy using regular insulin; Lispro, intensive insulin therapy using insulin lispro. Mean9/SD. subjects achieving an HbA 1c B/6% at the end of the study was similar in both groups (regular 73.9%, lispro 68.0%). Neither total exogenous insulin requirements nor the proportion of rapidacting insulin was different in the experimental groups (Fig. 3). It was necessary to add an extra dose of NPH insulin before lunch in six and three patients in the regular and lispro groups, respectively in order to optimize glucose profiles. Bedtime injection of NPH insulin was used in four and five subjects in regular and lispro groups, respectively. All subjects needed either regular or lispro before dinner to control postprandial glucose. At the end of the follow-up, body weight increased similarly in both groups of treatment (7.19/5.2 vs. 5.19/3.5 kg, regular and lispro, respectively). Fig. 1. Self-monitoring capillary blood glucose profiles in the experimental groups. Regular, intensive insulin therapy using regular insulin; Lispro, intensive insulin therapy using insulin lispro. Mean9/SD. Fig. 3. Insulin doses during the follow-up period. Regular, intensive insulin therapy using regular insulin; Lispro, intensive insulin therapy using insulin lispro. Mean9/SD.
5 M. Recasens et al. / Diabetes Research and Clinical Practice 60 (2003) 153/ Fasting C-peptide (0.279/0.12; 0.279/0.16 nmol/ l regular and lispro groups, respectively) and maximal-stimulated C-peptide (0.489/0.24; 0.469/ 0.22 nmol/l regular and lispro groups, respectively) were comparable at baseline. During follow-up, there were no significant differences in b-cell function surrogates in the two treatment groups (Figs. 4 and 5). Likewise, changes in both fasting and maximal glucagon-stimulated C-peptide from baseline to the end of the study did not differ between experimental groups. At baseline, the frequency of positivity for GADAb, IA2Ab and IAAb was similar in the regular and lispro groups (Table 1). During follow-up no differences in antibody titer behavior were observed. At the end of the study, IAAb level was 189/12% in the regular and 229/12% in the lispro group. 4. Discussion In our study, treatment of newly diagnosed type 1 diabetic subjects using intensive insulin therapy including either regular or lispro insulin is equally effective in achieving satisfactory metabolic control and preserving endogenous insulin production. Trials aimed at preservation of b-cell function in newly diagnosed type 1 diabetes are usually designed to provide insulin replacement therapy to maintain metabolic control as good as possible Fig. 4. Fasting C-peptide concentrations during the study. Regular, intensive insulin therapy using regular insulin; Lispro, intensive insulin therapy using insulin lispro. Mean9/SD. Fig. 5. Maximal glucagon stimulated C-peptide during followup. Regular, intensive insulin therapy using regular insulin; Lispro, intensive insulin therapy using insulin lispro. Mean9/ SD. [5]. In fact, the improvement of glycemic control is one of the main goals in the treatment of type 1 diabetes from the onset of the disease and it is associated per se with preservation of residual insulin secretion capacity [2]. Reciprocally, maintenance of residual C-peptide secretion facilitates the achievement of optimal metabolic control. An abnormal first-phase insulin response to intravenous glucose is one of the first recognizable metabolic alterations during the development of type 1 diabetes, leading to abnormal oral glucose tolerance in the final steps of the natural history of the disease [19 /21]. When type 1 diabetes is clinically evident and after treatment of the acute metabolic disturbances at the time of diagnosis, intensive insulin therapy is mainly addressed to mealtime glycemic control. Since the specific pharmacokinetic properties of insulin lispro achieve better control of the postprandial rise in plasma glucose than regular insulin [12], it could be considered as an alternative to regular insulin in order to release the b-cell from the strain of mealtime challenges. In our study, mean daily blood glucose profiles were not different using either lispro or regular insulin, although they tended to be lower postprandially using the analog, particularly after breakfast as has been observed previously in other studies performed in children [22]. However, we could not find differ-
6 158 M. Recasens et al. / Diabetes Research and Clinical Practice 60 (2003) 153/159 ences in terms of HbA 1c during the follow-up, with a tendency towards less hypoglycemic events in lispro than in the regular group. This finding was one of the advantages observed in a recent report evaluating the impact of insulin lispro on glycemic control and the number of hypoglycemic episodes [23]. In addition to this, insulin lispro did not show beneficial effects on residual C-peptide concentration throughout the study. In large trials in which subjects with long-term type 1 diabetes were changed from regular to insulin lispro, the analog failed to improve HbA 1c if no adjustment in basal insulin was performed in order to control the next premeal blood glucose level [24]. In our study, preprandial glycemic profiles of subjects on lispro were similar to those observed in the regular group and thus there was no need to add additional NPH insulin. It could be argued, that the beneficial effect of lispro on postprandial-induced b-cell stress could be potentially counterbalanced by the necessary compensation of increasing blood glucose before the next meal. However, this was not the case in our study. The time course and titers of GADAb and IA2Ab did not differ between the experimental groups during follow-up. In terms of immunogenicity, and in comparison with studies performed in previously treated type 1 diabetic patients, in our study the concentration of insulin antibodies induced by insulin lispro did not differ from regular insulin [25,26]. Higher patient preference and treatment satisfaction have been demonstrated for insulin lispro when comparing with regular insulin, this being mainly attributed to greater flexibility and convenience related to immediate injections before meals. In our study, we did not specifically address this subject, however, both flexibility and convenience could be especially welcome in the initiation and management of intensive insulin therapy at onset of type 1 diabetes [15,17]. In conclusion, our data show that both insulin lispro and regular insulin, used in intensive insulin therapy, are comparable in terms of efficacy in optimizing metabolic control and in preserving b- cell function in newly diagnosed type 1 diabetic subjects. References [1] H. Kolb, E.A. Gale, Does partial preservation of residual beta-cell function justify immune intervention in recent onset Type I diabetes?, Diabetologia 44 (2001) 1349/1353. [2] Effect of intensive therapy on residual beta-cell function in patients with type 1 diabetes in the diabetes control and complications trial. A randomized, controlled trial. The Diabetes Control and Complications Trial Research Group, Ann. Intern. Med. 128 (1998) 517/523. [3] Effects of age, duration and treatment of insulin-dependent diabetes mellitus on residual beta-cell function: observations during eligibility testing for the Diabetes Control and Complications Trial (DCCT). The DCCT Research Group, J. Clin. Endocrinol. Metab 65 (1987) 30/ 36. [4] S. Madsbad, T. Krarup, L. Regeur, O.K. Faber, C. Binder, Effects of strict blood glucose control on residual beta-cell function in insulin dependent diabetics, Diabetologia 20 (1981) 530/534. [5] J. Vidal, M. Fernández Balsells, G. Sesmilo, et al., Effects of nicotinamide and intravenous insulin therapy in newly diagnosed type 1 diabetes, Diabetes Care 23 (2000) 360/ 364. [6] M.A. Bowman, L. Campbell, B.L. Darrow, T.M. Ellis, A. Suresh, M.A. Atkinson, Immunological and metabolic effects of prophylactic insulin therapy in the NOD-scid/ scid adoptive transfer model of IDDM, Diabetes 45 (1996) 205/208. [7] S.C. Shaa, J.I. Malone, E.N. Simpson, A randomized trial on intensive insulin therapy in newly diagnosed insulindependent diabetes mellitus, N. Engl. J. Med. 320 (1989) 550/554. [8] J.C. Leahy, Natural history of beta cell dysfunction, Diabetes Care 13 (1990) 992/1010. [9] G.B. Bolli, R. Di Marchi, G.D. Park, S. Pramming, V.A. Koivisto, Insulin analogs and their potential in the management of diabetes mellitus, Diabetologia 42 (1999) 1151/1167. [10] D.C. Howey, R.R. Bowser, R.L. Brunelle, S. Vignati, Lys (B28), Pro (B29)] human insulin. A rapidly absorbed analog of human insulin, Diabetes 43 (1996) 396/402. [11] E. Tolone, C. Fanelli, A.M. Rombotti, et al., Pharmacokinetics, pharmacodynamics and glucose counterregulation following subcutaneous injection of the monomeric insulin analog [Lys (B28), Pro (B29)] in IDDM, Diabetologia 37 (1994) 713/720. [12] S. Pampanelli, E. Torlone, C. Lalli, et al., Improved postprandial metabolic control after subcutaneous injection of a short-acting insulin analog in IDDM of short duration with residual pancreatic b-cell function, Diabetes Care 18 (1995) 1452/1459. [13] J.H. Anderson, R.L. Brunelle, P. Keoane, Mealtime treatment with insulin analog improves postprandial hyperglycemia and hypoglycemia in patients with noninsulin-dependent diabetes mellitus, Arch. Intern. Med. 157 (1997) 1249/1255.
7 M. Recasens et al. / Diabetes Research and Clinical Practice 60 (2003) 153/ [14] J.H. Anderson, R.L. Brunelle, V.A. Koivisto, M.E. Trautmann, S. Vignati, R. Di Marchi, Reduction of postprandial hyperglycemia and frequency of hypoglycemia in IDDM patients on insulin-analog treatment, Diabetes 46 (1997) 265/270. [15] P.A. Jansson, P. Ebeling, U. Smith, et al., Improved glycemic control can be better mantained with insulin lispro than with human regular insulin, Diabetes Nutr. Metab. 11 (1998) 194/199. [16] S.R. Heller, S.A. Amiel, P. Mansell, Effect of the fastacting insulin analog lispro on the risk of nocturnal hypoglycemia during intensified insulin therapy, Diabetes Care 22 (1999) 1607/1611. [17] J.G. Kotsanos, L. Vignati, W. Huster, et al., Health related quality of life and insulin lispro, Diabetes Care 20 (1997) 948/958. [18] National Diabetes Data Group, Classification and diagnosis of diabetes mellitus and other categories of glucose intolerance, Diabetes 28 (1979) 1039/1057. [19] C. Rodriguez-Villar, I. Conget, J.M. Gonzalez-Clemente, et al., Effects of insulin administration on beta-cell function in subjects at high risk for type I diabetes mellitus, Metabolism 45 (1996) 873/875. [20] C. Rodriguez-Villar, I. Conget, R. Casamitjana, G. Ercilla, R. Gomis, Effects of insulin administration in a group of high-risk, non-diabetic, first-degree relatives of Type 1 diabetic patients: an open pilot trial, Diabetes Med. 16 (1999) 160/163. [21] P.J. Bingley, Interactions of age, islet cell antibodies, insulin autoantibodies, and first-phase insulin response in predicting risk of progression to IDDM in ICA/ relatives: the ICARUS data set. Islet Cell Antibody Register Users Study, Diabetes 45 (1996) 1720/1728. [22] L.C. Deeb, J.H. Holcombe, R. Brunelle, et al., Insulin lispro lowers postprandial glucose in prepubertal children with diabetes, Pediatrics 108 (2001) 1175/1179. [23] S.K. Garg, J.H. Anderson, S.V. Perry, et al., Long-term efficacy of humalog in subjects with Type 1 diabetes mellitus, Diabetes Med. 16 (1999) 384/387. [24] P. Ebeling, P.A. Jansson, U. Smith, C. Lalli, G.B. Bolli, V.A. Koivisto, Strategies toward improved control during insulin lispro therapy in IDDM. Importance of basal insulin, Diabetes Care 20 (1997) 1287/1289. [25] L. Jovanovic, S. Ilic, D.J. Pettitt, et al., Metabolic and immunologic effects of insulin lispro in gestational diabetes, Diabetes Care 22 (1999) 1422/1427. [26] N.S. Fineberg, S.E. Fineberg, J.H. Anderson, M.A. Birkett, R.G. Gibson, S. Hufferd, Immunologic effects of insulin lispro [Lys (B28), Pro (B29) human insulin] in IDDM and NIDDM patients previously treated with insulin, Diabetes 45 (1996) 1750/1754.
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