Skip to main content
Erschienen in: Journal of Medical Case Reports 1/2016

Open Access 01.12.2016 | Case report

The effects of liraglutide on both hypereosinophilic insulin allergy and the characteristics of anti-insulin antibodies in type 2 diabetes mellitus: a case report

verfasst von: Hiroyuki Hirai, Emi Ogata, Nobuyuki Kikuchi, Teruyuki Kohno, Noritaka Machii, Koji Hasegawa, Tsuyoshi Watanabe, Hiroaki Satoh

Erschienen in: Journal of Medical Case Reports | Ausgabe 1/2016

Abstract

Background

Liraglutide is one of the glucagon-like peptide-1 analogs; there are only a few reports of liraglutide being used for the treatment of insulin allergy. Furthermore, anti-insulin immunoglobulin G antibodies are occasionally detected in patients with diabetes. Hence, we report a case in which switching to liraglutide therapy ameliorated both the symptoms of insulin allergy with hypereosinophilia and the characteristics of insulin antibodies in a patient with type 2 diabetes mellitus.

Case presentation

We present the case of a 70-year-old Japanese man with type 2 diabetes who developed insulin allergy with hypereosinophilia. Anti-insulin antibodies, high glycated hemoglobin levels (approximately 12 %), and high serum insulin levels were detected. Because a change in his insulin treatment was inefficient, treatment with liraglutide to protect residual insulin secretion was started, resulting in improvements in his insulin allergy, serum glycated hemoglobin, insulin, and eosinophil levels. Scatchard plots revealed decreased binding capacity and increased affinity constant for high affinity sites of anti-insulin antibodies.

Conclusions

Liraglutide might be useful for treating insulin allergy and anti-insulin antibodies in patients with type 2 diabetes.

Background

Insulin allergy is an important adverse effect of insulin treatment in patients with diabetes. Ghazavi and Johnston recently reported that the prevalence of allergic reactions to insulin products is approximately 2 % at present [1]. Although the frequency of insulin allergy is low, the symptoms vary, ranging from local injection site reactions to complete anaphylactic reactions [2, 3]. Given that anaphylactic reactions are occasionally life-threatening, clinicians must act quickly and appropriately when allergy is suspected.
Glucagon-like peptide-1 (GLP-1) analogs have recently been introduced worldwide as a therapeutic option for the treatment of type 2 diabetes. Liraglutide is one such analog that improves blood glucose control by directly affecting both insulin and glucagon secretion in the pancreas [4]. However, there are only a few reports of liraglutide being used for the treatment of insulin allergy, and its effectiveness remains to be completely elucidated in this context [5, 6]. Furthermore, anti-insulin immunoglobulin G (IgG) antibodies [5, 7, 8] and anti-insulin receptor antibodies [5, 9] are occasionally detected in patients with diabetes who have brittle glycemic control or severe insulin resistance. The effectiveness of liraglutide remains unclear in these cases.
We report a case in which switching to liraglutide therapy ameliorated both the symptoms of insulin allergy with hypereosinophilia and the characteristics of insulin antibodies in patients with type 2 diabetes mellitus.

Case presentation

History leading to admission

Our patient is a 70-year-old Japanese man with diabetes. He was admitted to our hospital 4.5 years ago for further investigation and treatment of recent-onset insulin allergy. He had a 30-year history of type 2 diabetes mellitus and an approximately 6-year history of insulin injection administration, with an average glycated hemoglobin (HbA1c) level of 7.0 %. He reported a past history of myocardial infarction, hypertension, and dyslipidemia and had undergone coronary artery bypass grafting at 68 years. During that surgery, intravenous protamine sulfate was administrated, which induced anaphylaxis.
At that time, 4.5 years prior to the current presentation, he was receiving 100 mg/day aspirin, 100 mg/day clopidogrel, 100 mg/day imidapril, 20 mg/day isosorbide mononitrate, 5 mg/day nicorandil, and 10 mg/day pravastatin, and these had been stable for more than 3 years. In addition, he was being treated with 20 U/day insulin lispro and 8 U/day insulin glargine, which had also been unchanged for approximately 3 years. Finally, he had been receiving 0.9 mg/day voglibose to supplement his insulin therapy for approximately 5 years.
Approximately 5 months before his current presentation, he reported that he had started to develop wheals with redness and itching at the injection site, which occurred immediately after injecting insulin. Of note, these symptoms only occurred following the use of insulin lispro and not after insulin glargine. Over the subsequent months, part of the surface of the wheals had hardened and further investigation was performed. Two months before his current admission, blood samples were taken that revealed high serum levels of human insulin-specific immunoglobulin E (IgE; 4.21 U/mL; normal range <0.35 U/mL), hypereosinophilia (total white blood cell count, 6000/μL; total eosinophil granulocyte count, 780; percentage, 13 %), and a high level of total IgE (403 IU/mL; normal range <173 IU/mL). A pathology sample was taken 2 months before his admission, which revealed eosinophilic infiltration in the hardened part of the injection site (Fig. 1). Therefore, just before admission, he was diagnosed with insulin allergy and was switched from insulin lispro plus glargine to insulin aspart plus glargine.

Admission for further investigation

He was admitted to our hospital for treatment of his poor glycemic control and to evaluate his residual ability of insulin secretion. On admission, his physical examination was largely unremarkable (height, 157.1 cm; body weight, 53.0 kg; body mass index, 21.5 kg/m2; body temperature, 36.5 °C; blood pressure, 104/62 mmHg; and pulse, 75 beats/minute, regular), although there was induration with slight redness of his abdomen. His laboratory data at that time are shown in Table 1. Of note, his fasting plasma glucose level was 346 mg/dL, and his HbA1c level was 12.3 %. In addition, we detected high serum insulin, anti-insulin IgG antibody, and anti-insulin receptor antibody levels. Although there were no further symptoms of local allergy (wheals, redness, and itching) after injecting with insulin aspart, his postprandial hyperglycemia continued at approximately 350 mg/dL. Therefore, he was switched to insulin glulisine (24 U/day) plus glargine (22 U/day) after admission. On day 17 of admission, his 24-hour blood glucose profile was 88, 241, 241, 295, 297, and 292 mg/dL at 7:30 a.m., 10:00 a.m., 11:30 a.m., 2:00 p.m., 5:30 p.m., and 8:00 p.m., respectively, with an energy intake of 1600 kcal. On days 18 and 19, his urinary excretion of C-peptide was 42.8 to 51.5 μg/day (normal range 40 to 100 μg/day). On day 19, a glucagon stimulation test was performed, and his serum C-peptide response ranged from 3.2 to 3.6 ng/mL (Table 2). On day 22, although his high glucose levels persisted, he was discharged because we had confirmed his ability to secrete insulin. Although his hypereosinophilia was not resolved before his discharge, he had no further allergic symptoms (wheals, redness, and itchiness) at the injection site for glulisine, and the area of induration had almost disappeared.
Table 1
Laboratory data on admission
Parameter
Result (normal range)
Unit
Parameter
Result (normal range)
Unit
WBC
5400 (2800–8800)
/μL
γGTP
32 (10–47)
IU/L
Neutrophil
60 (32–79)
%
Ch-E
378 (214–466)
IU/L
Eosinophil
15 (0–6)
%
T-Bil
0.9 (0.2–1.2)
mg/dL
Lymphocyte
16 (18–59)
%
Na
138 (138–146)
mEq/L
Monocyte
7(0–8)
%
K
4.9 (3.6–4.9)
mEq/L
Basophil
2(0–2)
%
Cl
99 (99–109)
mEq/L
RBC
406×104 (366–478)
/μL
BUN
19 (8–22)
mg/dL
Hb
13.0 (11.6–14)
g/dL
Cre
1.0 (0.4–0.7)
mg/dL
Hct
38.0 (34.1–41.7)
%
UA
4.7 (2.3–7)
mg/dL
Plt
15.2×104 (14.7–34.1)
/μL
CK
209 (62–287)
IU/L
   
AMY
46 (42–132)
IU/L
TP
7.2 (6.7–8.3)
g/dL
CRP
0.62 (0–0.3)
mg/dL
Alb
3.6 (3.9–4.9)
g/dL
TC
149 (150–219)
mg/dL
AST
33 (13–33)
IU/L
TG
70 (30–150)
mg/dL
ALT
28 (6–27)
IU/L
HDL-C
50 (49–74)
mg/dL
FPG
346 (70–109)
mg/dL
ANA
Negative (<40×)
 
F-INS
9774 (5–10)
μIU/mL
CH50
<12 (25-48)
CH50/mL
F-CPR
4.9 (0.6–2.1)
ng/mL
IgG
1697 (870–1700)
mg/dL
HbA1c
12.3 (4.7–6.2)
%
Anti-SS-A antibody
Negative
 
Glycoalbumin
48.3 (12.4–16.3)
%
Anti-SS-B antibody
Negative
 
GAD antibody
0.3 (0–5.0)
U/mL
Anti-ds-DNA antibody
Negative
IU/mL
Human IgE
5.57 (0–0.34)
U/mL
RF
<3 (<15)
IU/mL
IgG-anti-insulin antibodies
14.5 (<0.3)
%
   
Anti-insulin receptor antibodies
Positive
 
Urine test
 
ACTH
11.6 (7.2–63.3)
pg/mL
U-Glucose
(4+)
 
Cortisol
17.9 (6.2–19.4)
μg/dL
U-Protein
Negative
 
TSH
1.747 (0.5–5.0)
μIU/mL
U-Blood
Negative
 
FT4
2.11 (0.9–1.7)
ng/dL
U-Ketone
Negative
 
ACTH adrenocorticotropic hormone, Alb albumin, ALT alanine aminotransferase, AMY amylase, ANA anti-nuclear antibody, Anti-ds-DNA anti-double-stranded DNA, anti-SS-A anti-Sjögren’s syndrome A, anti-SS-B anti-Sjögren’s syndrome B, AST aspartate aminotransferase, BUN blood urea nitrogen, Ch-E cholinesterase, CK creatine, Cl chloride, Cre creatinine, CRP C-reactive protein, F-CPR fasting C-peptide, F-INS fasting insulin, FPG fasting plasma glucose, FT4 free thyroxine, GAD glutamic acid decarboxylase, γ-GTP γ-glutamyl transpeptidase, Hb hemoglobin, HbA1c glycated hemoglobin, Hct hematocrit, HDL-C high density lipoprotein cholesterol, IgE immunoglobulin E, IgG immunoglobulin G, K potassium, Na sodium, Plt platelets, RBC red blood cells, RF rheumatoid factor, T-Bil total bilirubin, TC total cholesterol, TG triglyceride, TP total protein, TSH thyroid-stimulating hormone, UA uric acid, WBC white blood cells
Table 2
An evaluation of the patient’s insulin secretion ability
(a) Glucagon stimulation test
Time (minutes)
0
6
PG (pg/mL)
112
122
CP (ng/mL)
3.2
3.6
(b) Urinary C-peptide excretion
Day 18 (after admission)
Day 19
Normal range
42.8 μg/day
51.5 μg/day
(40–100)
CP C-peptide, PG plasma glucose

Progress since discharge and the introduction of liraglutide

Figure 2 summarizes his clinical course before and after the introduction of liraglutide. After discharge, although glulisine and glargine were continued, his glycemic control worsened, with fasting and postprandial hyperglycemia levels of approximately 200 and 300 mg/dL, respectively, and high serum insulin levels persisted (Fig. 2). Therefore, 2 months after his admission, we added 0.3 mg liraglutide, discontinued the insulin glulisine, and added 2 mg/day glimepiride and 500 mg/day metformin to decrease his total insulin requirements. However, he also started to develop intermittent induration at the site of insulin glargine injection, and although there was no evidence of wheals or redness, his hypereosinophilia persisted. Based on these findings, we reduced the dose of glargine (32→22→26→10 U/day) and increased the dose of liraglutide (0.3→0.6→0.9 mg/day; Fig. 2). This was followed by improvements in his HbA1c, serum insulin, and eosinophil levels; therefore, we decided to completely discontinue the insulin glargine after 3 months of the liraglutide treatment. On his new regimen of 0.9 mg/day liraglutide in combination with oral antidiabetic agents, his HbA1c level was maintained at approximately 7.0 %. The induration had almost completely disappeared 1 month after the insulin injections were discontinued. In addition, his body weight decreased by 1.7 kg after 2 months of liraglutide treatment. Table 3 indicates his diabetes-related medical history.
Table 3
Timeline
Time
Diabetes-related medical history
1980s
Onset of type 2 diabetes mellitus
2009
Coronary artery bypass grafting was conducted, anaphylaxis induced by intravenous protamine sulfate administration
May 2011
Onset of allergy
July 2011
A skin biopsy and blood tests confirmed an allergy
24 October 2011
Admission to our hospital
14 December 2011
Liraglutide was additionally started
21 March 2012
Insulin discontinued
April 2012
The symptoms of insulin allergy almost disappeared

Supplemental investigation by Scatchard analysis

We also elucidated the changes in the characteristics of anti-insulin IgG antibodies before and after treatment with liraglutide. Scatchard analysis of the anti-insulin IgG antibodies in our case indicated that there was a high binding capacity and a low affinity constant for the high affinity sites before liraglutide therapy (Fig. 3). After 1 year of treatment with liraglutide, the Scatchard plot indicated that the binding capacity decreased and the affinity constant for high affinity sites increased (Fig. 3). Of interest, the anti-insulin receptor antibodies had completely disappeared within 1 year after the injection of liraglutide.

Discussion

There are two important aspects to this case. First, we provide a rare description of insulin allergy associated with hypereosinophilia, anti-insulin IgG antibodies, and anti-insulin receptor antibodies in a patient with type 2 diabetes. Second, the marked efficacy of liraglutide suggests that it is useful in all patients with type 2 diabetes.
In our case, we believed that our patient’s insulin allergy was predominantly a type 1 immediate reaction based on the fact that insulin lispro induced wheals, itching, and redness immediately after injection. Insulin allergy is typically classified into the following: type 1, which is local and immediate; type 3, which is related to autoimmune disease; and type 4, which is a delayed-type reaction. Symptoms typically manifest within 15 minutes after insulin injection in type 1 reactions, approximately 6 hours after type 3 reactions, and 8 to 24 hours after type 4 reactions [2]. In our case, we confirmed that insulin lispro induced immediate symptoms but could not detect whether insulin aspart, glulisine, or glargine induced those reactions.
We did not perform either a skin prick test or an intradermal reaction test because of his past history of anaphylaxis. Out of concern for his safety, we substituted this with a non-invasive drug-induced lymphocyte stimulation test, which is normally considered best suited for delayed (type 4) reactions. Although this test was only positive for insulin glulisine, false-negatives have been detected in some cases, and we considered that insulin glargine was also associated with delayed-type allergy. This was because insulin glargine induced occasional induration and because its discontinuation resulted in improvement of both his induration and hypereosinophilia.
Based on the combination of these results, we concluded that our patient probably had a delayed-type allergic reaction that was complicated with a predominant immediate-type allergic reaction. Unfortunately, we did not obtain the list of additives in either the lispro or glargine, which could have been important given his history of protamine anaphylaxis. Further investigation of the cause of the allergic reactions could not be performed (for example, to other insulin preparations, including human neutral protamine Hagedorn, or the additives in the insulin types).
Previous reports of type 1 and type 4 allergic reactions to insulin indicate that hypereosinophilia does not necessarily occur. Therefore, the increase of eosinophilia in both local pathological findings and systemic peripheral blood is characteristic of this case. In general, although numerous eosinophils tend to be detected in local inflammation, such as allergy and parasitic infection, the complete role of eosinophils has not been elucidated [10]. For example, although hypereosinophilia has been observed in invasive parasitic infection, it has recently been reported to be partially defensive in vivo during such an infection [10]. In clinical cases of hypereosinophilia, clinicians must quickly and accurately diagnose the cause [11]. Potential causes in the differential diagnosis of this case included adrenal crisis, parasitic infection, and blood disease, but there was no evidence in support of these diagnoses. In addition, because hypereosinophilia simultaneously occurred with the observed clinical course of insulin allergy, we considered insulin allergy the more likely cause. This was consistent with the report by Nagai et al., who reported a case of immediate-type allergy against human insulin associated with marked eosinophilia in a patient with type 2 diabetes [12]. In that case, there was also the possibility of hypereosinophilia-induced renal dysfunction. Although there was no evidence of organ damage in this case, clinicians should remain vigilant for hypereosinophilic syndrome [11, 13] and be prepared to initiate appropriate therapy. Currently, treatment options for insulin allergy include switching to another insulin device [2], steroid therapy [2], continuous subcutaneous insulin infusion therapy [14], hyposensitization therapy [15], pancreas transplantation [16], and anti-IgE therapy [17]. However, reports on the treatment of insulin allergy with hypereosinophilia are limited, and new options are needed. Therefore, we consider that liraglutide might be a breakthrough agent in the treatment of insulin allergy with hypereosinophilia in patients with type 2 diabetes. Indeed, a Medline search indicated that at the time of writing, we are the first to report the beneficial effects of liraglutide in this setting.
Treatment with liraglutide requires the residual ability to secrete insulin, but we do not know the appropriate range of insulin secretion that is necessary. Previously, Kozawa et al. reported that the cut-off value for predicting the efficacy of liraglutide was 1.1 for the C-peptide index, which was defined as (fasting C-peptide/glucose)×100, and 1.5 ng/mL for fasting C-peptide [18]. This index was also shown to be a predictive marker for the beta-cell area of the human pancreas [18, 19]. Using a glucagon stimulation test, Usui et al. reported that a ΔC-peptide value of 1.34 ng/mL was a useful cut-off point for switching from insulin to liraglutide without developing hyperglycemia [20]. In this case, although the fasting C-peptide level was high, the ΔC-peptide in the glucagon stimulation test had a low value. Therefore, liraglutide alone could not inhibit postprandial hyperglycemia, and the antidiabetic drugs glimepiride, metformin, and voglibose were combined to achieve complete control. Moreover, the additional benefits of liraglutide include the prevention of body weight gain due to its appetite-suppressing and gastrointestinal peristaltic movement-suppressing effects. Liraglutide and other GLP-1 analogs have been reported to decrease body weight [21, 22]. In our case, our patient’s body weight decreased by only 1.7 kg, but we could not administer liraglutide at a dose of more than 0.9 mg/day. Worldwide, liraglutide is administered at a maximum dose of 1.8 mg/day; however, Japan has approved that liraglutide is administered at a maximum dose of only 0.9 mg/day.
In our case, it is possible that both the insulin allergy and the presence of anti-insulin IgG antibodies themselves aggravated our patient’s glycemic control. Therefore, we tested his human leukocyte antigen-antigen D related (HLA-DR) type based on the report by Uchigata et al. that insulin autoimmune syndromes are strongly associated with HLA-DR4 [23]. We showed that his HLA-DR types were DR-9 and DR-15 and not DR-4; thus, we did not consider HLA-DR to be a potential causative factor for producing anti-insulin IgG antibodies. Instead, we concluded that the anti-insulin IgG antibodies resulted from the exogenous insulin injection; thus, we used liraglutide without insulin to decrease the amount of anti-insulin IgG antibodies and to avoid further production.
Moreover, Scatchard analysis of the anti-insulin IgG antibodies in our patient indicated that there was a high binding capacity and a low affinity constant for high affinity sites. At high affinity sites, Eguchi reported two important patterns of Scatchard analysis of anti-insulin IgG antibodies: (1) high (11.5 to 53.2) binding capacity (10−8 M) and low (0.04 to 0.21) affinity constant (108 M−1) in insulin autoimmune syndrome; and (2) low (0.12 to 1.1) binding capacity (10−8 M) and high (1.45 to 7.11) affinity constant (108 M−1) in patients with diabetes requiring insulin therapy [24]. Therefore, the binding capacity and low affinity constant for high affinity sites are clinically important. Our patient had extremely high binding capacity and a low affinity constant compared with previous reports. In particular, his extremely high binding capacity was consistent with his high serum insulin levels.
After insulin therapy was discontinued and liraglutide was started, the characteristics of his anti-insulin IgG antibodies changed. Specifically, there was a notable decrease in the binding capacity and an increase in the affinity constant for high affinity sites (Fig. 3c). Hara et al. have reported that antibody-mediated insulin resistance was treated by ceasing insulin administration [25], whereas Tamura et al. reported that liraglutide ameliorated the anti-insulin IgG antibodies in a woman with type 2 diabetes receiving hemodialysis [26]. In our case, it remains unclear how liraglutide might have affected our patient’s anti-insulin IgG antibodies; however, a recent report has suggested that GLP-1 receptor agonists interact with the immune system. In fact, Hadjiyanni et al. reported that GLP-1 receptor signaling selectively regulated murine lymphocyte proliferation and maintained peripheral regulatory T cells in vivo [27]. In humans, the effects of GLP-1 receptor agonists have been investigated in patients with psoriasis [28], but the detailed mechanism of action is unclear. Further reports are needed to improve our understanding of these agents.
Anti-insulin IgG antibodies have often been reported to induce hypoglycemia [8, 21, 23, 24]. Unfortunately, we could not measure serum free insulin levels directly and do not know whether the anti-insulin receptor antibodies really affected glucose metabolism. Although Kim et al. reported that anti-insulin receptor antibodies often coexist with anti-insulin IgG antibodies in Korean patients with insulin autoimmune syndrome [29], the clinical significance of this finding has been not determined. Acquired anti-insulin receptor antibodies induce severe insulin resistance, called “type B insulin resistance,” which was first reported in 1976 [30]. However, we found no other symptoms or complications of type B insulin resistance, such as acanthosis nigricans or autoimmune disease (Table 1). In addition, the total insulin dose was smaller than that reported in previous studies on type B insulin resistance [9, 30]. Therefore, we considered the possibility that the presence of anti-insulin receptor antibodies is a false positive in this case. It is also possible that the method of measurement led to a false positive result for anti-insulin receptor antibodies because we used the insulin binding inhibition method [31]. Perhaps the high insulin levels and high anti-insulin IgG antibodies levels had some unknown influence on the measured values.

Conclusions

In conclusion, our case suggests that liraglutide is a useful treatment for insulin allergy associated with hypereosinophilia and anti-insulin IgG antibodies in patients with type 2 diabetes. However, similar case reports are limited, and further reports are clearly needed.

Abbreviations

GLP-1, glucagon-like peptide-1; HbA1c, glycated hemoglobin; HLA-DR, human leukocyte antigen-antigen D related; IgE, immunoglobulin E; IgG, immunoglobulin G

Acknowledgements

We gratefully acknowledge our patient who allowed us to publish his case. This work was supported in part by a Grant-in-Aid Scientific Research from the Ministry of Education, Culture, Sports, Science, and Technology (HS). The contents are solely the responsibility of the authors and do not represent the official views of the funding institutions.

Authors’ contributions

HH and HS were responsible for the original manuscript design and draft, and the acquisition of data. HH, HS, and TW were involved in drafting the manuscript. HS was involved in revision of the manuscript for important intellectual content. HH, EO, NK, TK, NM, and KH were the physicians involved in patient management. All authors read and approved the final manuscript.

Competing interests

The authors declare that they have no competing interests.
Written informed consent was obtained from the patient for publication of this case report and any accompanying images. A copy of the written consent is available for review by the Editor-in-Chief of this journal.
Open AccessThis article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://​creativecommons.​org/​licenses/​by/​4.​0/​), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver (http://​creativecommons.​org/​publicdomain/​zero/​1.​0/​) applies to the data made available in this article, unless otherwise stated.

Unsere Produktempfehlungen

e.Med Interdisziplinär

Kombi-Abonnement

Für Ihren Erfolg in Klinik und Praxis - Die beste Hilfe in Ihrem Arbeitsalltag

Mit e.Med Interdisziplinär erhalten Sie Zugang zu allen CME-Fortbildungen und Fachzeitschriften auf SpringerMedizin.de.

© Springer Medizin

Bis 11. April 2024 bestellen und im ersten Jahr 50 % sparen!

e.Med Allgemeinmedizin

Kombi-Abonnement

Mit e.Med Allgemeinmedizin erhalten Sie Zugang zu allen CME-Fortbildungen und Premium-Inhalten der allgemeinmedizinischen Zeitschriften, inklusive einer gedruckten Allgemeinmedizin-Zeitschrift Ihrer Wahl.

© Springer Medizin

Bis 11. April 2024 bestellen und im ersten Jahr 50 % sparen!

Literatur
2.
Zurück zum Zitat Heinzerling L, Raile K, Rochlitz H, Zuberbier T, Worm M. Insulin allergy: clinical manifestations and management strategies. Allergy. 2008;63(2):148–55.CrossRefPubMed Heinzerling L, Raile K, Rochlitz H, Zuberbier T, Worm M. Insulin allergy: clinical manifestations and management strategies. Allergy. 2008;63(2):148–55.CrossRefPubMed
3.
Zurück zum Zitat Blanco C, Castillo R, Quiralte J, Delgado J, García I, de Pablos P, et al. Anaphylaxis to subcutaneous neutral protamine Hagedorn insulin with simultaneous sensitization to protamine and insulin. Allergy. 1996;51(6):421–4.PubMed Blanco C, Castillo R, Quiralte J, Delgado J, García I, de Pablos P, et al. Anaphylaxis to subcutaneous neutral protamine Hagedorn insulin with simultaneous sensitization to protamine and insulin. Allergy. 1996;51(6):421–4.PubMed
4.
Zurück zum Zitat Seino Y, Yabe D. Glucose-dependent insulinotropic polypeptide and glucagon-like peptide-1: Incretin actions beyond the pancreas. J Diabetes Investig. 2013;4(2):108–30.CrossRefPubMedPubMedCentral Seino Y, Yabe D. Glucose-dependent insulinotropic polypeptide and glucagon-like peptide-1: Incretin actions beyond the pancreas. J Diabetes Investig. 2013;4(2):108–30.CrossRefPubMedPubMedCentral
5.
Zurück zum Zitat Kawanami D, Ito T, Watanabe Y, Kinoshita J, Sakamoto M, Isaka T, et al. Successful control of a case of severe insulin allergy with liraglutide. J Diabetes Investig. 2013;4(1):94–6.CrossRefPubMed Kawanami D, Ito T, Watanabe Y, Kinoshita J, Sakamoto M, Isaka T, et al. Successful control of a case of severe insulin allergy with liraglutide. J Diabetes Investig. 2013;4(1):94–6.CrossRefPubMed
6.
Zurück zum Zitat Fujishiro M, IzumidaY, Takemiya S, Kuwano Y, Takamoto I, Suzuki R, Yamauchi T, Ueki K, Kadowaki T. A case of insulin allergy successfully managed using multihexamer-forming insulin degludec combined with liraglutide. Diabet Med. 2015 Oct 20. doi:10.1111/dme.12998. Fujishiro M, IzumidaY, Takemiya S, Kuwano Y, Takamoto I, Suzuki R, Yamauchi T, Ueki K, Kadowaki T. A case of insulin allergy successfully managed using multihexamer-forming insulin degludec combined with liraglutide. Diabet Med. 2015 Oct 20. doi:10.​1111/​dme.​12998.
7.
Zurück zum Zitat Berson SA, Yalow RS, Bauman A, Rothschild MA, Newerly K. Insulin-I131 metabolism in human subjects: demonstration of insulin binding globulin in the circulation of insulin treated subjects. J Clin Invest. 1956;35(2):170–90.CrossRefPubMedPubMedCentral Berson SA, Yalow RS, Bauman A, Rothschild MA, Newerly K. Insulin-I131 metabolism in human subjects: demonstration of insulin binding globulin in the circulation of insulin treated subjects. J Clin Invest. 1956;35(2):170–90.CrossRefPubMedPubMedCentral
8.
Zurück zum Zitat Iizuka K, Tomita R, Horikawa Y, Takeda J. A case of glycemic instability and insulin allergy due to anti-insulin antibodies in a patient with type 2 diabetes. Diabetol Int. 2012;3(4):233–8.CrossRef Iizuka K, Tomita R, Horikawa Y, Takeda J. A case of glycemic instability and insulin allergy due to anti-insulin antibodies in a patient with type 2 diabetes. Diabetol Int. 2012;3(4):233–8.CrossRef
9.
Zurück zum Zitat Yamada H, Asano T, Kusaka I, Kakei M, Ishikawa S. Type B insulin resistance syndrome with fasting hypoglycemia and postprandial hyperglycemia. Diabetol Int. 2015;6(2):144–48.CrossRef Yamada H, Asano T, Kusaka I, Kakei M, Ishikawa S. Type B insulin resistance syndrome with fasting hypoglycemia and postprandial hyperglycemia. Diabetol Int. 2015;6(2):144–48.CrossRef
12.
Zurück zum Zitat Nagai Y, Mori T, Abe T, Nomura G. Immediate-type allergy against human insulin associated with marked eosinophilia in type 2 diabetic patient. Endocr J Jun. 2001;48(3):311–6.CrossRef Nagai Y, Mori T, Abe T, Nomura G. Immediate-type allergy against human insulin associated with marked eosinophilia in type 2 diabetic patient. Endocr J Jun. 2001;48(3):311–6.CrossRef
13.
Zurück zum Zitat Uriuhara A, Morita S, Kuroda S, Fumoto M, Araki S, Aoyama N, et al. Severe insulin-resistant diabetes mellitus associated with hypereosinophilic syndrome. Intern Med. 1994;33(10):632–6.CrossRefPubMed Uriuhara A, Morita S, Kuroda S, Fumoto M, Araki S, Aoyama N, et al. Severe insulin-resistant diabetes mellitus associated with hypereosinophilic syndrome. Intern Med. 1994;33(10):632–6.CrossRefPubMed
14.
Zurück zum Zitat Nagai T, Nagai Y, Tomizawa T, Mori M. Immediate-type human insulin allergy successfully treated by continuous subcutaneous insulin infusion. Intern Med. 1997;36(8):575–8.CrossRefPubMed Nagai T, Nagai Y, Tomizawa T, Mori M. Immediate-type human insulin allergy successfully treated by continuous subcutaneous insulin infusion. Intern Med. 1997;36(8):575–8.CrossRefPubMed
15.
Zurück zum Zitat Matheu V, Perez E, Hernández M, Díaz E, Darias R, González A, et al. Insulin allergy and resistance successfully treated by desensitisation with aspart insulin. Clin Mol Allergy. 2005;23(3):16.CrossRef Matheu V, Perez E, Hernández M, Díaz E, Darias R, González A, et al. Insulin allergy and resistance successfully treated by desensitisation with aspart insulin. Clin Mol Allergy. 2005;23(3):16.CrossRef
16.
Zurück zum Zitat Malaise J, Leonet J, Goffin E, Lefebvre C, Tennstedt D, Vandeleene B, et al. Pancreas transplantation for treatment of generalized allergy to human insulin in type 1 diabetes. Transplant Proc. 2005;37(6):2839.CrossRefPubMed Malaise J, Leonet J, Goffin E, Lefebvre C, Tennstedt D, Vandeleene B, et al. Pancreas transplantation for treatment of generalized allergy to human insulin in type 1 diabetes. Transplant Proc. 2005;37(6):2839.CrossRefPubMed
17.
Zurück zum Zitat Cavelti-Weder C, Muggli B, Keller C, Babians-Brunner A, Biason-Lauber A, Donath MY, et al. Successful use of omalizumab in an inadequately controlled type 2 diabetic patient with severe insulin allergy. Diabetes Care. 2012;35(6):e41.CrossRefPubMedPubMedCentral Cavelti-Weder C, Muggli B, Keller C, Babians-Brunner A, Biason-Lauber A, Donath MY, et al. Successful use of omalizumab in an inadequately controlled type 2 diabetic patient with severe insulin allergy. Diabetes Care. 2012;35(6):e41.CrossRefPubMedPubMedCentral
18.
Zurück zum Zitat Kozawa J, Inoue K, Iwamoto R, Kurashiki Y, Okauchi Y, Kashine S, et al. Liraglutide is effective in type 2 diabetic patients with sustained endogenous insulin-secreting capacity. J Diabetes Investig. 2012;3(3):294–7.CrossRefPubMed Kozawa J, Inoue K, Iwamoto R, Kurashiki Y, Okauchi Y, Kashine S, et al. Liraglutide is effective in type 2 diabetic patients with sustained endogenous insulin-secreting capacity. J Diabetes Investig. 2012;3(3):294–7.CrossRefPubMed
19.
Zurück zum Zitat Meier JJ, Menge BA, Breuer TG, Müller CA, Tannapfel A, Uhl W, et al. Functional assessment of pancreatic β-cell area in humans. Diabetes. 2009;58(7):1595–603.CrossRefPubMedPubMedCentral Meier JJ, Menge BA, Breuer TG, Müller CA, Tannapfel A, Uhl W, et al. Functional assessment of pancreatic β-cell area in humans. Diabetes. 2009;58(7):1595–603.CrossRefPubMedPubMedCentral
20.
Zurück zum Zitat Usui R, Yabe D, Kuwata H, Fujiwara S, Watanabe K, Hyo T, et al. Retrospective analysis of safety and efficacy of insulin-to-liraglutide switch in Japanese type 2 diabetes: A caution against inappropriate use in patients with reduced β-cell function. J Diabetes Investig. 2013;4(6):585–94.CrossRefPubMedPubMedCentral Usui R, Yabe D, Kuwata H, Fujiwara S, Watanabe K, Hyo T, et al. Retrospective analysis of safety and efficacy of insulin-to-liraglutide switch in Japanese type 2 diabetes: A caution against inappropriate use in patients with reduced β-cell function. J Diabetes Investig. 2013;4(6):585–94.CrossRefPubMedPubMedCentral
21.
Zurück zum Zitat Jendle J, Nauck MA, Matthews DR, Frid A, Hermansen K, Düring M, et al. LEAD-2 and LEAD-3 Study Groups: Weight loss with liraglutide, a once-daily human glucagon-like peptide-1 analogue for type 2 diabetes treatment as monotherapy or added to metformin, is primarily as a result of a reduction in fat tissue. Diabetes Obes Metab. 2009;11(12):1163–72.CrossRefPubMed Jendle J, Nauck MA, Matthews DR, Frid A, Hermansen K, Düring M, et al. LEAD-2 and LEAD-3 Study Groups: Weight loss with liraglutide, a once-daily human glucagon-like peptide-1 analogue for type 2 diabetes treatment as monotherapy or added to metformin, is primarily as a result of a reduction in fat tissue. Diabetes Obes Metab. 2009;11(12):1163–72.CrossRefPubMed
22.
Zurück zum Zitat Chen JH, Tang WH, Lee CH. Effective weight loss after treatment with a glucagon-like peptide-1 receptor agonist in a morbidly obese and diabetic patient before bariatric surgery: a case report. J Med Case Rep. 2014;8:304.CrossRefPubMedPubMedCentral Chen JH, Tang WH, Lee CH. Effective weight loss after treatment with a glucagon-like peptide-1 receptor agonist in a morbidly obese and diabetic patient before bariatric surgery: a case report. J Med Case Rep. 2014;8:304.CrossRefPubMedPubMedCentral
23.
Zurück zum Zitat Uchigata Y, Kuwata S, Tokunaga K, Eguchi Y, Takayama-Hasumi S, Miyamoto M, et al. Strong association of insulin autoimmune syndrome with HLA-DR4. Lancet. 1992;339(8790):393–4.CrossRefPubMed Uchigata Y, Kuwata S, Tokunaga K, Eguchi Y, Takayama-Hasumi S, Miyamoto M, et al. Strong association of insulin autoimmune syndrome with HLA-DR4. Lancet. 1992;339(8790):393–4.CrossRefPubMed
24.
Zurück zum Zitat Eguchi Y. Scatchard analysis of insulin autoantibodies in the insulin autoimmune syndrome (Japanese). J Tokyo Wom Med Univ. 1989;59:1296–305. Eguchi Y. Scatchard analysis of insulin autoantibodies in the insulin autoimmune syndrome (Japanese). J Tokyo Wom Med Univ. 1989;59:1296–305.
25.
Zurück zum Zitat Hara K, Tobe K, Uchigata Y, Nakazono M, Yasuda K, Terauchi Y, et al. Antibody-mediated insulin resistance treated by cessation of insulin administration. Intern Med. 2000;39(2):143–5.CrossRefPubMed Hara K, Tobe K, Uchigata Y, Nakazono M, Yasuda K, Terauchi Y, et al. Antibody-mediated insulin resistance treated by cessation of insulin administration. Intern Med. 2000;39(2):143–5.CrossRefPubMed
26.
Zurück zum Zitat Tamura Y, Kimbara Y, Funatsuki S, Mabuchi S, Kodera R, Yoshimoto A, et al. A case of insulin antibody-induced glucose instability in an elderly woman with type 2 diabetes on hemodialysis, successfully ameliorated with liraglutide. Diabetol Int. 2013;4(1):71–5.CrossRef Tamura Y, Kimbara Y, Funatsuki S, Mabuchi S, Kodera R, Yoshimoto A, et al. A case of insulin antibody-induced glucose instability in an elderly woman with type 2 diabetes on hemodialysis, successfully ameliorated with liraglutide. Diabetol Int. 2013;4(1):71–5.CrossRef
27.
Zurück zum Zitat Hadjiyanni KA, Siminovitch JS, Drucker DJ. Glucagon-like peptide-1 receptor signaling selectively regulates murine lymphocyte proliferation and maintenance of peripheral regulatory T cells. Diabetologia. 2010;53(4):730–40.CrossRefPubMed Hadjiyanni KA, Siminovitch JS, Drucker DJ. Glucagon-like peptide-1 receptor signaling selectively regulates murine lymphocyte proliferation and maintenance of peripheral regulatory T cells. Diabetologia. 2010;53(4):730–40.CrossRefPubMed
28.
Zurück zum Zitat Al-Badri MR, Azar ST. Effect of glucagon-like peptide-1 receptor agonists in patients with psoriasis. Ther Adv Endocrinol Metab. 2014;5(2):34–8.CrossRefPubMedPubMedCentral Al-Badri MR, Azar ST. Effect of glucagon-like peptide-1 receptor agonists in patients with psoriasis. Ther Adv Endocrinol Metab. 2014;5(2):34–8.CrossRefPubMedPubMedCentral
29.
Zurück zum Zitat Kim SW, Won HK, Seok H, Lee BW, Jung CH, Lee WJ, et al. High prevalence of both anti-insulin and anti-insulin receptor antibodies in Korean patients with insulin autoimmune syndrome. Diabetes Res Clin Pract Nov. 2012;98(2):e12–5.CrossRef Kim SW, Won HK, Seok H, Lee BW, Jung CH, Lee WJ, et al. High prevalence of both anti-insulin and anti-insulin receptor antibodies in Korean patients with insulin autoimmune syndrome. Diabetes Res Clin Pract Nov. 2012;98(2):e12–5.CrossRef
30.
Zurück zum Zitat Kahn CR, Flier JS, Bar RS, Archer JA, Gorden P, Martin MM, et al. The syndromes of insulin resistance and acanthosis nigricans – insulin-receptor disorders in man. N Engl J Med. 1976;294:739–45.CrossRefPubMed Kahn CR, Flier JS, Bar RS, Archer JA, Gorden P, Martin MM, et al. The syndromes of insulin resistance and acanthosis nigricans – insulin-receptor disorders in man. N Engl J Med. 1976;294:739–45.CrossRefPubMed
31.
Zurück zum Zitat Filier JS, Kahn CR, Roth J, Bar RS. Antibodies that impair insulin receptor binding in an unusual diabetic syndrome with severe insulin resistance. Science. 1975;190:63–5.CrossRef Filier JS, Kahn CR, Roth J, Bar RS. Antibodies that impair insulin receptor binding in an unusual diabetic syndrome with severe insulin resistance. Science. 1975;190:63–5.CrossRef
Metadaten
Titel
The effects of liraglutide on both hypereosinophilic insulin allergy and the characteristics of anti-insulin antibodies in type 2 diabetes mellitus: a case report
verfasst von
Hiroyuki Hirai
Emi Ogata
Nobuyuki Kikuchi
Teruyuki Kohno
Noritaka Machii
Koji Hasegawa
Tsuyoshi Watanabe
Hiroaki Satoh
Publikationsdatum
01.12.2016
Verlag
BioMed Central
Erschienen in
Journal of Medical Case Reports / Ausgabe 1/2016
Elektronische ISSN: 1752-1947
DOI
https://doi.org/10.1186/s13256-016-0994-4

Weitere Artikel der Ausgabe 1/2016

Journal of Medical Case Reports 1/2016 Zur Ausgabe