Journal List > J Korean Med Sci > v.38(24) > 1516082958

TOOLS
Huang, Liang, and He: New-Onset Fulminant Type 1 Diabetes Following SARS-CoV-2 Protein Subunit Vaccine: A Case Report and Literature Review
Case Report
Endocrinology, Nutrition & Metabolism

Journal of Korean Medical Science 2023; 38(24): e209.

Published online: 8 June 2023

DOI: https://doi.org/10.3346/jkms.2023.38.e209

New-Onset Fulminant Type 1 Diabetes Following SARS-CoV-2 Protein Subunit Vaccine: A Case Report and Literature Review

Lanhui Huang, Min Liang, Yuling He

Department of Geriatric Endocrinology and Metabolism, The First Affiliated Hospital of Guangxi Medical University, Nanning, China.

Address for Correspondence: Yuling He, MD. Department of Geriatric Endocrinology and Metabolism, The First Affiliated Hospital of Guangxi Medical University, No. 6 Shuangyong Road, Nanning, Guangxi 530021, China. heyulingy@163.com

Address for Correspondence: Min Liang, MD, PhD. Department of Geriatric Endocrinology and Metabolism, The First Affiliated Hospital of Guangxi Medical University, No. 6 Shuangyong Road, Nanning, Guangxi 530021, China. liangm@gxmu.edu.cn

Received 24 February 2023       Accepted 24 April 2023

© 2023 The Korean Academy of Medical Sciences.

The Korean Academy of Medical Sciences

https://creativecommons.org/licenses/by-nc/4.0/
This is an Open Access article distributed under the terms of the Creative Commons Attribution Non-Commercial License (https://creativecommons.org/licenses/by-nc/4.0/) which permits unrestricted non-commercial use, distribution, and reproduction in any medium, provided the original work is properly cited.

Abstract

The ravages of severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2) worldwide have sped up the development of relevant vaccines, which is accompanied by public concerns over possible adverse effects. We report a rare case of a 39-year-old woman who suffered from severe hyperglycemia and ketoacidosis with normal hemoglobin A1c four days after SARS-CoV-2 protein subunit vaccine, which is consistent with the diagnosis of fulminant type 1 diabetes (FT1D). She received insulin therapy and recovered after 24 days from onset of the symptoms. This is the first case of new-onset FT1D after SARS-CoV-2 protein subunit vaccination and one of only six that developed after any form of SARS-CoV-2 vaccination. We hope to raise awareness of this potential adverse consequence and recommend careful monitoring after vaccination in patients even without a medical history of diabetes.

Graphical Abstract

jkms-38-e209-abf001.jpg

Keywords: Fulminant Type 1 Diabetes, SARS-CoV-2 Vaccine, Protein Subunit Vaccine, Adverse Effects

INTRODUCTION

With the outbreak of the coronavirus disease 2019 (COVID-19) across the world, vaccines against severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2) have achieved accelerated clinical development to alleviate the burden of COVID-19 on public health. More than 11 billion SARS-CoV-2 vaccine doses have been administered in the world.1 According to World Health Organization statistics,2 the protein subunit vaccine has become the predominant category (accounting for 32% of all vaccines), followed by the RNA-based vaccine (23%), the non-replicating viral vector (14%), and the inactivated virus (12%).
Considering the unprecedented health burden induced by the COVID-19 pandemic, most vaccines have received emergency use authorization, though they have not been extensively whetted for their possible adverse effects. Therefore, public concerns over the possible adverse effects of these vaccines have emerged. A series of reports about autoimmune/inflammatory diseases induced by SARS-CoV-2 vaccines have attracted more and more attention, such as Graves’ disease,3 autoimmune hepatitis,456 systemic lupus erythematosus,7 and so on. Fulminant type 1 diabetes (FT1D) is a rapidly progressing and severe subtype of type 1 diabetes (T1D) with high mortality and disability rate. Recently, several cases have been reported about new-onset FT1D following SARS-CoV-2 vaccination, but only limited to mRNA vaccine891011 and inactivated vaccine.12 Up to now, no cases have been reported about FT1D followed by SARS-CoV-2 protein subunit vaccination.
Herein, we reported a 39-year-old Chinese woman with new-onset FT1D four days after SARS-CoV-2 protein subunit vaccination. Meanwhile, we conducted a systematic review on the comparison between FT1D and autoimmune T1D followed by SARS-CoV-2 vaccination, so as to gain a better understanding of SARS-CoV-2 vaccine-related FT1D. We highly acknowledge the importance and benefits of mass SARS-CoV-2 vaccination, but we still hope to raise public awareness of its possible adverse effects and attach importance to the pharmacovigilance in guiding treatment.

CASE DESCRIPTION

We reported a 39-year-old woman with a family history of diabetes. She had no medical history of diabetes and the fasting blood glucose from her annual physical examination report seven weeks ago was 104.4 mg/dL. She attended a nearby hospital six days after the fourth dose of SARS-CoV-2 vaccination (Zifivax/ZF2001, Protein subunit vaccine) and complained of general fatigue, thirst, nausea and vomiting for 2 days. At presentation, the laboratory tests reported hyperglycemia (plasma glucose: 508.50 mg/dL) and ketoacidosis with a decreased bicarbonate and an increased anion gap (anion gap = [Sodium – {Bicarbonate + Chloride}] = 18.23 mmol/L, normal range ≤ 16 mmol/L). It was worth noting that the onset hemoglobin A1c (HbA1c) (5.9%) was below the threshold of diabetes. Pancreatic enzymes and thyroid function were normal. The initial diagnoses were diabetes and diabetes ketoacidosis (DKA). Then she received massive fluid infusion and intravenous insulin infusion and her symptoms relieved during a 10-day hospitalization in the nearby hospital.
Ten days later, she was transferred to our hospital due to poor blood glucose control and hoped for a definite diagnosis. On admission, her body mass index (BMI) was 17.97 kg/m2. Oral glucose tolerance test showed exhaustion of endogenous insulin secretion (fasting C-peptide: 0.01 ng/mL, 120-minute C-peptide: 0.13 ng/ml). In terms of islet-specific pancreatic autoantibodies, anti-glutamic acid decarboxylase (GAD) antibody, anti-islet cell antibody (ICA), insulin autoantibody, insulinoma-associated antigen-2 (IA-2) antibody and zinc-transporter 8 (ZnT8) antibody showed all negative. In light of the characteristics at onset and results above, she was diagnosed with FT1D. Further immunological tests showed a significantly reduction in T lymphocyte count. The CD4+ and CD8+ T lymphocyte count were both at a lower level though within the normal range (Table 1). We applied the continuous glucose monitoring after admission, and found high glucose variability (time in range [TIR]: 55.2–65.0%; time below range [TBR]: 10.4–33.3%; time above range [TAR]: 1.7–34.4%; glucose range: 2.2–25.0mmol/L; coefficient of variation [CV]: 45.05–70.02%) and recurrent hypoglycemia, which frequently occurred in the early morning. In order to control the blood glucose, insulin pump (Medtronic, Minneapolis, MN, USA) was used for five days. The dosage and category of insulin used in the insulin pump was 8.1 units of insulin aspart per day (the hourly dosage of insulin: 0.4 units per hour from 8 a.m.to 10 p.m., 0.2 units per hour from 10 p.m. to 3 a.m. of the next day and 0.3 units per hour from 3 a.m. to 8 a.m. of the next day). Five days later, she gained a more stable blood glucose curve (TIR: 76.1%; TBR: 0%; TAR: 23.9%; glucose range: 7.4–14.0 mmol/L; CV: 15.52%), so we switched the insulin pump to subcutaneous injection of insulin four times per day. Two weeks later, the blood glucose curve remained stable (TIR: 88.3%; TBR: 0%; TAR: 11.7%; glucose range: 4.7–15.6mmol/L; CV: 36.34%) and we completed the continuous glucose monitoring.
Table 1

Laboratory findings

jkms-38-e209-i001
Assessment Results Reference range
Peripheral blood
White blood cell, ×109/L 7.64 4.00–10.00
Red blood cell, ×1012/L 4.79 3.50–5.50
Hemoglobin, g/L 132.00 110.00–160.00
Hematocrit, % 40.10 35.00–50.00
Platelet, ×109/L 230.00 100.00–300.00
Biochemistry
ALT, U/L 7.00 0–40.00
AST, U/L 17.95 0–40.00
GGT, U/L 13.30 7.00–45.00
ALP, U/L 53.59 35.00–100.00
Albumin, g/L 32.71 35.00–55.00
BUN, mmol/L 6.57 1.70–8.30
Creatinine, µmol/L 76.14 35.00–80.00
Creatine kinase, U/L 93.16 24.00–170.00
Bicarbonate, mmol/L 12.87 20.00–29.00
Potassium, mmol/L 4.44 3.50–5.30
Sodium, mmol/L 137.10 135.00–147.00
Chloride, mmol/L 106.00 96.00–108.00
Free thyroxine, ng/dL 0.83 0.70–1.48
TSH, µIU/mL 2.64 0.35–4.94
Plasma amylase, U/L 109.54 10.00–120.00
Glucose, mg/dL 508.50 60.48–109.98
HbA1c, % 5.90 4.27–6.07
Plasma ketone, mmol/L 2.90
Serum insulin, pmol/L 13.00–161.00
0 min 0.01
30 min 2.07
60 min 3.42
120 min 5.60
180 min 5.90
Serum C-peptide, ng/mL 0.93–3.73
0 min 0.01
30 min 0.03
60 min 0.07
120 min 0.13
180 min 0.13
Immunological data
GAD antibody Negative
IA-2 antibody Negative
ZnT8 antibody Negative
Insulin autoantibody Negative
Anti-islet cell antibody Negative
T lymphocyte count, /μL 1,078 1,185–1,901
CD4+ T lymphocyte count, /μL 665 561–1,137
CD8+ T lymphocyte count, /μL 367 220–1,030
IL-6, pg/mL 2.77 0–7.00
Ferritin, ng/mL 24.53 4.63–204.00
Urinary test
Urinary glucose 4+
Urinary ketone 3+
Urinary protein Negative
Urinary occult blood Negative
Urinary amylase, U/L 269.51 120.00–1,100.00
ALT = alanine aminotransferase, AST = aspartate transaminase, GGT = glutamyl transpeptidase, ALP = alkaline phosphatase, BUN = blood urea nitrogen, TSH = thyroid-stimulating hormone, HbA1c = hemoglobin A1c, GAD = glutamic acid decarboxylase, IA-2 = insulinoma-associated antigen-2, ZnT8 = zinc-transporter 8, IL-6 = interleukin-6.

Ethics statement

Ethical review of the present case report was waived by the review board of the First Affiliated Hospital of Guangxi Medical University. Informed consent for data collection and publication of the study was obtained from the patient.

DISCUSSION

To the best of our knowledge, this is the first case of FT1D induced by SARS-CoV-2 protein subunit vaccine. Although we could not confirm the objective causal relationship, the temporal relationship indicated a strong link between SARS-CoV-2 protein subunit vaccine and FT1D.
New-onset T1D has been observed following SARS-CoV-2 infection.1314 This phenomenon could be explained by the fact that the spike protein on the surface of SARS-CoV-2 virus can facilitate viral entry into islet cells via angiotensin converting enzyme 2 (ACE2), a membrane-bound receptor, and then initiate the imbalance of T lymphocytes and the activation of cytokine storm, thus inducing islet beta cell apoptosis and DKA.15161718 As an emerging and promising SARS-CoV-2 vaccine, the protein subunit vaccine utilizes recombinant protein technology to produce the extracellular portion of the spike protein of SARS-CoV-2.1920 Due to structural homology, molecular mimicry could be proposed to cause hyperglycemia after SARS-CoV-2 vaccination. It is possible that the spike protein in the SARS-CoV-2 vaccines could cross-react with the ACE2 receptors of islet cells target proteins due to molecular mimicry to cause islet cells damage. The mechanism of molecular mimicry has been also proposed to prove the causal relationship between thyroid dysfunction and SARS-CoV-2 vaccination.21 However, the mechanism of FT1D induced by SARS-CoV-2 vaccination still needs further research.
We further conducted searches in PubMed, Web of Science, and MEDLINE database for existing reported cases of FT1D induced by SARS-CoV-2 vaccination in order to have a better understanding of the clinical characteristics of SARS-CoV-2 vaccine-related FT1D. Five related cases were finally included. As shown in Table 2, patients with FT1D followed by SARS-CoV-2 vaccination were predominantly female (four female vs. two male), young and middle-aged (range from 36 to 59 years old) and thin (BMI range from 17.97 to 20.6 kg/m2). These reported vaccines included four mRNA vaccines and one inactivated vaccine while our present case was the first case with respect to the protein subunit vaccine. The duration from symptoms onset to diagnosis among these cases were all within seven days. The levels of serum pancreatic enzyme were slightly elevated in some cases,81012 corresponding to previous reported cases of FT1D.2223 This phenomenon could be explained by leukomonocyte infiltration in exocrine pancreatic acinar cells rather than insulitis.24 As for islet-specific pancreatic autoantibodies, there were only two cases with positive GAD antibody. We further compared the cases with positive and negative GAD antibodies, and found that positive GAD antibodies were significantly associated with more complete destruction and worse secretion capacity of islet beta cells. Kawasaki et al. have showed that the proportion of GAD antibody accounted for 9% of FT1D patients,23 which shared a similarity with these cases. This indicated that islet-associated autoimmune processes may partake in the pathogenesis of FT1D patients with positive GAD antibodies.22
Table 2

Comparison of characteristics of FT1D after SARS-CoV-2 vaccination

jkms-38-e209-i002
Characteristics Reported cases
Case 1 Case 2 Case 3 Case 4 Case 5 Case 6
Author Sakurai et al.8 Lin et al.9 Tang et al.12 Kobayashi et al.10 Sasaki et al.11 Present case
Sex Female Female Male Male Female Female
Age, yr 36 39 50 59 45 39
Vaccine RNA RNA Inactivated vaccine RNA RNA Protein subunit
Time from vaccination to onset 3 days 14 wk 6 days 15 wk 3 days 4 days
Time from symptom onset to DKA 7 days ≤ 7 days 1 days 6 days 5 days 2 days
BMI, kg/m2 NA 19.2 18.1 NA 20.6 17.97
Plasma glucose levels, mg/dL 501 364 Elevated 1454 469 508
HbA1c, % 7 6.4 Elevated 7.8 7.2 5.9
Serum pancreatic enzyme, U/L Slightly elevated NA Slightly elevated Slightly elevated NA Normal
Fasting C-peptide 0.55 < 0.02 0.01 < 0.03 0.33 0.01
GAD antibody (−) (+) (−) (+) (−) (−)
IA-2 antibody (−) (+) (−) (−) (−) (−)
ZnT8 antibody (−) NA (−) (−) (−) (−)
Insulin autoantibody (−) NA NA NA (−) (−)
TPOAb NA NA NA (−) (−) NA
TgAb NA NA NA (−) (−) NA
Previous diabetes history (−) (−) (−) (−) NA (−)
Family history of diabetes (−) T2D T2D (−) NA T2D
FT1D = fulminant type 1 diabetes, SARS-CoV-2 = severe acute respiratory syndrome coronavirus 2, DKA = diabetes ketoacidosis, BMI = body mass index, HbA1c = hemoglobin A1c, GAD = glutamic acid decarboxylase, IA-2 = insulinoma-associated antigen-2, ZnT8 = zinc-transporter 8, TPOAb = thyroperoxidase antibodies, TgAb = thyroglobulin antibodies, T2D = type 2 diabetes, (−) = negative, NA = not available.
Moreover, we conducted a systematic review on the comparison between FT1D and autoimmune T1D followed by SARS-CoV-2 vaccination. After searching PubMed, Web of Science, and MEDLINE database for existing reported cases of new-onset T1D following SARS-CoV-2 vaccination, six cases with FT1D and eight cases with autoimmune T1D following SARS-CoV-2 vaccination were included. The characteristics of FT1D and autoimmune T1D after SARS-CoV-2 vaccination were summarized in Table 3. Patients with FT1D following vaccination were predominantly younger, female, and thinner. The first symptoms of FT1D were mostly typical symptoms of DKA, and some were accompanied by adverse reactions of vaccines such as fatigue and a slight fever.101112 Patients with FT1D were more likely to have shorter onset time, more serious ketoacidosis, and lower HbA1c. The levels of amylase increased in some FT1D patients.81012 Most cases with FT1D reported negative GAD antibodies while all patients with autoimmune T1D had positive GAD antibodies.
Table 3

Comparison between fulminant T1DM and autoimmune T1DM after SARS-CoV-2 vaccination

jkms-38-e209-i003
Variables Fulminant T1DM Autoimmune T1DM
Age, yr
Median (range) 42 (36–59) 54 (27–73)
Sex
Female/Male 4/2 4/4
BMI, kg/m2
Median (range) 18.6 (17.97–20.6) 21.9 (18.3–27.4)
HbA1c, %
Median (range) 7 (5.9–7.8) 10.3 (8.2–12.6)
Serum pancreatic enzyme Slightly high/Normal Normal
Serum C-peptide, ng/mL
Median (range) 0.01 (0.01–0.55) 0.92 (0.4–1.5)
Severity of acidosis Serious Partly serious
GAD antibody
Positive ratio 2/6 8/8
IA-2 antibody
Positive ratio 1/6 1/3
TPOAb Negative Partly positive
TgAb Negative Partly positive
T1DM = type 1 diabetes mellitus, SARS-CoV-2 = severe acute respiratory syndrome coronavirus 2, BMI = body mass index, HbA1c = hemoglobin A1c, GAD = glutamic acid decarboxylase, IA-2 = insulinoma-associated antigen-2, TPOAb = thyroperoxidase antibodies, TgAb = thyroglobulin antibodies.
In conclusion, we reported a patient with typical fulminant type 1 diabetes four days after SARS-CoV-2 protein subunit vaccination. The normal fasting blood glucose in the physical examination report seven weeks ago and normal HbA1c onset of this patient confirmed the connection between FT1D and this vaccine. We could not confirm the causal relationship between them, which requires long-term and large-scale population research. Nevertheless, we summarized the characteristics of the currently published FT1D following SARS-CoV-2 vaccination to help clinicians make early diagnosis and treatment. We highly appreciate the tremendous benefits of large-scale SARS-CoV-2 vaccination, but we still hope to alert about related adverse consequences and strengthen the pharmacovigilance and supervision during mass SARS-CoV-2 vaccination. It is important for clinicians to remain vigilant for acute deterioration of hyperglycemia and acidosis and we also recommend careful monitoring following SARS-CoV-2 vaccination even without a medical history of diabetes. Early identification and treatment can halt the progression of FT1D and prevent complications.

ACKNOWLEDGMENTS

We acknowledge the patient who agreed to participate in our study and all employees who were involved in the treatment of the patient.

Notes

Funding: This study was supported by National Natural Science Foundation of China (grant No. 81860163).

Disclosure: The authors have no potential conflicts of interest to disclose.

Author Contributions:

  • Conceptualization: Liang M, He Y.

  • Data curation: Huang L.

  • Formal analysis: Huang L.

  • Funding acquisition: Huang L.

  • Investigation: Huang L.

  • Methodology: Huang L.

  • Project administration: Huang L.

  • Resources: Huang L.

  • Supervision: Liang M, He Y.

  • Validation: Liang M, He Y.

  • Visualization: Liang M.

  • Writing - original draft: Huang L.

  • Writing - review & editing: Liang M, He Y.

References

1. Forgacs D, Silva-Moraes V, Sautto GA, Hanley HB, Gattiker JL, Jefferson AM, et al. The effect of waning on antibody levels and memory B cell recall following SARS-CoV-2 infection or vaccination. Vaccines (Basel). 2022; 10(5):696. PMID: 35632452.
2. World Health Organization. COVID-19 vaccine tracker and landscape. Accessed February 7, 2023. https://www.who.int/publications/m/item/draft-landscape-of-covid-19-candidate-vaccines. Updated 2023 .
3. Patrizio A, Ferrari SM, Antonelli A, Fallahi P. A case of Graves’ disease and type 1 diabetes mellitus following SARS-CoV-2 vaccination. J Autoimmun. 2021; 125:102738. PMID: 34653776.
4. Rela M, Jothimani D, Vij M, Rajakumar A, Rammohan A. Auto-immune hepatitis following COVID vaccination. J Autoimmun. 2021; 123:102688. PMID: 34225251.
5. Vuille-Lessard É, Montani M, Bosch J, Semmo N. Autoimmune hepatitis triggered by SARS-CoV-2 vaccination. J Autoimmun. 2021; 123:102710. PMID: 34332438.
6. Garrido I, Lopes S, Simões MS, Liberal R, Lopes J, Carneiro F, et al. Autoimmune hepatitis after COVID-19 vaccine - more than a coincidence. J Autoimmun. 2021; 125:102741. PMID: 34717185.
7. Sagy I, Zeller L, Raviv Y, Porges T, Bieber A, Abu-Shakra M. New-onset systemic lupus erythematosus following BNT162b2 mRNA COVID-19 vaccine: a case series and literature review. Rheumatol Int. 2022; 42(12):2261–2266. PMID: 36098769.
8. Sakurai K, Narita D, Saito N, Ueno T, Sato R, Niitsuma S, et al. Type 1 diabetes mellitus following COVID-19 RNA-based vaccine. J Diabetes Investig. 2022; 13(7):1290–1292.
9. Lin R, Lin YW, Chen MH. Fulminant type 1 diabetes mellitus after SARS-CoV-2 vaccination: a case report. Vaccines (Basel). 2022; 10(11):1905. PMID: 36423001.
10. Kobayashi T, Yakou F, Saburi M, Hirose A, Akaoka H, Hirota Y, et al. New-onset atypical fulminant type 1 diabetes after COVID-19 vaccination: a case report. Clin Case Rep. 2022; 10(10):e6473. PMID: 36267825.
11. Sasaki K, Morioka T, Okada N, Natsuki Y, Kakutani Y, Ochi A, et al. New-onset fulminant type 1 diabetes after severe acute respiratory syndrome coronavirus 2 vaccination: a case report. J Diabetes Investig. 2022; 13(7):1286–1289.
12. Tang X, He B, Liu Z, Zhou Z, Li X. Fulminant type 1 diabetes after COVID-19 vaccination. Diabetes Metab. 2022; 48(2):101324. PMID: 35091092.
13. Chee YJ, Ng SJ, Yeoh E. Diabetic ketoacidosis precipitated by Covid-19 in a patient with newly diagnosed diabetes mellitus. Diabetes Res Clin Pract. 2020; 164:108166. PMID: 32339533.
14. Fadini GP, Morieri ML, Boscari F, Fioretto P, Maran A, Busetto L, et al. Newly-diagnosed diabetes and admission hyperglycemia predict COVID-19 severity by aggravating respiratory deterioration. Diabetes Res Clin Pract. 2020; 168:108374. PMID: 32805345.
15. Liao HC, Wu WL, Chiang CY, Huang MS, Shen KY, Huang YL, et al. Low-dose SARS-CoV-2 S-trimer with an emulsion adjuvant induced th1-biased protective immunity. Int J Mol Sci. 2022; 23(9):4902. PMID: 35563292.
16. Silveira MM, Moreira GM, Mendonça M. DNA vaccines against COVID-19: perspectives and challenges. Life Sci. 2021; 267:118919. PMID: 33352173.
17. Ibrahim S, Monaco GS, Sims EK. Not so sweet and simple: impacts of SARS-CoV-2 on the β cell. Islets. 2021; 13(3-4):66–79. PMID: 33970787.
18. Drucker DJ. Diabetes, obesity, metabolism, and SARS-CoV-2 infection: the end of the beginning. Cell Metab. 2021; 33(3):479–498. PMID: 33529600.
19. Yang S, Li Y, Dai L, Wang J, He P, Li C, et al. Safety and immunogenicity of a recombinant tandem-repeat dimeric RBD-based protein subunit vaccine (ZF2001) against COVID-19 in adults: two randomised, double-blind, placebo-controlled, phase 1 and 2 trials. Lancet Infect Dis. 2021; 21(8):1107–1119. PMID: 33773111.
20. Tran TN, May BP, Ung TT, Nguyen MK, Nguyen TT, Dinh VL, et al. Preclinical immune response and safety evaluation of the protein subunit vaccine Nanocovax for COVID-19. Front Immunol. 2021; 12:766112. PMID: 34938290.
21. Lui DT, Lee KK, Lee CH, Lee AC, Hung IF, Tan KC. Development of Graves’ disease after SARS-CoV-2 mRNA vaccination: a case report and literature review. Front Public Health. 2021; 9:778964. PMID: 34888290.
22. Oikawa Y, Shimada A. Possible involvement of autoimmunity in fulminant type 1 diabetes. Diabetol Int. 2020; 11(4):329–335. PMID: 33088639.
23. Luo S, Ma X, Li X, Xie Z, Zhou Z. Fulminant type 1 diabetes: a comprehensive review of an autoimmune condition. Diabetes Metab Res Rev. 2020; 36(6):e3317. PMID: 32223049.
24. Imagawa A, Hanafusa T, Miyagawa J, Matsuzawa Y. Osaka IDDM Study Group. A novel subtype of type 1 diabetes mellitus characterized by a rapid onset and an absence of diabetes-related antibodies. N Engl J Med. 2000; 342(5):301–307. PMID: 10655528.
TOOLS
Similar articles