Signa Vitae. 2021; 17(2): 181-187. doi: 10.22514/sv.2020.16.0113
Original Research

Comparison of clinical characteristics in acute pancreatitis with and without diabetes mellitus: a retrospective study

Kun Song1,†, Cui-Rong Guo1,†, Chang-Luo Li1,*,, Ning Ding1,*,

1Department of Emergency Medicine, Changsha Central Hospital, University of South China, NO.161 Shaoshan South Road, Changsha, 410004 Hunan, P. R. China

*Corresponding Author(s):doctorlichangluo@sina.com (Chang-Luo Li) doctordingning@csu.edu.cn, doctordingning@sina.com (Ning Ding)

† These authors contributed equally.

† These authors contributed equally.

History Submitted: 31 October 2020 | Accepted: 25 November 2020 | Published: 08 March 2021
Copyright:  ©2021  The Author(s). Published by MRE Press.
This is an open access article under the CC BY 4.0 license (https://creativecommons.org/licenses/by/4.0/).

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Abstract

Background: Current research shows a cause-and-effect relationship between acute pancreatitis (AP) and diabetes mellitus (DM). In this study the difference in clinical features between AP with DM and AP without DM was analyzed to explore implications for the treatment of these two conditions. Methods: From January 2016 to December 2018 all patients with AP admitted to the Changsha Central Hospital were included in a retrospective study. Clinical and laboratory variables obtained from AP patients were analyzed and compared with a DM group and a non-DM group. Results: A total of 869 patients with AP including 139 patients in DM the group and 730 patients in the non-DM group were analyzed. Hypertension (P = 0.002), coronary heart disease (CHD, P = 0.003) and hypertriglyceridemia (P = 0.045) were more common in the DM than the non-DM group, while BISAP (P < 0.001) and Ranson (P < 0.001), the incidence of AP recurrence (P = 0.034) and length of hospital stay (P = 0.045) were significantly higher for the DM group as were levels of blood sugar (P < 0.001), glycated hemoglobin (P < 0.001), ALT (P = 0.003), AST (P = 0.032), BUN (P = 0.017), creatinine (P = 0.003), cholesterol (P < 0.001), LDL (P < 0.001) and TG (P < 0.001). Conclusion: AP patients with DM were prone to comorbidities with higher levels of organ function indicators and higher incidence of dyslipidemia and recurrence of AP.

Keywords:Acute pancreatitis;Diabetes mellitus;Comorbidity;Dyslipidemia
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Cite this article

Kun Song, Cui-Rong Guo, Chang-Luo Li, Ning Ding. Comparison of clinical characteristics in acute pancreatitis with and without diabetes mellitus: a retrospective study. Signa Vitae. 2021; 17(2): 181-187. doi: 10.22514/sv.2020.16.0113

1. Introduction

AP is still a disease with different clinical outcomes that vary from mild to severe depending on different clinical features such as comorbidities [1]. DM is a metabolic disorder with a chronically progressive evolution. It has a detrimental impact on multiple organs with both local and system complications and an incidence that has increased significantly over the last two decades [2]. Many researchers have shown a cause-and-effect relationship between AP and DM. A systemic review that included a total of 31 relevant studies with 13,894 subjects clarified that 23% patients with AP developed DM after discharge from hospital. Moreover, with the disease severity increasing, the occurrence of DM after AP similarly increased [3]. Other research in children with AP also showed that 6% of patients diagnosed with AP were subsequently diagnosed with DM when the exposure risk for DM was much higher, about 30-fold higher than expected in the general pediatric population [4]. In the case of chronic pancreatitis, DM was detected in more than 10% of pediatric patients and 31% of adult patients [5]. Alternatively, DM was one potential risk factor in patients that developed AP, especially when they were also diagnosed with severe hypertriglyceridemia [6]. A meta-analysis with eight cohort studies that included 14,124 cases and 5.7 million participants showed that DM was linked with a 74% increase in the risk of AP, a 39% increase in the risk of pancreatitis overall and a 40% increase in risk of chronic pancreatitis [7].

Recently, AP patients with DM have increasingly been admitted to hospitals. However, few studies have investigated the clinical characteristics of AP in the presence of DM. In the study reported here, the aim was to analyze the differences in clinical features between AP with DM and AP without DM to explore the implications for treatment of AP in the presence of DM.

2. Methods

2.1 Study design and patients

From January 2016 until December 2018, all patients with AP admitted to the Changsha Central Hospital were included in this retrospective study. Inclusion criteria were defined as follows: age ≥ 18 and confirmed diagnosis of AP. Study exclusion criteria included: death, age < 18, chronic pancreatitis, malignant tumors, chronic organ dysfunction (kidney, heart or liver dysfunction), pregnancy and patients with missing data.

AP was diagnosed based on its typical gastrointestinal symptoms (abdominal pain, distention or vomiting), laboratory tests (amylase or lipase) and medical imaging (abdominal ultrasonography or CT). Recurrent AP (RAP) was defined as: [1] confirmed AP, and [2] the interval between two or more separate attacks of AP with complete recovery was more than 3 months.

In this study, patients with a medical history of diabetes before an AP attack (based on medical records) and patients without a medical history of diabetes diagnosed with DM when admitted in hospital due to AP attack were included in the DM group. Following several AP attacks, only the clinical and laboratory data of the first attack were analyzed.

2.2 Data collection

The medical information of AP patients admitted within 24 hours of an attack was recorded. Data collected included: age, gender, body mass index (BMI), etiology (alcohol, hyperlipidemia, cholelithiasis), comorbidities (hypertension, COPD, coronary heart disease (CHD)) and laboratory variables. Laboratory variables including white blood cell (WBC), neutrophil, hematocrit (HCT), platelet (PLT), platelet distribution width (PDW), blood sugar, glycated hemoglobin, prothrombin time (PT), activated partial thromboplastin time (APTT), fibrinogen (Fbg), albumin (ALB), total bilirubin, creatinine, urea acid, amylase, lipase, lactate dehydrogenase (LDH), total calcium, alanine aminotransferase (ALT), aspartate aminotransferase (AST), blood urea nitrogen (BUN), cholesterol, low density lipoprotein (LDL), high density lipoprotein (HDL) and triglyceride (TG).

CT images were also recorded including CT grades, pleural effusion, abdominal effusion and lung infection. The scores of sequential organ failure assessment, bedside index of severity in acute pancreatitis (BISAP) and Ranson were calculated based on clinical and laboratory variables.

Clinical managements and outcomes included in-hospital incidence of acute respiratory distress syndrome (ARDS) and liver dysfunction, ICU admission, mechanical ventilation, length of stay (LOS) in hospital and AP recurrence.

2.3 Statistical analysis

Statistical results were given as mean ± standard deviation for normal data, while for non-normal data, interquartile range (IQR) and median were utilized. Categorical data were given as percentage and value. Comparison between two groups was made by a chi-squared test or Mann-Whitney U-test.

3. Results

Initially, a total of 898 patients with AP were enrolled. Based on the exclusion criteria, 29 patients were excluded and 869 patients with AP included. 139 patients in the DM group and 730 patients in non-DM group were analyzed retrospectively (Fig. 1). In the DM group, 118 patients had a medical history of diabetes while 21 patients were diagnosed with DM when admitted to hospital due to an AP attack. The general characteristics of the two groups are given in Table 1. There were no significant differences in age, BMI and sex within these two groups. In the DM group, the proportion of hypertension and CHD were 27.34% and 7.91% respectively, which were higher than that of the non-DM group. Hypertriglyceridemia, 49.64% in the DM and 40.68% in the non-DM group, was the most common etiology, followed by alcohol (19.42% vs. 24.38%) and cholelithiasis (15.83% vs. 22.05%). CT images showed no difference in grades, pleural effusion, abdominal effusion and lung infection between two groups. Only a few patients (1.47% vs. 2.33%) needed mechanical ventilation and CRRT was applied in some patients (13.67% vs. 14.11%). The scores of BISAP and Ranson were significantly higher in the DM group. The incidence of ICU admission (17.27% vs. 13.7%), ARDS (8.63% vs. 6.84%) and liver dysfunction (12.2% vs. 16.44%) in the two groups showed no significant differences. The median length of stay in hospital in the DM and non-DM groups was seven days (IQR5-10 days) and 6 days (IQR5-9 days), respectively. The recurrence incidence of AP in DM the group was significant higher than that seen for the non-DM group (32.37% vs. 23.84%).

Flow chart for patients enrollment and study design. Abbreviations: AP = acute pancreatitis.

Fig. 1.Flow chart for patients enrollment and study design. Abbreviations: AP = acute pancreatitis.

Table 1.General characteristics in DM group and non-DM group.
CharacteristicsDM group (n = 139)Non-DM group (n = 730)Total (n = 869)P value
Age (years)47.62 ± 15.7846.17 ± 14.130.277
18-44 (n, %)70 (50.36%)363 (49.73%)0.220
45-65 (n, %)46 (33.09%)281 (38.49%)0.234
> 65 (n, %)23 (16.55%)86 (11.78%)0.522
BMI (kg/m2)25.44 (23.97, 27.10)25.92 (22.95, 28.68)0.193
Sex (n,%)
Male96 (69.06%)516 (70.68%)6120.701
Female43 (30.94%)214 (29.32%)257
Smoking (n, %)40 (28.78%)220 (30.82%)0.105
Comorbidities (n, %)
Hypertension
Yes38 (27.34%)118 (16.16%)1560.002
No101 (72.66%)612 (83.84%)713
COPD
Yes3 (2.16%)9 (1.23%)120.392
No136 (97.84%)721 (98.77%)857
Coronary heart disease
Yes11 (7.91%)20 (2.74%)310.003
No128 (92.09%)710 (97.26%)838
Etiologies (n, %)
Alcohol
Yes27 (19.42%)178 (24.38%)2050.207
No112 (80.58%)552 (75.62%)664
Hypertriglyceridemia
Yes69 (49.64%%)297 (40.68%)3660.045
No70 (50.36%)433 (59.32%)503
Cholelithiasis
Yes22 (15.83%)161 (22.05%)1830.099
No117 (84.17%)569 (77.95%)686
CT grade (n, %)
D, E grade12 (8.63%)49 (6.71%)610.417
A, B, C grade127 (91.37%)681 (93.29%)808
Pleural effusion (n, %)
Yes29 (20.86%)128 (17.53%)1570.350
No110 (79.14%)602 (82.47%)713
Abdominal effusion (n, %)
Yes26 (18.71%)111 (15.21%)1370.299
No113 (81.29%)619 (84.79%)732
Lung infection (n, %)
Yes25 (17.77%)116 (15.89%)1410.539
No114 (82.01%)614 (84.11%)728
ICU admission (n, %)
Yes24 (17.27%)100 (13.70%)1240.270
No115 (82.73%)630 (86.30%)745
Mechanical ventilation (n, %)
Yes2 (1.47%)17 (2.33%)190.525
No126 (98.53%)666 (97.67%)792
Organ dysfunction (n, %)
ARDS12 (8.63%)50 (6.84%)0.472
Liver dysfunction17 (12.2%)120 (16.44%)0.253
Scoring system
BISAP1 (0,1)0 (0,1)< 0.001
SOFA0 (0,0.75)0 (0.1)0.870
RANSON1 (1,2.75)1 (0,1)< 0.001
LOS in hospital (days)7 (5,10)6 (5,9)0.045
Recurrence (n, %)
Yes45 (32.37%)174 (23.84%)2190.034
No94 (67.63%)556 (76.16)650
Abbreviations: AP = acute pancreatitis, DM = diabetes mellitus, BMI = body mass index, ARDS = acute respiratory distress syndrome, LOS = length of stay, SOFA = sequential organ failure assessment, BISAP = bedside index of severity in acute pancreatitis.

Laboratory variables are given in Table 2. There were no significant differences in WBC (P = 0.756), neutrophil (P = 0.808), HCT (P =0.152), PLT (P = 0.881), PDW (P = 0.242), PT (P = 0.745), APTT (P = 0.221), Fbg (P = 0.084), ALB (P = 0.088), total bilirubin (P = 0.264), urea acid (P = 0.953), amylase (P = 0.189), lipase (P = 0.169), LDH (P = 0.191), total calcium (P = 0.057) and HDL(P = 0.984) between two groups. The levels of blood sugar (P < 0.001), glycated hemoglobin (P< 0.001), ALT (P = 0.003), AST (P = 0.032), BUN (P = 0.017), creatinine (P = 0.003), cholesterol (P< 0.001), LDL (P < 0.001) and TG (P < 0.001) were significantly higher in the DM group.

Table 2.Comparison of laboratory characteristics between DM group and non-DM group.
VariablesDM group (n = 139)non-DM group (n = 730)P value
WBC ( 109/L)12.75 ± 5.9812.58 ± 4.450.756
Neutrophi l( 109/L)9.94 ± 4.3910.04 ± 4.510.808
HCT0.44 (0.41, 0.48)0.45 (0.41, 0.48)0.152
PLT ( 109/L)223.50 (174.25, 253.50)203.00 (165.50, 246.00)0.881
PDW (%)13.83 ± 2.7313.32 ± 4.950.242
Blood sugar (mmol/L)14.50 (11.80, 16.48)7.25 (6.20, 8.98)< 0.001
Glycated hemoglobin (mmol/L)10.15 (7.93, 11.17)5.60 (5.30, 6.10)< 0.001
PT (s)11.83 ± 1.5312.00 ± 5.760.745
APTT (s)24.45 (21.73, 27.95)27.65 (25.05, 29.80)0.221
Fbg (mg/dL)3.30 (2.65, 4.93)3.26 (2.59, 4.37)0.084
ALB (g/l)44.11 ± 7.2743.16 ± 5.620.088
ALT (u/L)32.40 (22.23, 49.33)25.75 (17.48, 44.08)0.003
AST (u/L)26.50 (19.55, 33.90)24.00 (17.30, 31.05)0.032
Total bilirubin (mmol/L)14.00 (10.97, 20.74)15.53 (10.54, 20.42)0.264
BUN (mmol/L)4.35 (3.30, 5.25)4.29 (3.52, 5.05)0.017
Creatinine (ummol/L)77.18 ± 60.1270.77 ± 36.060.003
Urea acid (ummol/L)350.10 ± 122.48350.75 ± 113.060.953
Amylase (u/L)269.50 (71.25, 644.00)218.00 (95.03, 491.00)0.189
Lipase (u/L)344.00 (85.50, 865.25)311.50 (81.25, 693.00)0.169
LDH (u/L)242.00 (172.50, 315.50)196.00 (165.50, 256.25)0.191
Total Cacium (mmol/L)2.35 (2.25, 2.55)2.33 (2.23, 2.49)0.057
Cholesterol (mmol/L)7.49 (4.92, 12.22)6.13 (4.79, 8.10)< 0.001
LDL (mmol/L)1.95 (1.16, 3.16)1.80 (1.30, 2.62)< 0.001
HDL (mmol/L)0.69 (0.51, 1.31)0.80 (0.66, 1.20)0.984
TG (mmol/L)14.76 (2.08, 22.76)9.48 (1.71, 15.01)< 0.001
Abbreviations: AP = acute pancreatitis, DM = diabetes mellitus, WBC = white blood cell, HCT = hematocrit, PLT = platelet, PDW = platelet distribution width, PT = prothrombin time, APTT = activated partial thromboplastin time, Fbg = fibrinogen, ALB = albumin, LDH = lactate dehydrogenase, ALT = alanine aminotransferase, AST = aspartate aminotransferase, BUN = blood urea nitrogen, LDL = low density lipoprotein, HDL = high density lipoprotein, TG = triglyceride.

4. Discussion

This study showed that in the DM group hypertension and CHD were more likely to be comorbidities and hypertriglyceridemia was more common than in the AP group. Much clinical research shows that DM, CHD, hypertension and hypertriglyceridemia affect each other. One study with a total of 643,439 subjects showed that hypertension and DM were the main manifestations of metabolic syndrome and that the incidence of hypertension in patients with DM was 43.7%, a factor of 1.49 times greater than that in patients without DM [8]. In a hypertensive population, systolic blood pressure (SBP) was associated with DM occurrence The higher the level of SBP, the higher the morbidity of DM [9]. Moreover, DM increased both the incidence and mortality of CHD by at least a factor of two due to dyslipidemia [10]. Hypertriglyceridemia as an abnormality of lipid metabolism is associated with insulin resistance. In a study with 15,932 participants, hypertriglyceridemia that persisted for more than two years was significantly associated with the incidence risk of DM [11].

BISAP and Ranson scores were higher and hospital LOS days were longer in the DM group, which indicated that disease severity was greater for those patients. A retrospective research study showed AP patients with DM to be more likely to developing severe pancreatitis and that DM was correlated with the MRI characteristics of pancreatic necrosis, infection, hemorrhage, and abdominal wall edema [12]. Previous studies have shown that the blood glucose level of patients with DM had a significant impact on AP progression, which may aggravate the development of local fluid collections or necrosis formation and lead to a prolonged disease period [13]. DM, as a one of the systematic metabolic disorders, was shown to impair immune system function and infection occurrence [14]. In the study reported here, no significant differences were found in lung infection and fluid collection, which was partly explained by the difference of clinical characteristics in patients between different hospitals.

Compared with the occurrence incidence of AP, patients with DM were prone to repeated AP attacks. Factors including alcohol, hypertriglyceridemia, higher CT scores and systemic inflammatory reaction have been associated with AP recurrence [15, 16, 17]. Hypertriglyceridemia is also an important risk factor for the development and recurrence of AP [18]. The excess hydrolyzed particles of TG in circulation are capable of ruining the vascular bed of the pancreas and vascular endothelium in microcirculation, which results in systemic inflammation and damage to pancreatic acinar cells [19].

In a comparison of laboratory variables between the two group, not only the level of blood sugar and glycated hemoglobin but also organ function indicators including ALT, AST, BUN and creatinine were significantly higher in the DM group. DM was associated with long-term damage to blood vessels including macrovascular and microvascular systems, which results in kidney and liver disfunction [20, 21]. A study of 9,621 DM patients verified that ALT and AST levels exceeding the upper limit of the normal range were present in 16.0% and 8.8%, respectively [22]. Higher levels of BUN and creatinine were associated with an increased risk of DM, while DM exacerbated kidney dysfunction [23].

Dyslipidemia, including elevated cholesterol, TG and LDL occurred in more AP patients with DM in this study. More patients in the DM group were diagnosed with AP due to hypertriglyceridemia, while DM was also associated with dyslipidemia.

A retrospective study of 1,999 DM patients concluded that the proportion with elevated LDL, TG and HDL were 34.8%, 27.8% and 15.4% of patients, respectively [24]. In children and youth with DM from India the prevalence of dyslipidemia was shown to be approximately 47.2% [25].

A recent study of the association of clinical features and outcomes of AP between diabetic and non-diabetic hospitalized patients showed that, with the exception of serum albumin, major clinical features and laboratory markers were significantly higher in a DM group and DM increased the disease severity of AP [26]. However, in the study reported here, larger samples were enrolled and the incidence of hypertriglyceridemia in AP was likely higher due to sample differences in the different studies and countries.

The strength of this study was that various significant clinical characteristics in AP with DM were identified. AP patients with DM were prone to having comorbidities with higher levels of kidney and liver function indicators and a higher incidence of dyslipidemia. During the COVID-19 pandemic period, clinical evidence suggested that the overall survival time of patients may be shortened, their quality of life reduced and that the risk of complications and need for critical care in the most severe cases would increase [27]. Hence, monitoring vital signs and laboratory variables more frequently is necessary for AP patients with DM.

One limitation of this study was that it was conducted at a single center in China and differences compared to other countries and populations should be considered. Another was that in this retrospective study, with some data missing, although patients in the DM group had a medical history of diabetes or had been diagnosed with DM after admission, T3cDM could not be clearly made as a diagnosis for them. Further research should be conducted to analyze the association of different types of diabetes with the effect of AP on clinical characteristics and outcomes. Finally, due to its retrospective design, longer patient follow-ups were not performed and data were collected from electronic clinical records and only clinical characteristics were analyzed. Future studies should focus on constructing models for predicting the risk of disease progression, evaluating the management of patients with severe complications and the discovery of indicators linked to different disease stages.

5. Conclusions

In this study, AP patients with DM were prone to having comorbidities with higher levels of organ function indicators and higher incidence of dyslipidemia and recurrence of AP.

Abbreviations

ALB, albumin; ALT, alanine aminotransferase; AP, acute pancreatitis; APTT, activated partial thromboplastin time; ARDS, acute respiratory distress syndrome; AST, aspartate aminotransferase; BMI, body mass index; BUN, blood urea nitrogen; CHD, coronary heart disease; DM, diabetes mellitus; Fbg, fibrinogen; HCT, hematocrit; HDL, high density lipoprotein; IQR, interquartile range; LDH, lactate dehydrogenase; LDL, low density lipoprotein; LOS, length of stay; PDW, platelet distribution width; PLT, platelet; PT, prothrombin time; RAP, recurrent acute pancreatitis; SBP, systolic blood pressure; TG: triglyceride; WBC, white blood cell.

Ethics approval and consent to participate

Ethics approval was provided by the Medical Ethics Committee of Changsha central Hospital (NO.CSH2020088). Due to the nature of retrospective study, informed consent was waived.

Availability of Data and Materials

Datasets used and/or analyzed in the present study were availed by the corresponding author on reasonable request.

Author contributions

The manuscript writing and patient’s data recording were done by Kun Song and Cuirong Guo. Ning Ding assisted in information collection. Changluo Li and Ning Ding analyzed and interpreted the patients’ general indices. The final manuscript was read and ratified by all authors.

Acknowledgements

I would like to express my gratitude to all those who helped me during the writing of this manuscript.

Funding

This manuscript was supported by the Sanitation and Health Committee Foundation of Hunan Province, China (NO.20200075).

Conflict of interest

The authors have no conflict of interest in this article.

Disclosure Statement

There are no real or apparent conflicts of interest to disclose.

References

Cho J, Scragg R, Petrov MS. Risk of Mortality and Hospitalization after Post-Pancreatitis Diabetes Mellitus vs Type 2 Diabetes Mellitus: a Population-Based Matched Cohort Study. American Journal of Gastroenterology. 2019; 114: 804-812.

[Google Scholar]

Yuanmei L, Qian Z, Fengsen X, Yankui W. Restricted gestational weight gain in overweight/obese women with gestational diabetes mellitus and pregnancy outcomes. Clinical and Experimental Obstetrics & Gynecology. 2019; 46: 763-769.

[Google Scholar]

Zhi M, Zhu X, Lugea A, Waldron RT, Pandol SJ, Li L. Incidence of new onset diabetes mellitus secondary to acute pancreatitis: a systematic review and meta-analysis. Frontiers in Physiology. 2020; 10: 637.

[Google Scholar]

Bellin MD, Lowe M, Zimmerman MB, Wilschanski M, Werlin S, Troendle DM, et al. Diabetes mellitus in children with acute recurrent and chronic pancreatitis: data from the international study group of pediatric pancreatitis: in search for a cure cohort. Journal of Pediatric Gastroenterology and Nutrition. 2019; 69: 599-606.

[Google Scholar]

Xie T, Hao L, Liu Y, Zhang D, Bi YW, Wang T, et al. Risk factor for diabetes mellitus in pediatric chronic pancreatitis patients. Medicine. 2019; 98: e17984.

[Google Scholar]

Li Q, Hou C, Peng Y, Zhu X, Shi C, Zhang K, et al. Diabetes and younger age are vital and independent risk factors for acute pancreatitis in patients with severe hypertriglyceridemia. BioMed Research International. 2019; 2019: 1-6.

[Google Scholar]

Aune D, Mahamat-Saleh Y, Norat T, Riboli E. Diabetes mellitus and the risk of pancreatitis: a systematic review and meta-analysis of cohort studies. Pancreatology. 2020; 20: 602-607.

[Google Scholar]

Xue M, Liu L, Wang S, Su Y, Lv K, Zhang M, et al. A simple nomogram score for screening patients with type 2 diabetes to detect those with hypertension: a cross-sectional study based on a large community survey in China. PLoS one. 2020; 15: e0236957.

[Google Scholar]

Zhang Y, Nie J, Zhang Y, Li J, Liang M, Wang G, et al. Degree of blood pressure control and incident diabetes mellitus in chinese adults with hypertension. Journal of the American Heart Association. 2020; 9: e017015.

[Google Scholar]

Găman MA, Cozma MA, Dobrică EC, Bacalbașa N, Bratu OG, Diaconu CC. Dyslipidemia: a trigger for coronary heart disease in romanian patients with diabetes. Metabolites. 2020; 10: 195.

[Google Scholar]

Kwon YH, Kim S, Cho JH, Kwon H, Park SE, Oh H, et al. The association between persistent hypertriglyceridemia and the risk of diabetes development: the kangbuk samsung health study. Endocrinology and Metabolism. 2018; 33: 55.

[Google Scholar]

Xiao B, Xu H, Jiang Z, Hu J, Yang G. Acute pancreatitis in patients with a medical history of type 2 diabetes mellitus. Pancreas. 2020; 49: 591-597.

[Google Scholar]

Singh S, Chang H, Richards TM, Weiner JP, Clark JM, Segal JB. Glucagonlike peptide 1-based therapies and risk of hospitalization for acute pancreatitis in type 2 diabetes mellitus: a population-based matched case-control study. JAMA Internal Medicine. 2013; 173: 534-539.

[Google Scholar]

Dunachie S, Chamnan P. The double burden of diabetes and global infection in low and middle-income countries. Transactions of the Royal Society of Tropical Medicine and Hygiene. 2019; 113: 56-64.

[Google Scholar]

Zhang W, Shan H, Gu Y. Recurrent acute pancreatitis and its relative factors. World Journal of Gastroenterology. 2005; 11: 3002-3004.

[Google Scholar]

Guda NM, Muddana V, Whitcomb DC, Levy P, Garg P, Cote G, et al. Recurrent acute pancreatitis: international state-of-the-science conference with recommendations. Pancreas. 2018; 47: 653-666.

[Google Scholar]

Gullo L, Migliori M, Pezzilli R, Oláh A, Farkas G, Levy P, et al. An update on recurrent acute pancreatitis: data from five European countries. The American Journal of Gastroenterology. 2002; 97: 1959-1962.

[Google Scholar]

Shemesh E, Zafrir B. Hypertriglyceridemia-related pancreatitis in patients with type 2 diabetes: links and risks. Diabetes, Metabolic Syndrome and Obesity: Targets and Therapy. 2019; 12: 2041-2052.

[Google Scholar]

Zhang R, Deng L, Jin T, Zhu P, Shi N, Jiang K, et al. Hypertriglyceridaemia-associated acute pancreatitis: diagnosis and impact on severity. HPB. 2019; 21: 1240-1249.

[Google Scholar]

Cole JB, Florez JC. Genetics of diabetes mellitus and diabetes complications. Nature Reviews Nephrology. 2020; 16: 377-390.

[Google Scholar]

Abro MUR, Butt A, Baqa K, Waris N, Khalaid M, Fawwad A. Association of serum liver enzyme Alanine Aminotransferase (ALT) in patients with type 2 diabetes. Pakistan Journal of Medical Sciences. 2018; 34: 839-843.

[Google Scholar]

Forlani G, Di Bonito P, Mannucci E, Capaldo B, Genovese S, Orrasch M, et al. Prevalence of elevated liver enzymes in Type 2 diabetes mellitus and its association with the metabolic syndrome. Journal of Endocrinological Investigation. 2008; 31: 146-152.

[Google Scholar]

Xie Y, Bowe B, Li T, Xian H, Yan Y, Al-Aly Z. Higher blood urea nitrogen is associated with increased risk of incident diabetes mellitus. Kidney International. 2018; 93: 741-752.

[Google Scholar]

Kim G, DeSalvo D, Guffey D, Minard CG, Cephus C, Moodie D, et al. Dyslipidemia in adolescents and young adults with type 1 and type 2 diabetes: a retrospective analysis. International Journal of Pediatric Endocrinology. 2020; 2020: 11.

[Google Scholar]

Shah N, Khadilkar A, Gondhalekar K, Khadilkar V. Prevalence of dyslipidemia in Indian children with poorly controlled type 1 diabetes mellitus. Pediatric Diabetes. 2020; 21: 987-994.

[Google Scholar]

Hossain M, Hosen Z, Kabir I, Karim MR, Rahim MA, Uddin KN. A comparative study on clinical features and outcomes of acute pancreatitis between diabetic and non-diabetic hospitalized patients. BIRDEM Medical Journal. 2020; 10: 172-181.

[Google Scholar]

Mitura K. The impact of COVID-19 pandemic on critical care and surgical services availability. Critical Care Innovations. 2020; 3: 43-50.

[Google Scholar]