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The clinical significance of body mass index in the early evaluation of acute biliary pancreatitis

Objective Obesity has increased across the globe in recent years and is considered an established risk factor for many diseases. The main objective was to investigate the early assessment value of Body Mass Index (BMI) in the prediction of severity in acute biliary pancreatitis (ABP) and by using BMI to evaluate the severity of ABP. Methods The retrospective analysis was designed to assess the relationship between Body Mass Index and the severity of acute pancreatitis in Beijing Jishuitan Hospital from January 2019 to December 2021. The SPSS 24.0 software was used for statistical analysis, Logistic Regression, and ROC curve for the factors affecting the severity of acute biliary pancreatitis. Results A total of 259 ABP patients were analyzed in our study. The BMI was significantly correlated with the Ranson scoring and MCTSI scoring (p = 0.000, 0.000). The difference in BMI in different severity of ABP patients was statistically significant (p = 0.000). The Logistic Regression analyses confirmed that BMI was an independent risk factor for the severity of ABP (p = 0.035). Combined detection of BMI, WBC, serum calcium, and SAMY in prognosis of the severity of acute pancreatitis positive rate is higher than single positive rate. Conclusion The BMI gradually increased with the severity of acute pancreatitis and was an independent risk factor for the condition. Combined detection of BMI and medical tests can effectively improve acute pancreatitis patients' clinical diagnostic accuracy and early treatment, and help to reduce complications.

Acute pancreatitis is one of the leading gastrointestinal disorders that require urgent clinical treatment and increase globally in recent years [1,2,3]. The most common cause of AP was gallstones and alcohol consumption, hypertriglyceridemia, obesity, diabetes, smoking, drugs, endoscopic retrograde cholangiopancreatography (ERCP), trauma, and infection are also well-known suspected risk factors of pancreatitis [4,5,6,7,8,9]. It represents a disease characterized by symptoms such as severe abdominal pain, nausea, and vomiting, which is due to the activation of various digestive enzymes [10,11]. The clinical course of acute pancreatitis is variable, ranging from local pancreatic inflammation to consequently systemic inflammatory response, which is divided into mild acute pancreatitis (MAP), moderately severe acute pancreatitis (MSAP), and severe acute pancreatitis (SAP). Infected pancreatic necrosis and/or sepsis are major complications contributing to death at any stage [12,13,14,15]. Most acute pancreatitis patients experience mild courses with early oral feeding result in rapid clinical recovery [16]. Nearly about 30% of patients may progress onto severe forms named hemorrhagic necrotizing pancreatitis or SAP, which would lead to systemic inflammatory response syndrome (SIRS), and even multiple organ dysfunction syndromeswith poor prognosis [17,18,19,20]. Therefore, early diagnosis and timely treatment are critical to guide fluid resuscitation and initiate high-dependency or intensive care treatment and reduce morbidity and mortality of SAP. Early and accurate evaluation of AP severity is important to prevent progression and clinical outcomes [21,22,23].
With the improvement of people's living standards and the change in dietary habits, overweight and obese people have increased across the globe in recent years. Obesity is measured by body mass index (BMI, kg/ m 2 ), and is considered an established risk factor for type 2 diabetes, hyperlipidemia, and gallstone, which are all risk factors for pancreatitis [24,25,26,27]. It has likely contributed to increasing the incidence and severity of acute pancreatitis [28,29,30,31]. In addition, high BMI has also been directly associated with an increased risk of acute pancreatitis in some prospective studies [32]. Moreover, obese patients have a higher risk of severe acute pancreatitis. Currently, there is no uniform standard for the diagnosis of obesity all over the world, and we have adjusted the obesity judgment criteria based on BMI in China by the Chinese Society for Metabolic & Bariatric Surgery (CSMBS), which makes it more suitable for Chinese conditions. According to the latest criteria, Chinese adults define a BMI in the range of 18.5 BMI<24.9 kg/m 2 as normal weight, 25.0 BMI<27.5 kg/m 2 as overweight, and BMI !27.5 kg/m 2 as obese [33,34,35]. Because of various definitions of BMI standards for obesity at home and abroad, this study is based on the most recent BMI standards in China to explore the judgment value of BMI and related clinical examinations in the evaluation of the early condition of acute pancreatitis. Since obesity and biliary diseases especially biliary stones are important factors causing pancreatitis, this study aimed to evaluate the clinical significance of BMI in the early assessment of the severity of acute biliary pancreatitis.

Patient selection
This study retrospectively included ABP cases who were admitted to Beijing Jishuitan Hospital from January 1, 2019, to December 31, 2021. The clinical features data analyzed in the study included general information such as sex, age, body mass index (BMI), history, and vital signs when admitted. Meanwhile, laboratory results, imaging tests, treatments, complications, and hospital stays. This study was approved by the Ethics Committee of the Beijing Jishuitan Hospital, and informed consent was obtained from all individuals.

Diagnostic criteria for acute pancreatitis
The diagnosis and classification of the severity of AP were defined according to the 2012 revision of the Atlanta Classification [14]. The diagnosis of AP requires 2 of the following 3 features: (1) abdominal pain consistent with the disease (2) serum lipase activity (or amylase activity) at least three times greater than the upper limit of normal; and (3) characteristic findings from abdominal imaging. Disease severity was graded as mild or moderately severe, based on the presence of local or systemic complications and transient/persistent organ failure. The diagnostic criteria of acute biliary pancreatitis (ABP) were as follows: the patients were grouped under the diagnostic criteria of AP, imaging examination found gallbladder stones and/or bile duct stones, and laboratory exams showed increased levels of ALT and bilirubin [36].

Modified CT severity index (MCTSI) scoring criteria
The degree of AP was also obtained by the established CT severity index (CTSI) developed by Balthazar et al. and the modified CT severity index (MCTSI) by Mortele et al [39,40] (Table 1). For the MCTSI, the morphologic severity of pancreatitis was categorized as mild (0-2 points), moderate (4-6 points), or severe (8-10 points). The MCTSI was easy to calculate, and more accurately to judge the severity of infection, organ failure, the length of hospital stays, and death [41,42,43]. Each score was applied independently to the investigated CT studies by both observers, who were blinded to all clinical parameters and the scoring results of their counterparts.

Statistical analysis
The categorical variables are presented as numbers and continuous variables are presented as medians and mean differences. The categorical variables were statistically compared by the chi-square Â 2 test. The Mann-Whitney U-test and t-test were used for continuous variables and measurement data. The logistic regression model was used to determine the independent factors for variables with significance in the univariate and multivariate analyses. The logistic regression was done by forward stepwise and wald p-value. The results are expressed as odds ratios (ORs) with 95% confidence intervals (CIs). The ROC curve was used for predicting SAP sensitivity analysis. P < 0.05 was considered as the significance level. SPSS 24.0 statistical software was used for all data analysis.

Results
A total of 259 patients with ABP were admitted to the study. There were 138 males (53.3%) and 121 females (46.7%). The mean age was 60.98 AE 1.03 (19-

The relationship between BMI and ranson score, MCTSI score in ABP patients
The BMI was significantly correlated with the Ranson score for ABP patients (p ¼ 0.000), and the results showed that the higher the Ranson score, the higher the proportion of patients with high BMI. Similarly, the BMI was also significantly correlated with the MCTSI score (p ¼ 0.000), and the difference was statistically significant. The higher the Ranson score, the higher the proportion of ABP patients with high BMI (Table 2).

The analyses of risk factors for the severity of ABP pancreatitis
The analysis was performed to evaluate the risk factors for the severity of acute pancreatitis. The BMI, Ranson score, MCTSI score, Recurrence, Live or not, and clinical complications were experienced higher in different severity of ABP patients, and the difference was statistically significant (p ¼ 0.000, 0.000, 0.000, 0.024, 0.000, 0.000). And the length of stay in the hospital was significantly longer for MSAP and SAP (p ¼ 0.003). With the gradual severity of ABP, the BMI level, WBC, AST, DBIL, blood glucose, UREA, LDH, D-dimer, serum amylase, and Creactive protein (CRP) were significantly increased (p ¼ 0.000, 0.000, 0.006, 0.034, 0.010, 0.031, 0.000, 0.000, 0.000 and 0.010), and the serum calcium level was significantly decreased (p ¼ 0.000), the difference was statistically significant. But there were no significant differences with sex, age, fatty liver, ALT, TBIL, CREA, triglyceride, total cholesterol, urinary amylase, and PCT (p > 0.05, Table 3). For further study, we divided the ABP patients into two groups including MAP and MSAP/SAP group, and we found that the severity of ABP were significantly associated with BMI, WBC, AST, blood glucose, UREA, CREA, Calcium, LDH, D-dimer, serum amylase, and C-reactive protein (CRP) were significantly increased (p ¼ 0.000, 0.000, 0.007, 0.002, 0.003, 0.023, 0.000, 0.001, 0.000 and 0.017). In the multivariate analysis, the BMI (p ¼ 0.035), WBC (p ¼ 0.025), serum calcium level (p ¼ 0.030), and serum amylase level (p ¼ 0.020) were all verified as independent risk factors for the severity of ABP (Table 4).

The diagnostic value of BMI, WBC, serum calcium, and serum amylase in the severity of ABP
The ROC curve showed that BMI, WBC, serum calcium and serum amylase had certain diagnostic values for the different severity of ABP, but combined examination of the four factors had the highest diagnostic value, with the Area Under Curve (AUC) of 0.887 and the sensitivity of 77.5% and the specificity of 85.7% (Table 5, Figure 1).

Discussion
Acute pancreatitis is a common acute abdominal disease, as an inflammatory disorder of the pancreas. It takes a great economic cost for a lot of hospital admissions, especially for moderately severe and severe AP [44]. For this reason, the determination of the severity of AP in early stage is crucial for achieving good clinical outcomes and reducing costs. Until now, there are many different scoring systems for the severity of acute pancreatitis, including the Ranson score, MCTSI score, BISAP score, APACHE-II scores, et al [45,46,47,48]. The severity of AP can be predicted based on clinical, laboratory, radiology, and biomarkers. However, the evaluation process of these scoring systems is too cumbersome, especially for the early judgment of SAP, and some coring systems could only be estimated 48 h or more after admission. The good predictor should be rapid, inexpensive, and easy to be implemented. With the improvement of people's living standards and changes in eating habits, the incidence of biliary tract diseases is getting higher and higher, and the resulting biliary pancreatitis is also gradually increasing. Therefore, we must evaluate the condition of ABP as soon as possible.
The serological test is simple and fast, easy for dynamic observation, and has good clinical application value. At present, the most commonly used diagnostic indicator for ABP is serum amylase, but serum amylase also tends to increase in patients with other abdominal diseases such as some biliary diseases, hepatitis, or tumors, while serum amylase in patients with pancreatic necrosis does not find an abnormal increase, and it is not directly proportional to the severity of the disease. Consequently, serum amylase is not the only index to judge the condition of ABP [49]. The ABP patients with severe stage often have elevated body temperature, elevated leukocytes, and organ dysfunction. Thus, the level of serum white blood cells (WBC) is an important reference factor to evaluate the condition of AP patients. In a prospective and multicenter study, the WBC and CRP level with in 24h from the onset of pain were significantly lower in mild and moderately severe than in severe AP [50]. A similar result for WBC and CRP was found in our study, but not for PCT, although the severe patients had a higher level of PCT. The decrease in serum calcium level is correlated with the severity of AP, and it is one of the sensitive  factors to evaluate the severity of AP [51]. Low serum calcium level has been demonstrated that it played as an important role in judging patients with severe AP, which was verified as an independent risk factor [52,53]. In our study, we also observed that the severity of ABP was not only significantly related to the Ranson score and MCTSI score but also closely related to the patient's WBC level, liver and kidney function, blood glucose, calcium, amylase, and other serological tests. These are similar to previous findings. With the change in people's lifestyle and dietary habits in recent years, the number of overweight and obese people is increasing. The BMI has become one of the most widely used evaluate the degree of obesity. Previous studies have shown that obesity is closely related to a variety of diseases, and more and more studies have shown that it may be related to the severity of acute pancreatitis, but fewer in China [54,55,56]. Lankisch PG et al. introduced BMI into acute pancreatitis for the first time in 1990, and proposed that obese patients were related to the acute occurrence of metabolic abnormalities, cholecystitis, hyperlipidemia, and acute pancreatitis [57]. De Waele et al. have shown that being overweight and obese can obviously promote the occurrence of various complications of acute pancreatitis and are high-risk factors for severe patients [58]. To date, one prospective study (68,158 participants and 424 cases) has investigated the association of both BMI and Waist circumference (WC) with acute pancreatitis [59]. Most obese patients have a large amount of fat accumulation around the abdominal viscera. A lot of fat accumulated around the pancreas provides the basis for pancreatic bleeding, necrosis, and saponification. Fat decomposition releases a large amount of free fatty acids, which in turn damages pancreatic acinar cells and capillaries and accelerates the activation of trypsinogen, In addition, free fatty acids and chyle particles can block pancreatic capillaries, easily form microthrombosis, block pancreatic blood vessels, lead to pancreatic microcirculation disorder, release a variety of inflammatory factors, aggravate systemic inflammatory response syndrome, and easily complicated with multiple organ failure. The condition of acute pancreatitis in obese patients may be more serious and the incidence of complications is higher [60,61,62,63] . Consistent with these previous studies, the BMI level of ABP patients is not only closely related to the Ranson score and MCTSI score of patients, but also the higher proportion of overweight and obese patients with the increase of score, and it is more prone to complications in our observations. The latest study showed that the obese patients carried an increased risk for longer hospitalization, morbidity, and mortality [64]. Although hypertriglyceridemia is a more common cause of acute pancreatitis, and its prevalence is higher in obese and overweight individuals, the severity of disease and clinical outcomes are not significantly associated with it [65]. Our study supports this view, but it remains controversial [66,67]and one of the reasons may be that the number of ABP patients in this study is too small. Moreover, BMI is also an independent risk factor for the severity of a patient's condition, which also confirms the above view. Furthermore, according to these independent factors, we combined the BMI level, serum WBC, calcium, and amylase to predict the severity of ABP with good sensitivity and specificity. This provides a good method for early judgment of the severity of ABP in the future. However, there are several limitations to the study. This study is a retrospective single-center study, and it has a certain deviation in case screening. We expect to conduct a larger-sample, multicenter research to improve the reliability and value of the combined factors in future research.

Conclusion
In conclusion, patients with high BMI are more likely to develop more serious acute biliary pancreatitis. BMI is an independent risk factor for the severity of acute pancreatitis. Combined detection of BMI, serum WBC, calcium, and amylase levels will help to improve the early judgment of SAP, more conducive to early and timely detection and treatment, further reducing complications and mortality.

Declarations
Author contribution statement Zhixue Zheng: Conceived and designed the experiments; Analyzed and interpreted the data; Wrote the paper.
Jing Tao Bi: Analyzed and interpreted the data. Xuan Cai and Ya Qi Liu: Contributed regents, materials, and data.

Funding statement
This research did not receive any specific grant from funding agencies in the public, commercial, or not-for-profit sectors.

Data availability statement
Data included in article/supp. material/referenced in article.