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 Table of Contents  
ORIGINAL ARTICLE
Year : 2021  |  Volume : 8  |  Issue : 4  |  Page : 140-149

Impact of fatty liver on acute pancreatitis severity and prognosis: A meta-analysis of English and Chinese studies


1 Department of Graduate School, Baotou Medical College, Inner Mongolia University of Science and Technology; Department of Imaging, The First Affiliated Hospital of Baotou Medical College, Inner Mongolia University of Science and Technology, Baotou City, Inner Mongolia Autonomous Region, China
2 Department of Imaging, The First Affiliated Hospital of Baotou Medical College, Inner Mongolia University of Science and Technology, Baotou City, Inner Mongolia Autonomous Region, China

Date of Submission28-Jun-2021
Date of Acceptance25-Nov-2021
Date of Web Publication17-Aug-2022

Correspondence Address:
Lin Luo
Department of Imaging, The First Affiliated Hospital of Baotou Medical College, Inner Mongolia University of Science and Technology, Baotou City 014 010, Inner Mongolia Autonomous Region
China
Qiang Chen
Department of Imaging, The First Affiliated Hospital of Baotou Medical College, Inner Mongolia University of Science and Technology, Baotou City 014 010, Inner Mongolia Autonomous Region
China
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Source of Support: None, Conflict of Interest: None


DOI: 10.4103/RID.RID_10_22

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  Abstract 


BACKGROUND: Previous studies showed a significant correlation between fatty liver (FL) and acute pancreatitis (AP) onset, but the impact of FL on AP severity and prognosis remains uncertain. Therefore, we systematically searched existing publications in English and Chinese and conducted a meta-analysis to evaluate the effect of FL on AP severity and prognosis.
OBJECTIVE: The purpose of this study was to analyze the correlation between FL and AP severity and prognosis.
MATERIALS
AND METHODS:
All published controlled clinical studies on the relationship between FL and AP were identified by searching available electronic databases. We assessed the impact of FL disease on AP biochemical indicators, severity, and prognosis using pooled individual studies with an odds ratio (OR), standardized mean difference, and weighted mean difference.
RESULTS: Thirteen clinical case − control studies met the meta-analysis entry criteria, and these studies included 6570 patients; among them, 2110 were patients with FL-relatedAP (FLAP) and 4460 were patients with non-FL-related AP (NFLAP). The meta-analysis results showed that the percentage of mild AP in FLAP was lower than that in NFLAP (OR = 0.32, P < 0.001), but the percentage of moderately severe AP (MSAP) and severe AP (SAP) in FLAP was higher than that in NFLAP (OR = 2.66 and 2.57, respectively, P < 0.001). The various prognostic indicators included the acute physiology and chronic health evaluation II score, systemic complications, local complications, total length of hospital stay, and mortality, which were all significantly higher in FLAP than in NFLAP (P < 0.05 for all).
CONCLUSION: AP severity and prognosis were different between FLAP and NFLAP patients, and FL could be used as an independent risk factor for MSAP and SAP.

Keywords: Acute pancreatitis, fatty liver, meta-analysis, prognosis, severity


How to cite this article:
Jiang M, Zhang M, Zhang L, Luo L, Chen Q. Impact of fatty liver on acute pancreatitis severity and prognosis: A meta-analysis of English and Chinese studies. Radiol Infect Dis 2021;8:140-9

How to cite this URL:
Jiang M, Zhang M, Zhang L, Luo L, Chen Q. Impact of fatty liver on acute pancreatitis severity and prognosis: A meta-analysis of English and Chinese studies. Radiol Infect Dis [serial online] 2021 [cited 2022 Oct 6];8:140-9. Available from: http://www.ridiseases.org/text.asp?2021/8/4/140/353891




  Introduction Top


Acute pancreatitis (AP) is a common disease of the digestive system. It is generally caused by trypsin activation, pancreatic tissue digestion, and local pancreatic inflammation with or without changes in other organ functions. Clinically, most AP patients usually show mild and self-limited disease. However, 20%–30% of AP patients develop severe disease, and mortality for these patients can be 5%–10%.[1] AP clinical characteristics include rapid disease progression, poor treatment effect, easy recurrence, multiple complications, easy progression to multiorgan dysfunction, and a high fatality rate.

Some studies[2],[3],[4],[5] have shown that metabolic syndrome (MetS) can affect AP progress and prognosis. AP patients with MetS at admission have a higher risk of moderately severe AP (MSAP) and severe AP (SAP) and mortality.[2] Nonalcoholic fatty liver disease (NAFLD) is considered to be a manifestation of obesity and MetS involving the liver, and there is an interactive relationship between NAFLD and MetS.[4] NAFLD is a phenotype of hepatic MetS with a worldwide incidence of 28.01–52.34/1000 general population.[6] NAFLD is also a leading cause of chronic liver disease and has become a leading cause of liver disease-related morbidity and mortality in western countries.[7] A meta-analysis[8] reported that the prevalence of NAFLD is estimated to be 29.2% in China, which exceeds the global prevalence, and its incidence is increasing rapidly at a rate of 0.594% per year from 2008 to 2018. Therefore, it is important to explore the relationship between NAFLD and AP severity for early prediction of AP severity and active prevention and treatment of its serious complications. Although fatty liver (FL) is significantly associated with AP onset, it is important to further determine the effect of FL on AP patient prognosis.


  Materials and Methods Top


Search strategy

The literature was searched from January 2000 to July 2021 without restricting the region, publication type, or language. The main sources were PubMed, EMBASE, the Cochrane Library, WEB OF SCIENCE, and OVID for articles in English, and CNKI, CQVIP, and WANFANG electronic databases for articles in Chinese. Search keywords were as follows: (”FL” OR “steatohepatitis” OR “steatohepatitides” OR “steatosis of liver” OR “visceral steatosis” OR “visceral steatoses” OR “liver steatosis” OR “liver steatoses” OR “hepatic steatosis”) AND (”pancreatitis” OR “pancreatitides”). A manual search of the references in the retrieved articles was also performed to check for all relevant publications and avoid omissions.

Definitions and diagnostic criteria

Two of the following three features are required to diagnose AP:[9] (1) persistent pain in the upper abdomen (pain is acute, severe, and often radiating from the back); (2) serum amylase and/or lipase levels exceeding three-times the normal upper limit; and (3) classical imaging findings consistent with AP.

In accordance with the revised Atlanta Classification,[10] AP severity is divided into the following three grades: mild (MAP), MS (MSAP), and SAP. MAP involves no organ failure and no local or systemic complications. MSAP is characterized by temporary organ failure and/or local or systemic complications within 48 h without persistent organ failure. SAP is defined as persistent organ failure lasting more than 48 h.

FL is diagnosed when the liver density is lower than that of the spleen or vessels in the liver on computed tomography (CT) imaging[9] or when the liver echo is stronger than that of the spleen or kidney on abdominal ultrasound.[11]

NAFLD was diagnosed when all the following criteria were met:[12],[13] (1) liver steatosis detected by imaging (CT scan or abdominal ultrasound); (2) absence of alcoholic liver disease; (3) absence of medications and diseases that can cause liver steatosis; and (4) absence of other chronic liver disease causes.

The World Health Organization Western Pacific Region[14] has indicated the body mass index (BMI) cutoff points that were used to define an obese state (BMI ≥25 kg/m2).

Systemic inflammatory response syndrome (SIRS) is defined as the presence of two or more of the following:[15] (1) temperature >38°C or <36°C; (2) heart rate >90 beats/min or hypotension (systolic blood pressure <90 mmHg or >40 mmHg lower than the baseline); (3) shortness of breath (>20 breaths/min) or hyperventilation (partial pressure of carbon dioxide [PaCO2] <32 mmHg); and (4) peripheral blood leukocyte count >12 × 109/L or neutral rod-shaped granulocyte ratio >10%.

Organ failure was defined as a score ≥2 on one of the three assessed organ systems (cardiovascular, respiratory, and renal) using the modified Marshal scoring system. Persistent organ failure was considered if organ failure lasted more than 48 h.[16] Local complications included acute peripancreatic fluid collection, pancreatic pseudocyst, acute necrotic collection, and walled-off necrosis.[17],[18] Systemic complications were defined as an exacerbation of preexisting comorbid disease precipitated by AP.

Inclusion and exclusion criteria for studies

The inclusion criteria for the present study were as follows: (1) AP patients with or without FL (study population); (2) patients with FL AP (experimental group) or patients with non-FL AP (NFLAP) (control group); (3) randomized control grouping design; and (4) the purpose of each study was to compare the characteristics of fatty liver-related acute pancreatitis (FLAP) and NFLAP patients, and the data provided was complete.

The exclusion criteria for this study included the following: (1) studies irrelevant to the subject of this study; (2) case reports, literature reviews, and matched case − control studies with a certain age or sex ratio; (3) the Atlanta Classification criteria[10] was not used to grade AP severity; and (4) duplicate or poor quality reports.

Data extraction

Two investigators (MKJ and MZ) extracted the data independently using a unified standardized statistical table, and the data were extracted in a double-blind manner, with disputes resolved through discussion or by consensus with a third reviewer (quality control). Extracted data included the following:first author name, publication year, country, clinical results, Newcastle–Ottawa score (NOS), and participant characteristics (such as average age, sample size, and imaging method). For studies with insufficient data, the reviewers contacted thefirst author to obtain and verify the data. All researchers who participated in data extraction had more than 5 years of clinical experience.

Article quality evaluation

Retrospective study quality was assessed using a modified NOS, which consisted of the following three factors: object selection, study group comparability, and outcome assessment. Each study received a score of 0–9 (allocated as stars). Randomized controlled trials and observational studies achieving six or more stars were considered to be of high quality. Two investigators (LRZ and LL) had more than 10 years of clinical experience, and they independently assessed the studies' quality. The Preferred Reporting Items for Systematic Reviews and Meta-Analyses guidelines[19],[20] were used to design and perform this study.

Statistical analysis

Statistical analysis was performed using STATA version 15.0 software (StataCorp LP, College Station, TX, USA). Each experimental variable was calculated using the weighted mean difference (WMD), if the same unit was used in the included studies) or standardized mean difference (SMD, if the unit used in the included studies was different) for continuous data, and the odds ratio (OR) was used for binary data. For continuous data, the sample mean and standard deviation were estimated using the sample size, median, range, and/or quartile range in accordance with the method reported by Shi et al.[21] and Wan et al.[22] All results were reported with 95% confidence intervals (CIs). The Chi-square test was used for quantitative analysis of inter-study heterogeneity in the included studies. I2 <50% was defined as low heterogeneity, and I2 ≥50% was considered to represent high inter-study heterogeneity. If there was significant heterogeneity between studies, the random effects model was used; otherwise the fixed effects model was used. Subgroup analysis was conducted in accordance with the language and imaging method used for FL examination. Publication bias was reflected by the Begg rank correlation method and a funnel plot. When the funnel plot was nonsymmetrical or the Z-statistic was >1.96, P < 0.05 was calculated using the Begg rank correlation method, and this suggested publication bias; otherwise there was no publication bias. A two-sided P < 0.05 was considered to be statistically significant.


  Results Top


Articles retrieved

Initially, 281 related articles (125 in English and 156 in Chinese) were selected on the basis of the search keywords, and 126 possibly related clinical studies (52 in English and 74 in Chinese) were obtained after removing duplicates. After reading the title and abstract, 76 (18 in English and 58 in Chinese) of the 126 articles met the criteria. After reading the full text, 13 articles (four in English and nine in Chinese)[7],[9],[11],[23],[24],[25],[26],[27],[28],[29],[30],[31],[32] met the inclusion and exclusion criteria. [Figure 1] shows the screening process for the eligible studies, and the characteristics of each included article is presented in [Table 1].
Figure 1: Flowchart for identifying relevant studies. If the studies were from same institute and the sampling time was similar, the higher quality study (NOS score) was included in our study and the lower quality study was excluded. NOS: Newcastle–Ottawa score.

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Table 1: General characteristics of included studies

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Quality evaluation of the included articles

The 13 included studies were all clinical case − control studies. Our quality evaluation of the included articles showed that all the articles scored between 7 and 8 points (stars). This indicated that the included articles were of good quality [Table 1].

General situation, etiology, and basic disease in fatty liver-related acute pancreatitis and Non fatty liver-related acute pancreatitis patients

As shown in [Table 2], the mean age of FLAP patients was significantly lower than that of NFLAP patients (WMD = −5.21, P < 0.001), whereas the percentage of male FLAP patients was significantly higher than that of NFLAP patients (OR = 2.11, P < 0.001). The percentage of obesity, BMI, and waist circumference (WC) in FLAP patients were all significantly higher than those in NFLAP patients (OR = 2.33 for percentage of obesity, WMD = 2.41 and 6.20 for BMI and WC, respectively; P < 0.001 for all).
Table 2: Comparison of variables of patients in fatty liver-related acute pancreatitis and nonfatty liver-related acute pancreatitis

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The main cause of AP was different between FLAP and NFLAP patients. Gallstones were a more common cause in NFLAP than in FLAP patients (OR = 0.38, P < 0.001). Conversely, alcohol-induced AP and hyperlipidemic AP were more commonly observed in FLAP than in NFLAP patients [OR = 1.78 and 3.88, respectively; P < 0.001, [Table 2].

The prevalence of chronic disease was different in FLAP and NFLAP patients. Diabetes was more common in FLAP than in NFLAP patients (OR = 1.51, P = 0.006), while coronary heart disease was more common in NFLAP than in FLAP patients (OR = 0.54, P = 0.017). There was no significant difference in the incidence of hypertension between the two groups (P = 0.294).

Biochemical indicators for fatty liver-related acute pancreatitis and Non fatty liver-related acute pancreatitis

Triglycerides (TGs), alanine aminotransferase (ALT), aspartate amino transferase (AST), and blood glucose levels in FLAP patients were all significantly higher than those in NFLAP patients (WMD = −18.87 and − 23.94 for ALT and AST, respectively; SMD = 0.62 and 0.47 for TG and blood glucose, respectively; P < 0.05 for all). However, the white blood cell (WBC) count and total cholesterol (TC) in FLAP patients were significantly lower than those in NFLAP patients (WMD = 2.19 and 1.29 for WBC count and TC, respectively; P < 0.001 for all). There was no significant difference in C-reactive protein between the two groups [P = 0.164, [Table 2].

Impact of fatty liver on acute pancreatitis severity

The incidence of MAP in FLAP patients was lower than that in NFLAP patients [OR = 0.32, P < 0.001, [Table 2] and [Figure 2]a. Conversely, the incidence of MSAP, SAP, and MSAP + SAP in FLAP was all significantly higher than those in NFLAP patients [OR = 2.66, 2.57, and 3.17, respectively, P < 0.001, [Table 2] and [Figure 2]b, [Figure 2]c, [Figure 2]d.
Figure 2: Forest map of acute pancreatitis severity. (a) Forest map for mild acute pancreatitis; (b) Forest map for moderately severe acute pancreatitis; (c) Forest map for severe acute pancreatitis; (d) Forest map for moderately severe + severe acute pancreatitis

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Effect of fatty liver on acute pancreatitis patient prognosis

The outcome variables reflecting the prognosis of AP patients with FLAP or NFLAP included local complications, organ failure, acute physiology and chronic health evaluation II (APACHE II) score, systemic complications, total length of hospital stay (LHS), and mortality. A comprehensive analysis of local complications showed that the incidence of acute fluid accumulation and acute necrotic material accumulation in the FLAP group were all significantly higher than those in the NFLAP group (OR = 3.28 and 2.84, respectively, P < 0.001 for all). FLAP patients had a higher incidence of circulatory failure, respiratory failure, metabolic disorders, infection, and SIRS than NFLAP patients (OR = 2.64, 3.40, 3.85, 1.48, and 2.64, respectively, P < 0.001 for all). The incidence of persistent organ failure was also higher in FLAP compared with NFLAP patients (OR = 2.28, P < 0.001). However, the incidence of renal failure was not statistically significantly different between the two groups (P = 0.366). The APACHE II score and LHS (WMD = 2.11, P < 0.001 for the APACHE II score; WMD = 1.49, P = 0.010 for LHS) as well as the incidence of systemic complications and mortality (OR = 3.38 and 2.78, respectively, P < 0.001) were all significantly higher in FLAP compared with NFLAP patients.

Publication bias and subgroup analysis

Publication bias was assessed using funnel plots, and the analysis focused on the publication bias for the three AP grades. Funnel plots were mostly symmetrical across the MAP, MSAP and SAP groups [Figure 3]. The Begg rank correlation method showed that all the results met the Z-score criterion of z < 1.96, P > 0.05 (P > 0.373, z = 0.89; P > 0.902, z = 0.12; P > 0.348, z = 0.94; and P > 0.373, z = 0.89 for MAP, MSAP, SAP, and MSAP + SAP, respectively). The above analysis indicated that there was no publication bias. There was no significant reduction in heterogeneity in subgroup analyses of language and the FL imaging method in MAP and MSAP.
Figure 3: Funnel graph of acute pancreatitis severity. (a) Funnel graph for mild acute pancreatitis; (b) Funnel graph for moderately severe acute pancreatitis; (c) Funnel graph for severe acute pancreatitis; (d) Funnel graph for moderately severe + severe acute pancreatitis

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  Discussion Top


AP combined with FL is commonly observed in clinical practice. Previous reports indicated that 18%–59% of AP patients had concurrent FL.[7],[9],[11],[23],[24],[25],[26],[27],[28],[29],[30],[31],[32] However, the effect of FL on AP severity and prognosis remains unclear. In this meta-analysis, we reviewed 281 related English and Chinese articles, and included 13 clinical case − control studies that met the inclusion and exclusion criteria. Among these studies, 11 were from China,[7],[11],[24],[25],[26],[27],[28],[29],[30],[31],[32] one was from Korea,[9] and one was from Croatia.[23] There were 6570 patients included in these 13 articles. To the best of our knowledge, two meta-analyses with similar topics have been reported by Hou et al.[33] and Váncsa et al.[34] The former study focused on English studies, and no studies in other languages were included. The latter meta-analysis focused on the correlation between FL and AP patient outcomes, but the relevant clinical indicators were not discussed. Our study included high-quality recent studies in both English and Chinese, and we analyzed the difference in the patients' general situation, etiology, basic disease, biochemical indicators, AP severity, and factors related to AP patient prognosis between the FLAP and NFLAP groups.

With the current rapid economic development, an increasing number of young people prefer a diet that is high in fat and calories. The incidence of obesity, hyperlipidemia, and FL is gradually increasing, especially in younger people.[33] The results of the present study suggest that FLAP patients are younger and have a higher proportion of obesity, and hyperlipidemia is a main cause of AP in these patients. Although it is widely recognized that the underlying chronic disease is a risk factor influencing AP severity and prognosis,[35],[36],[37] we found no difference in the incidence of basic disease in FLAP and NFLAP patients. This may be related to the younger age of patients in the FLAP group, but it may also be due to the different criteria for judging chronic disease that were used in the included studies. Biochemical indicator levels such as WBC count, TG, ALT, AST, and blood glucose were all different between FLAP and NFLAP patients. These differences may derive from the different main causes of AP; gallstones were the main cause of NFLAP, while alcohol abuse and hyperlipidemia were main causes of FLAP.[7]

FLAP patients have a higher proportion of MSAP and SAP; incidence of local complications, organ failure, and systemic complications; and APACHE II score, LHS, and mortality. These results suggest that FL may be an independent risk factor for a severe clinical course of AP, in addition to alcohol, gallstones, and obesity. The clinical course of AP is variable, ranging from mild or moderate to severe. The Chinese Guidelines for Diagnosis and Treatment of AP (Shenyang, 2019)[18] indicate that organ failure is a key factor in AP severity and clinical outcome. In clinical practice, persistent organ failure is the most clinically significant indicator of AP severity, and mortality of patients with persistent organ failure is over 30%.[38] Although infectious necrosis of the pancreas and sepsis are major complications that lead to death, the leading cause of early death is persistent organ failure. Thus, early identification of patients who are at risk of developing persistent organ failure is critical.

The pathogenesis of FL aggravating pancreatitis is complex, and its underlying mechanism has not been clarified. The following hypotheses have recently been suggested. First, FL is often accompanied by hyperlipidemia. The direct cytotoxic effects of free fatty acids may impact on the pancreatic acinus and vascular endothelial cells, while a high concentration of free fatty acids and TGs may increase blood viscosity and block pancreatic blood circulation. The presence of free fatty acids can also induce acidosis.[39] Second, in the rat models of AP, hepatic steatosis inhibits alpha 1-antitrypsin (PPARα1) levels, and decreased serum PPARα1 levels may further lead to overactivation of inflammation, which exacerbates AP.[40] Third, studies have shown that PPARα signaling and fatty acid degradation pathways are involved in the pathological process of FLAP, suggesting that FL may aggravate pancreatitis through these pathways.[41] Finally, in AP, destruction of the internal environment, the cytotoxic effect of free fatty acids on pancreatic tissues, and activation of granulocytes caused by trypsin activation can all initiate the inflammatory response, cause SIRS or multiple organ dysfunction syndrome, and aggravate pancreatic tissue damage.

The above analysis shows that FL may be an independent risk factor for a severe clinical AP disease course, and it can be diagnosed using CT or ultrasound in the early disease stage. FL examination may contribute to the early prediction and identification of MSAP and SAP as well as to timely guidance of fluid resuscitation and initiation of high dependence or intensive care treatment. Currently, some scoring systems allow clinicians to judge AP severity, such as improved Marshall ratings, APACHE II, the bedside index for severity in AP, and the Japanese pancreatitis severity score, which have been used for decades.[42] However, all of these systems have common shortcomings such as numerous monitored parameters, complicated calculations, poor operability, limited clinical application (especially in the emergency department), difficulty making a prediction in a timely and accurate manner, difficulty identifying severe risks, and inability to use corresponding measures to reduce the damage to distant organs. Therefore, a rapid, simple, and accurate method is urgently required for early assessment of AP patients who are at severe risk. We know that the severity and prognosis in FLAP patients are significantly different from those in NFLAP patients, so FL should be included in the primary early assessment of AP patients. FLAP patients should undergo more aggressive symptomatic treatment and clinical care as well as intensive monitoring.

There are some limitations in this meta-analysis. On the one hand, only 13 related studies were included in the present study, and the number of studies involving a certain indicator is even smaller, which limits the strength of the systematic evaluation of the results. On the other hand, the subgroup analysis showed that heterogeneity of some indicators was still relatively high. We speculate that the heterogeneity may result from the different criteria that were used in different studies.


  Conclusion Top


This meta-analysis suggests that FL could affect AP biochemical marker levels, severity, and clinical outcomes. These results indicate that FL could be used as a timely and accurate method to predict and identify MSAP and SAP.

Acknowledgments

The authors thank Min Zhang MD, Dou Jin MD, and Professors Yanbing Ding and Chunyan Niu, who provided us with the original experimental data. This study was supported by grants from the Scientific Research Foundation of Baotou Medical College (BYJJ-QM 201753). We also thank Jodi Smith, PhD, ELS, from Liwen Bianji (Edanz) (www.liwenbianji.cn/), for editing the English text of a draft of this manuscript.

Financial support and sponsorship

Nil.

Conflicts of interest

There are no conflicts of interest.



 
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