key: cord-1001936-umqak71b
authors: Miró, Òscar; Llorens, Pere; Jiménez, Sònia; Piñera, Pascual; Burillo‐Putze, Guillermo; Martín, Alfonso; Martín‐Sánchez, Francisco Javier; Lambereche, Jorge; Alquézar‐Arbé, Aitor; Jacob, Javier; Noceda, José; Cano, María José Cano; Fortuny Bayarri, María José; Marín Porrino, Juan Miguel; Meléndez, Napoleón; Pérez García, Carles; Brasó Aznar, José Vicente; Ponce, María Carmen; Díaz Fernández, Elena; Ejarque Martínez, Laura; Peiró Gómez, Ana; Tost, Josep; Domínguez, María Jesús; Teigell Muñoz, Francisco Javier; González del Castillo, Juan
title: A case‐control emergency department‐based analysis of acute pancreatitis in Covid‐19: Results of the UMC‐19‐S(6)
date: 2020-12-01
journal: J Hepatobiliary Pancreat Sci
DOI: 10.1002/jhbp.873
sha: 4c57b13a097811e9cf1e02940ffc4354f5243ab7
doc_id: 1001936
cord_uid: umqak71b

OBJECTIVE: We investigated the incidence, risk factors, clinical characteristics and outcomes of acute pancreatitis (AP) in patients with COVID‐19 attending the emergency department (ED), before hospitalization. METHODS: We retrospectively reviewed all COVID patients diagnosed with AP in 62 Spanish EDs (20% of Spanish EDs, COVID‐AP) during the COVID outbreak. We formed two control groups: COVID patients without AP (COVID‐non‐AP) and non‐COVID patients with AP (non‐COVID‐AP). Unadjusted comparisons between cases and controls were performed regarding 59 baseline and clinical characteristics and 4 outcomes. RESULTS: We identified 54 AP in 74,814 patients with COVID‐19 attending the ED (frequency=0.72‰, 95%CI=0.54‐0.94‰). This frequency was lower than in non‐COVID patients (2,231/1,388,879, 1.61‰, 95%CI=1.54‐1.67; OR=0.44, 95%CI=0.34‐0.58). Etiology of AP was similar in both groups, being biliary origin in about 50%. Twenty‐six clinical characteristics of COVID patients were associated with a higher risk of developing AP: abdominal pain (OR=59.4, 95%CI=23.7‐149), raised blood amylase (OR=31.8; 95%CI=1.60‐632) and vomiting (OR=15.8, 95%CI=6.69‐37.2) being the strongest, and some inflammatory markers (C‐reactive protein, procalcitonin, platelets, D‐dimer) were more increased. Compared to non‐COVID‐AP, COVID‐AP patients differed in 23 variables; the strongest ones related to COVID symptoms, but less abdominal pain was reported, pancreatic enzymes raise was lower, and severity (estimated by BISAP and SOFA score at ED arrival) was higher. The in‐hospital mortality (adjusted for age and sex) of COVID‐AP did not differ from COVID‐non‐AP (OR=1.12, 95%CI=0.45‐245) but was higher than non‐COVID‐AP (OR=2.46, 95%CI=1.35‐4.48). CONCLUSIONS: Acute pancreatitis as presenting form of COVID‐19 in the ED is unusual (<1‰ cases). Some clinically distinctive characteristics are present compared to the remaining COVID patients and can help to identify this unusual manifestation. In‐hospital mortality of COVID‐AP does not differ from COVID‐non‐AP but is higher than non‐COVID‐AP, and the higher severity of AP in COVID patients could partially contribute to this increment.

Participating centres: 

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Infection by SARS-Cov-2 is mainly characterized by fever and respiratory symptoms, with dyspnea and lung infiltrates being present in more than 50% of hospitalized cases 1 . A significant number of other signs and symptoms can also be present, involving the gastrointestinal tract, hepatic inflammation, myalgia and rhabdomyolysis, or a pro-coagulant state, biochemically detected by increased D-dimers, which is related to complications and a worse prognosis [1] [2] [3] [4] . In addition, isolated case reports and short case series have described unusual clinical manifestations in patients with COVID-19. However in some patients, some of these entities appear after the patient has been admitted -o -while the patient is hospitalized and, to some extent, represent the expression of the increased number of complications that may be developed by patients who are bedridden, multidrug-treated and/or in very poor condition. In this scenario, it is difficult to quantify the real association of a certain manifestation with the pathogenesis of the disease caused by SARS-Cov-2 infection.

Acute pancreatitis is a potential manifestation of viral infections and has been reported in connection with mumps, coxsackievirus, hepatitis B, cytomegalovirus, varicella-zoster, herpes simplex and human immunodeficiency virus (HIV) 5, 6 . Some isolated cases of acute pancreatitis have been reported during SARS-CoV-2 infection 7-10 , although the real frequency in patients with COVID-19 is currently unknown. Indeed, there is no case series of acute pancreatitis in COVID patients allowing estimation of its frequency. In the present study, we aimed to investigate the incidence of acute pancreatitis in patients attending the emergency department (ED), before hospitalization and treatment with specific drugs for SARS-Cov-2 infection. The specific objectives were: 1) to determine the frequency of acute pancreatitis in patients with COVID-19; 2) to uncover the risk factors associated with the development of acute pancreatitis in patients with COVID-19; 3) to describe whether there are any distinctive clinical characteristics in these patients in comparison with acute pancreatitis observed in non-COVID patients; and 4) to investigate the outcomes of COVID patients presenting acute pancreatitis.

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The present study forms part of the Unusual Manifestations of Covid-19 (UMC-19) project, which was designed to investigate the potential relationship between COVID-19 and 10 different entities that could be influenced by SARS-Cov-2 infection itself: acute pancreatitis, meningoencephalitis, Guillain-Barre syndrome, (myo)pericarditis, spontaneous pneumothorax, acute coronary syndrome, deep venous thrombosis, pulmonary embolism, ictus and gastrointestinal bleeding. The main objectives of the UMC-19 project were common for all entities and consisted in the description of the incidence, risk factors, clinical characteristics, and outcomes for each particular entity, including COVID patients who did not develop these entities as well as non-COVID patients that presented these entities as comparators.

In Spain, the first case of SARS-Cov-2 infection was detected on January 31 st , 2020. The definition of the COVID period for the inclusion of cases in the present UMC-19 project study was set from March 1 st to April 30 th , 2020. The investigators forming the steering committee of the UMC-19 project initially contacted 152 Spanish EDs, which roughly constitute half of the 312 hospital EDs of the Spanish public health network. Of these, 81 considered participation and analyzed the protocol, and finally 62 (20% of Spanish EDs) consented to participate and duly sent all the data required ( Figure 1 ). Altogether these 62 hospitals provide health coverage to 15.5 million citizens (33% of the population of 46.9 million of Spain) and make up a balanced representation of the Spanish territory (representing 12 of the 17 Spanish autonomous communities), type of hospital (community, reference and hightechnology university hospitals were included) and involvement in the pandemic (with EDs attending from 1% to 47% of the ED census during the COVID outbreak period corresponding to COVID patients) 12 .

The investigation of acute pancreatitis in COVID patients, one of the entities included in the UMC-19 project, was labeled as the UMC-19 Study 6 (UMC-19-S 6 ) and consisted of a retrospective, case-control, ED-based, multicenter study that reviewed the medical reports of COVID patients who were diagnosed with acute pancreatitis during ED assessment and were managed in Spanish EDs before hospitalization.

The case group was formed by COVID patients with the diagnosis of acute pancreatitis made at ED presentation based on the presence of at least two of the following three manifestations: (1) acute abdominal pain and tenderness in the upper abdomen; (2) elevated pancreatic enzyme levels (amylase or lipase elevated > 3 times the

This article is protected by copyright. All rights reserved upper limit of normal) in the blood, urine, or ascitic fluid; and (3) abnormal imaging findings in the pancreas associated with acute pancreatitis 13,14 . Diagnostic adjudication was locally made by the principal investigator of each center, without external review. On the other hand, diagnosis of COVID-19 was accepted based on SARS-CoV-2 antigen detection in a nasopharyngeal swab by reverse transcriptase polymerase chain reaction (PCR) and/or based on a clinically compatible clinical picture (including at least malaise, fever and cough) or the presence of typical lung parenchymal infiltrates in chest X-rays (bilateral interstitial lung infiltrates and ground-glass infiltrates) in patients with some clinical symptoms attributable to COVID-19.

Controls of the UMC-19-S 6 We defined two different control groups. One group was formed by COVID patients (without acute pancreatitis) attending the ED during the same COVID outbreak period used for case inclusion (March 1 st to April 30 th , 2020). This group was constituted by selecting 3 COVID patients for every case detected by each center. Selection was randomly performed by the inclusion of the 3 COVID patients seen immediately before or after each case. Controls were not matched with cases for any variable at this point. This group, named control group A, was specifically designed to uncover the risk factors associated with the development of acute pancreatitis in COVID patients.

The second control group was made up of all non-COVID patients diagnosed with acute pancreatitis attending the ED during the same period as the cases (March 1 st to April 30 th , 2020), which was defined in the same terms as the cases. In order to avoid the possibility that some of these control cases could eventually have an inadvertent infection by SARS-Cov-2, and could have a different clinical profile from those usually attending the ED due to the population lockdown during the outbreak, we also included all patients with acute pancreatitis diagnosed in the ED Controls were not matched with cases for any variable at this point. This group was denominated control group B and was specifically designed to uncover the particular distinctive clinical characteristics of acute pancreatitis in COVID patients with respect to acute pancreatitis developed in the general population.

We collected 59 independent variables in cases and controls, which included 2 demographic data (age, sex), 14 comorbidities (hypertension, dyslipidemia, diabetes mellitus, coronary artery disease, chronic heart failure, obesityclinically estimated-, chronic liver disease, chronic obstructive pulmonary disease, asthma, active smoker, cerebrovascular disease, chronic kidney disease -creatinine> 2 mg/dL-, dementia, active cancer), 12 symptoms (time elapsed from symptom onset to ED attendance, fever, rhinorrhea, cough, expectoration, dyspnea, chest pain, abdominal pain, vomiting, diarrhea, anosmia, dysgeusia), 5 vitals at ED arrival (temperature, systolic blood pressure, heart rate, respiratory rate, room air pulsioxymetry), 22 blood parameters (amylase, lipase, aspartate

This article is protected by copyright. All rights reserved aminotransferase -AST-, alanine aminotransferase -ALT-, bilirubin, alkaline phosphatase, lactate dehydrogenase -LDH-, C-reactive protein -CRP-, procalcitonin, creatinine, sodium, potassium, calcium, magnesium, hemoglobin, leucocytes, lymphocytes, platelets, activated partial thromboplastin time, prothrombin time, fibrinogen, D-dimer) and 4 radiological findings in chest X-rays (cardiomegaly, pleural effusion, interstitial lung infiltrates and ground-glass opacities).

In patients with acute pancreatitis (cases and control group B), we also recorded specific risk factors for acute pancreatitis (chronic alcoholism, and previous antecedent of alcohol abuse and episodes of acute pancreatitis), severity of the current episode of acute pancreatitis at ED arrival assessed by two different scores, one specifically developed for acute pancreatitis (BISAP score 15 ) and one developed of critical patients with sepsis (SOFA score 16 ), the type of imaging (ultroasonography and/or computerized tomography) and the main results and endoscopic interventions recorded or performed during ED patient management, and the final etiological diagnosis of the current episode.

We defined 4 different outcomes for cases and controls which consisted in: 1) the need for hospitalization; 2) the need for admission to intensive care; 3) prolonged hospitalization (defined as a length of stay > 7 days, which is the median length of stay of hospitalized patients in Spain); and 4) in-hospital all-cause mortality.

Discrete variables were expressed as absolute values and percentages, and continuous variables as median and interquartile range (IQR). Frequencies were expressed per thousand (‰) cases or controls, with 95% confidence interval (CI). Differences between the case and the control groups were assessed by the chi-square test (or Fisher exact test if needed) for qualitative variables and by the Mann-Whitney non-parametric test for quantitative variables. The magnitude of associations was expressed as unadjusted odds ratio (OR) with 95%CI. Continuous variables were dichotomized using clinically meaningful cut-offs or around the median of the distribution. As the number of patients with acute pancreatitis we expected to identify was not large, we did not plan to go further in the investigation of the significant relationships identified in the unadjusted analysis using adjusted models. As an exception, outcomes were adjusted for age and sex. 

This article is protected by copyright. All rights reserved with unequally (p<0.05) distributed between groups. For case and control B groups matching, BISAP score was added to the model. A relative difference of less than 10% in propensity score was required for matching.

In all comparisons, statistical significance was accepted if the p value was < 0.05 or if the 95%CI of the risk estimations excluded the value 1. The analyses were performed with the SPSS (v.24) statistical software package (IBM, Armonk, New York, USA).

The UMC-19 project was approved by the Ethics Committee of the Hospital Clínic of Barcelona (Spain), with the reference number HCB/2020/0534, and acted as the central ethical committee. Under the exceptional circumstances generated by the COVID-19 pandemic, the urgent need to obtain feasible data related to this new disease, and the non-interventional and retrospective nature of the project, the requirement of obtaining written patient consent to be included in the study was waived. All patients were codified by investigators of the participating centers before entering their data into the general database, thereby ensuring patient anonymity to investigators analyzing the database. The UMC-19-S 6 was carried out in strict compliance with the principles of the Declaration of Helsinki. The authors designed the study, gathered and analyzed the data, vouched for the data and analysis, wrote the paper, and decided to publish.

This article is protected by copyright. All rights reserved The mean age of COVID patients with acute pancreatitis (cases) was 68 years; 72% were males, and the most frequent comorbidities were hypertension (65%), dyslipidemia (50%), diabetes mellitus (28%), and active cancer and obesity (24% each). The most frequent symptomatology was abdominal pain (80%), vomiting (48%), fever (43%) and dyspnea (29%), and the median time from symptom onset to ED consultation (whichever was first) was 3 days. The remaining clinical characteristics, as well as the vitals at ED arrival, laboratory findings and chest X-ray alterations are presented in Table 1 .

In patients with acute pancreatitis, chronic alcoholism was less frequently present in cases than in control group B patients, and severity of the current episode of pancreatitis assessed when patient arrived to ED was higher in cases, either assessed by BISAP or by SOFA score ( Table 2) . Imaging studies to assess acute pancreatitis were ordered in the ED in 74% of COVID patients and in 85% of non-COVID patients (p=0.10; Table 2 ). Ultrasonography and dual imaging studies (by ultrasonography and computerized tomography) were more frequently performed in non-COVID patients. The main findings did not differ between the two groups, and a similar percentage of patients were treated with endoscopic retrograde cholangiopancreatography and sphincterotomy during ED stay (5.6% and 6.8%, respectively). Final etiologic diagnosis of the current episode of pancreatitis did not differ among COVID and non-COVID patients: about 50% were biliary, about 10% alcoholic and in about 25% the origin was unknown or unreported ( Table 2) .

When cases were compared with controls, some statistically significant differences were found ( Table 1) , and the magnitudes of these associations are shown in Table 3 . In COVID patients, complaints of abdominal pain and vomiting and a rise in blood amylase levels were the most indicative of the presence of a concomitant acute pancreatitis, all with ORs 10-fold greater with respect to COVID patients without acute pancreatitis (ORs of 59, 16 and 32, respectively). Similarly, chest X-ray findings such as lung interstitial infiltrates, parenchymal glass-ground opacities and pleural effusion were extremely increased (ORs of 24, 19 and 11, respectively). As expected, abnormalities in hepatic and biliary blood tests were also more frequently present among cases than in patients in control group B. Remarkably, some inflammatory markers (CRP, procalcitonine, platelets, D-dimer) as well as pleural

This article is protected by copyright. All rights reserved effusion (OR of 5) were also more frequently seen in cases than in control A patients. Conversely, cases less frequently presented cough and dyspnea. Finally, acute pancreatitis was also found to be associated with male sex and hypertension, dyslipidemia, diabetes mellitus and active cancer as comorbidities.

On the other hand, compared to non-COVID patients with acute pancreatitis (control group B patients), the most distinctive findings in COVID patients with acute pancreatitis were the presence of the symptoms of COVID infection: fever, cough, expectoration, dyspnea, dysgeusia and anosmia, with ORs over 10-fold higher (ORs of 14, 32, 13, 21, 22 and 22, respectively, Table 3 ). They were also more frequently male and, remarkably, the complaint of abdominal pain was not as frequent in COVID patients with acute pancreatitis as in non-COVID patients (OR of 0.12) and neither were blood amylase concentrations over 1000 IU/L (ORs of 0.34).

COVID patients with acute pancreatitis were hospitalized in 96% of cases; 9% were admitted to the ICU at some point during hospital stay, 53% experienced prolonged hospitalization (>7 days) and 17% died during hospital stay.

With respect to COVID patients without acute pancreatitis, and after adjustment for age and sex, the only outcome 

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We found that around 0.75‰ of COVID patients coming to the ED were concomitantly diagnosed with acute pancreatitis. This frequency, found during a 2-month period of the COVID outbreak in Spain, should be considered as low compared with both the frequency observed in non-COVID patients coming to the ED found in the present study (around 1.5‰) and the annual incidence reported in the general population in the United States (up to 0.35‰) 17 .

Remarkably, our study did not include cases of acute pancreatitis appearing after the initiation of antibiotics or antiviral drugs, a circumstance that could increase the risk due to drug-related adverse events. Therefore, the decreased OR of 0.44 for COVID patients found in the UMC-19-S 6 suggests that pancreas may not be a target for direct SARS-CoV-2 tropism or indirect viral-induced damage due to inflammatory or for immunological response 10 . In another two cases of acute pancreatitis reported separately, the temporal relationship with COVID-19 and the lack of other etiologies suggest coronavirus-induced pancreatitis 8, 9 .

The presence of angiotensin-converting enzyme-2 (ACE-2) receptors in pancreatic islet cells has been suggested as a potential link, since part of the pathogenesis of COVID-19 is thought to be mediated by such receptors 9, 19 . According to this hypothesis, acute pancreatitis in COVID-19 could be directly due to the cytopathic effect of local SARS-CoV-2 replication or indirectly due to harmful immune response induced by the virus. Nevertheless, if this mechanism really exists, one would expect the frequency of acute pancreatitis to be increased in COVID patients compared to the general population, and in the present study this increased incidence was not found.

COVID patients developing acute pancreatitis differed from the remaining COVID patients in that the differences in their data were more related to acute pancreatitis than to COVID infection. Abdominal pain and vomiting are two signatures of acute pancreatitis, but these manifestations can be present in up to 17% of COVID patients 16 . This could lead to the misdiagnosis of acute pancreatitis in patients with a mild rise in enzyme levels and digestive symptoms derived from the COVID infection itself. Our patients fulfilled at least two out of the three criteria internationally accepted for the diagnosis of acute pancreatitis 13,14 . Remarkably, our COVID patients with acute pancreatitis had a higher increase in inflammatory markers (CRP, procalcitonin, platelets, D-dimer) than those without acute pancreatitis. The significance of these findings is unknown and merits further studies to elucidate if they imply any connection between inflammatory activity in COVID patients and pancreas involvement. The

This article is protected by copyright. All rights reserved presence of pleural effusion in chest X-ray, barely seen in COVID-19, could be an additional red flag when abdominal pain is present in these patients.

The clinical characteristics of acute pancreatitis in COVID patients differed from those of acute pancreatitis in non-COVID patients in relation to many baseline, clinical and analytical data, with most of these characteristics depending on the presence of SAR-CoV-2 infection. Of note, increases in amylase and lipase levels were more moderate and abdominal pain was less frequent in COVID patients with acute pancreatitis which may make it more difficult to diagnose acute pancreatitis in these patients than in the general population. Thus, a high degree of suspicion is recommended in EDs. On the other hand, although we did not explore the potential effect of patient race, results from the Inamdar et al. study suggest that Black and Hispanic races are more represented in acute pancreatitis developed in COVID patients than in acute pancreatitis developed in non-COVID patients 18 .

COVID patients with acute pancreatitis showed similar outcomes to those of the rest of COVID patients, with the exception that the former more frequently need hospitalization. However, in-hospital mortality did not significantly differ. On the other hand, there was a clear increment of mortality in these patients with respect to acute pancreatitis in non-COVID patients. Probably, part of this increment in in-hospital mortality is in relation to the severity of the viral infection because, as a general rule, mortality rates between 10% and 20% have been reported in hospitalized COVID patients [20] [21] [22] . Nonetheless, we have identified that severity of the current episode of acute pancreatitis, assessed by two different scores when patient arrived at ED, seems to be higher in COVID patients, and therefore, acute pancreatitis itself could be contributing, in some extend, in the worse prognosis observed in acute pancreatitis developed by COVID patients respect to non-COVID patients.

This study has several limitations. First, as abdominal pain and vomiting can be seen as constitutive symptoms of COVID-19, some cases of mild, paucisymptomatic acute pancreatitis could have remained undiagnosed if pancreatic enzyme determination was not ordered. Second, we did not adjust the incidence of acute pancreatitis in COVID for all relevant patient-related or disease-related factors influencing the relative frequency of acute pancreatitis presentation and outcomes, and this could somewhat alter the estimations presented in the current study. Third, in around one quarter of COVID-19 patients the diagnosis was based exclusively on clinical and/or radiological findings, with no microbiological confirmation. This was due to shortage of diagnostic tests during the first pandemic surge in Spain 23 . We have tried to cover this gap by repeating the outcome analysis using only cases and control A patients with SARS-CoV-2 infection confirmed by RT-PCR, and such analysis (the sensitivity analysis A) rendered the same significant associations as the main analysis. Fourth, as a retrospective study, although the case record form was standardized, there was no monitoring of data collection methods, and diagnosis and outcome adjudication were done locally. Fifth, the UMC-19-S 6 was designed to randomly select patients for control groups A and B no planned matching for any patient characteristic. Therefore, as we did not balance any potential confounder in the study design, our study design produced groups that diverged in many baseline characteristics.

This article is protected by copyright. All rights reserved Although the sensitivity analysis B tried to overcome this limitation and obtained similar estimations as those found in the main analysis, we cannot rule out that a different design could modify, in some extend, our findings.

Finally, in depth analysis of the severity of acute pancreatitis in patients with COVID with was not performed and we were not able to identify the real role of acute pancreatitis in the increment of in-hospital mortality observed when it is developed by COVID patients respect to non-COVID patients.

Despite these limitations, we conclude that the incidence of acute pancreatitis in COVID patients attending the ED is low and less than expected in the general population (non-COVID patients) attending the ED. A high degree of suspicion of acute pancreatitis must be considered in COVID patients, as they can present abdominal pain and vomiting as a mere consequence of viral infection while, on the other hand, these symptoms of pancreatic inflammation may not be as evident as in non-COVID patients. At the time of patient arrival to ED, severity of acute pancreatitis seems to be higher in COVID than in non-COVID patients, although the role of this finding in the increased mortality found in the former group respect to the latter group is not determined by the present study. On the other hand, the development of acute pancreatitis in COVID patients is not associated with a higher mortality. 

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This article is protected by copyright. All rights reserved 

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Room air pulsioxymetry (%)

Leucocyte count

Lymphocyte count (cells/μL)

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