COVID-19 Associated Pancreatitis: A Review of 66 Cases

doi:10.21203/rs.3.rs-154488/v1

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COVID-19 Associated Pancreatitis: A Review of 66 Cases

https://doi.org/10.21203/rs.3.rs-154488/v1

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Background: Severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2) has shown itself with different clinical manifestations. Besides respiratory distress, cough, and fever, which were the most common symptoms, pancreatitis has been reported as a rare presentation of this disease, but the knowledge on this association and its pathogenesis is sparse.

Methods: Four databases, including Pub Med, Scopus, Web of Science, and Google Scholar, were searched for the association of pancreatitis and SARS-CoV- 2 infection, and 29 relevant articles were extracted and reviewed.

Results: We reviewed 29 studies provided 66 cases developed acute pancreatitis while they were infected with SARS-CoV-2. The mean age of patients was 49.94 ± 16.96. The female to male ratio was 1.06 (33 to 31). In 44% of cases, acute pancreatitis developed as the primary presentation of Coronavirus Disease 2019 (COVID-19) and 9% of reported cases, expired.

Conclusions: During this pandemic, SARS-CoV-2 should be considered in the differential diagnosis of the patients presenting with acute pancreatitis. Although pancreatitis will respond to standard care, these patients need isolation and observation for later development of respiratory symptoms.

Gastroenterology & Hepatology

Acute pancreatitis

COVID-19

Coronavirus disease 2019 (COVID-19) emerged in Wuhan city in December 2019, and rapidly involved almost all countries and territories in the world (1, 2). The most common manifestations of this disease include fever, cough, dyspnea, sore throat, headache, and myalgia (3). Although it mainly involves the respiratory system, many studies have reported various extrapulmonary manifestations such as acute cardiac injury, heart failure, cardiac arrhythmia, acute ischemic stroke, cerebral venous thrombosis, encephalitis, and gastrointestinal symptoms (4-8). Digestive manifestations such as anorexia, nausea, vomiting, abdominal pain, diarrhea can range from mild to severe in their presentation. There are reports of more severe complications which may need urgent interventions including bowel ischemia and hepatic necrosis (9, 10). Acute pancreatitis is a relatively rare presentation of severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2) infection (6). Pancreatitis has been reported with several different types of viruses through diverse mechanisms (11). It seems that the coronavirus can also affect the pancreas and cause pancreatic injury (12). The mechanism of pancreatitis in the course of COVID-19 is not entirely known.(13)

In recent months, publications have reported acute pancreatitis as a COVID-19 manifestation. This study gives a detailed review of relevant articles and summarizes their findings to clarify acute pancreatitis features induced by COVID-19.

This literature review was performed through a comprehensive search in three databases, including Pub Med, Scopus, and Web of Science. English articles about the association of SARS-CoV-2 and pancreatitis, published before 30^th of October 2020, were included in this review. We also searched Google Scholar or the grey literature and examined the first 100 results. The search strategy employed for each database is shown in Table1.

All of the citations were imported to Endnote X9 software (Clarivate Analytics, USA), and all duplicates were excluded. Then we carried out the first screening, and irrelevant articles were excluded according to their titles and abstracts. In the next step, full-text screening was performed to detect the eligible studies. Finally, an Excel (Microsoft, Redmond, WA, USA) spreadsheet was used to extract the key findings of the studies. All steps were done by two authors separately. In case of disagreements, a third person was consulted.

We identified 73, 117, 51, 17 records in Pub Med, Scopus, Web of Science, and Google Scholar, respectively. After removing duplicates and screening, we found 29 publications (Figure 1), including 27 case reports and 2 cohort studies. Taken together, 66 patients with COVID-19 associated pancreatitis were reported. Table 2 represents the key characteristics of the cases. In terms of geographical location, nine studies (33.3 %) were from Asia, eight studies (29.6%) were from Europe, seven studies (25.9%) were from North America, two studies (7.4%) were from South America, and one study (3.7%) was from Africa. In total, the female to male ratio was 1.06 (33 to 31); gender was not mentioned in two cases (14, 15). The mean age of patients (n=66) was 49.94 ± 16.96. Reviewed records indicated that in 44% of patients, acute pancreatitis presented as the initial manifestation of COVID-19. No significant past medical or surgical history was reported for 35% of cases. Among underlying disease reported in 65% of patients, hypertension was the most common. In a cohort study conducted by Inamdar et al., thirty-two COVID-19 positive patients with pancreatitis were reported. Idiopathic pancreatitis accounts for the majority of these cases. Gallstone, alcohol, and drugs were responsible for 16%, 6%, and 3% of pancreatitis in these patients, respectively (16). The mortality rate was 9% among all patients reported in the studies.

Pathogenicity:

Studies have suggested a causal relationship between SARS-CoV-2 infection and acute pancreatitis (17, 18). Pancreatic injury may emerge directly due to viral replications, or it may be due to inflammatory processes and immune dysregulation caused by COVID-19 (12, 17-20).

As mentioned earlier, SARS-CoV-2 pathogenicity for acute pancreatitis is not clear yet (13). Investigations have reported several mechanisms that explain pancreatic involvement during this disease. One of these mechanisms is based on Angiotensin-converting enzyme 2 (ACE2) receptor expression on the pancreatic cells (21). The pathogenicity of SARS-CoV-2 is through binding to the ACE2 receptor on alveolar cells in the lung (22). ACE2 receptor is also present on other organs such as the pancreas (23). According to this fact, the pancreatic tropism of the COVID-19 virus could be justified.

Timing ofpancreatitis presentation:

The onset of pancreatitis presentations varied among studied cases. In some cases, acute pancreatitis was presented as the initial manifestation of COVID-19. In other ones, pancreatic injury developed from days to weeks after the emergence of respiratory symptoms. Evidently, the time of emerging pancreatitis presentations has not the same pattern in different patients.

Diagnosis:

COVID-19 can involve the gastrointestinal tract and may lead to pancreatic enzyme elevation (11, 24). Although pancreatic enzyme elevation is one of the diagnostic criteria for acute pancreatitis, rising pancreatic enzymes is possible in infected patients in the absence of any pancreatitis presentations (25, 26). Therefore, in addition to the enzyme elevation, at least one of the following criteria should be considered in the diagnosis of acute pancreatitis in patients with COVID-19: characteristic acute pain in epigastric or right upper quadrant and abdominal imaging in favor of acute pancreatitis (26).

In the reviewed studies, pancreatic enzyme levels were detected from normal (27) to above 20 to 30 times more than the normal range (19, 28). In addition to that, the C-Reactive Protein (CRP) level also was up to 20-times elevated (17). The most common pancreatitis presentation was sudden onset epigastric pain, which was reported mild to severe in different individuals. Other manifestations such as anorexia, nausea, vomiting, diarrhea, fever varied among patients. In one study, no abdominal symptoms were reported, and investigations to confirm acute Pancreatitis were done just due to persistent fever (14).

Acute pancreatitis was confirmed through abdominal imaging, especially Computed Tomography (CT) scans in the majority of the studies. The most common imaging findings in publications were peripancreatic fat stranding and fluid collection. Necrotizing pancreatitis, pancreatic fluid collection, and pancreatic pseudocyst were also reported (29-32). Although it is not a common procedure, in one study pseudocyst sample was tested positive for SARS-CoV-2 (33). Ultrasonography was also a standard modality to exclude cholelithiasis as a common reason for pancreatitis.

Treatment and outcomes:

After confirming the diagnosis of the COVID-19, nearly all cases of COVID-19 associated pancreatitis were treated by two main strategies: (1) Treatment of COVID-19, which is supportive care in most cases or can include antiviral and anti-inflammatory drugs based on patients’ conditions and each country guideline. (2) Treating pancreatitis as routine (fluid resuscitation, analgesics, and antibiotics if indicated). Considering these treatments, the symptoms of most of the cases were resolved.

Although we reviewed databases thoroughly, the infancy of the publications could impact our study.

Based on this review, we strongly recommend that during this pandemic, it should be borne in mind that every patient with pancreatitis presentations can be a possible case of COVID-19. Although pancreatitis will respond to standard care, these patients need isolation and observation for later development of respiratory symptoms.

COVID-19: Coronavirus Disease 2019, SARS-CoV-2: Severe Acute Respiratory Syndrome Coronavirus 2, US: Ultrasonography, CT scan: Computed Tomography scan, ACE2: Angiotensin-converting enzyme 2

Ethics approval and consent to participate

Not applicable

Consent for publication

Not applicable

Availability of data and materials

Not applicable

Competing interests

The authors declare that they have no competing interests.

Funding

Not applicable

Authors’ contribution

ZR: study design, data collection, manuscript preparation. AA: data collection, analysis, manuscript preparation. AF: Data collection, manuscript preparation, KBL: conceptualized the study, manuscript preparation. All authors read and approved the final manuscript.

Acknowledgements

None

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Table 1. Search strategies

Database	Search strategy
Pub med	((coronavirus[MeSH Terms] or coronavirus[Title/Abstract] OR COVID-19[Title/Abstract] OR SARS-Cov-2[Title/Abstract] OR 2019-nCoV[Title/Abstract] OR 2019 novel coronavirus[Title/Abstract] OR coronavirus disease[Title/Abstract])) AND (pancreatitis[Title/Abstract] OR pancreatitis[MeSH Terms] OR "acute pancreatitis"[Title/Abstract] )
Scopus	(INDEXTERMS (“coronavirus”) OR TITLE-ABS-KEY ("coronavirus" or "COVID-19" OR "SARS-Cov-2" OR "2019-nCoV" or "2019 novel coronavirus" or "coronavirus disease*")) AND (INDEXTERMS("pancreatitis") OR TITLE-ABS-KEY ("pancreatitis" OR "acute pancreatitis"))
Web of science	(TS= ("coronavirus" or "COVID-19" OR "SARS-Cov-2" OR "2019-nCoV" or "2019 novel coronavirus" or "coronavirus disease")) AND (TS=(“pancreatitis” OR “acute pancreatitis”))

Table 2. Key findings of the studies

Author(s)

Type of study

Age and sex

Past medical and surgical history

Pancreatitis presentations (CC, P/E)

Enzyme elevation

CRP elevation

Abdominal imaging

The onset of pancreatitis symptoms

Outcome

Alloway et al.⁽³²⁾

Case Report

7-year-old girl

Abdominal pain, anorexia, and then two weeks later, abdominal pain, fever, non-bloody, non-bilious vomiting, left lower quadrant, and epigastric pain.

Distension, tenderness to palpation in the left upper and left lower quadrant, and epigastric region, fullness noted in the left upper quadrant

Abdominal Ultrasound (US) and Computed Tomography (CT) scan were suggestive of necrotizing Pancreatitis

Presented as Pancreatitis

For the first time, the patient was discharged with normal lipase

In the second admission, she improved significantly over two days and was discharged with a trending down lipase

Aloysius et al.⁽³⁴⁾

Case report

36-year-old woman

Chronic anxiety, obesity

Nausea, vomiting, diarrhea,

severe stabbing epigastric pain radiating to back, severe epigastric tenderness

CT scan: unremarkable pancreas

Six days after respiratory symptoms

Improved with treatment

Alves et al.⁽³⁵⁾

Case report

56-year old woman

HTN, minimal alcohol consumption

Epigastric pain on admission but no relevant abdominal symptoms during hospitalization

Chest CT: tail parenchymal enlargement and surrounding retroperitoneal fat stranding of the pancreas.

MRCP: acute Pancreatitis, diffusely enlarged pancreas

The endoscopic US showed no microlithiasis.

Amylase and lipase elevated during hospitalization. The timing was not mentioned

The patient was discharged after 35 days without any long-term sequelae.

Bokhari and Mahmood.⁽²⁹⁾

Case report

32-year-old man

Severe mid epigastric pain radiating to back, intermittent fever, chills, non-biliary vomiting

US: unremarkable

CT scan: a bulky and

swollen pancreas with significant peripancreatic inflammatory changes and fluid collection along the gastrosplenic ligament.

Fourteen days after respiratory symptoms

Discharged after treatment

Brikman et al.⁽³⁶⁾

Case report

61-year-old

man

Sudden diffuse abdominal pain with anorexia. No fever, no vomiting, or diarrhea.

the abdomen was soft, with mild diffuse tenderness

CT scan: focal parenchymal enhancement of the pancreas head with inflammatory changes in peripancreatic fat suggestive of acute Pancreatitis.

14^th day of admission

19 days after developing a fever, dyspnea, and cough

Improved with treatment

Charra et al.⁽¹⁴⁾

Case report

67-year-old

(gender was not mentioned)

Cholecystectomy, DM type 2, obesity

Without any abdominal symptoms on admission (the patient intubated on the 5th day of admission); investigations were due to persistent fever

CT scan: stage C pancreatitis according to the Balthazar classification

US: unremarkable

13^th day of admission (persistent fever)

expired

Cheung et al.⁽³⁷⁾

Case report

38-year-old man

Fever, severe epigastric pain, nausea, and vomiting. One week after discharge, the patient returned to the ED complaining of recurrent sharp epigastric pain with radiation to the back, nausea and vomiting. On the second time, a physical examination revealed moderate tenderness to light palpation in the epigastric region

US: unremarkable

CT scan: acute Pancreatitis

MRCP and MRI of the abdomen showed evidence of acute Pancreatitis and normal gallbladder.

One week after a positive test for COVID-19 (symptoms were not mentioned), gastrointestinal symptoms started.

Discharged after treatment

Dietrich et al.⁽³⁸⁾

Case report

72-year-old man

HTN, Overweight

BMI 29.4 kg/m2

Nausea and mild abdominal pain.

The abdomen was bloated and tender, with diffuse pain

US: cholecystolithiasis, but

no signs of obstructive cholestasis. The pancreas was barely visible, but the parenchyma seemed to be inhomogeneous.

Endo US showed inhomogeneous pancreatic tissue without any

focal mass. A lean bile duct with no signs of an intraluminal stone or papilla passage of a stone was seen.

Abdominal CT was normal.

Presented as Pancreatitis

The patient was intubated, developed pulmonary embolism bilaterally, small cerebral infarction, and ventilator-associated pneumonia.

The patient was weaned on day 64 with a tracheostomy.

Fernandes et al.⁽³⁰⁾

Case report

36-year-old woman

Intense upper abdominal pain, tachycardia

CT scan: signs of acute interstitial edematous Pancreatitis with an acute peripancreatic fluid collection.

US: unremarkable

Two days after onset of fever, cough, and dyspnea

Discharged after treatment

Hadi et al.⁽¹⁷⁾

Case report

47-year-old woman

Fever, headache, and neck pain for one week and anorexia, sore throat, and dyspnea for a couple of days (does not have a specific abdominal pain)

US: acute Pancreatitis

with a diffusely voluminous pancreas without focal lesions or gallstones

In the course of admission

ICU care

Hadi et al.⁽¹⁷⁾

Case report

68-year-old woman

HTN, hypothyroidism, osteoporosis

Epigastric pain, fever, vomiting, diarrhea, fatigue, polydipsia abdominal pain and slight abdominal distension

physical examination showed direct epigastric and periumbilical

tenderness

6^th day of admission

ICU care

Inamdar et al.⁽¹⁶⁾

retrospective observational cohort study

18 women

14 men

Mean age :53.44 ± 16.60

Ten had DM.

Fifteen had HTN.

Two had congestive heart failure.

All of the patients met all three of the following criteria: 1) lipase greater than three times the upper limit of normal, 2) cross-sectional imaging (CT or MRI) indicative of Pancreatitis, and 3) characteristic upper abdominal pain at admission

Four patients developed pancreatic necrosis.

Four patients expired.

The average hospital stay was 21.22 days

Karimzadeh et al.⁽³⁹⁾

Case report

65-year-old woman

Asthma, HTN

Upper abdominal pain, constant nausea, chills, and myalgia for five days. the dry mucous membrane, pallor, and mild tenderness on the right upper quadrant of the abdomen

CT scan: unremarkable

Two days after chills and myalgia

Discharged after treatment

Katarina et al.⁽⁴⁰⁾

Case report

49-year-old woman

Severe epigastric pain radiating to back, nausea and one episode of vomiting containing food particles, epigastric tenderness

CT scan: edematous pancreas with diffuse enlargement and ill-defined border

US: unremarkable

2^nd day of

Admission (5 days after respiratory symptoms)

Discharged after treatment

Kumaran et al.⁽³¹⁾

Case report

67-year-old woman

Small bowel resection and anastomosis due to

superior mesenteric artery stenosis, HTN

Epigastric pain, diarrhea, and vomiting

CT scan: extensive peripancreatic fluid collection

CT angiogram:

interval progression of previously seen peripancreatic inflammatory changes and non-enhancement of most

of the head and proximal body (necrotizing Pancreatitis

US: unremarkable

One day before admission

Continued treatment as a stable inpatient

Kurihara et al.⁽¹⁵⁾

Case report

55-year-old patient

Abnormalities of pancreatic enzymes were found in a routine blood test. Due to intubation, the patient was not able to express symptoms associated with Pancreatitis

US: unremarkable

CT scan: suggestive of acute Pancreatitis.

14 days after onset of symptoms (fever, cough)

6^th day of admission

Discharged after treatment

Lakshmanan et al.⁽⁴¹⁾

Case report

68-year-old

man

DM, HTN, chronic kidney disease stage IV

Persistent nausea, vomiting, and anorexia, but no abdominal pain

CT scan: peripancreatic fat stranding, especially around the tail, with mild duodenal wall thickening and adjacent fat stranding

Few days after admission

Discharged after treatment

Mazrouei et al^.⁽⁴²⁾

Case report

24-year-old man

Non-radiating sharp, epigastric pain for the last two days. Nausea and vomiting,

soft abdomen with epigastric discomfort on palpation

CT scan: mild edema of the distal pancreas with a non-encapsulated peripancreatic low-density fluid around pancreatic tail extending to the splenorenal recess.

Two days before admission

Discharged after treatment

Meireles et al.⁽¹¹⁾

Case report

36-year-old

woman

post-HELLP syndrome chronic kidney disease stage V, arterial HTN

Nausea, vomiting, and a belt-like epigastric pain without other specific findings

CT angiogram: no ischemic changes.

US: unremarkable

11 day after dry cough, breathlessness, and fever

(on the 7^th day of admission)

The patient recovered through supportive care only

Meyers et al.⁽²⁸⁾

Letters to the Editor

67-year-old

Man

HTN, cholecystectomy, alcohol consumption

Sudden onset epigastric abdominal discomfort, tachycardia, fever, and

epigastric tenderness

CT scan: interstitial edematous Pancreatitis with moderate peripancreatic stranding and edema

Three days before developing fever and dyspnea

Not mentioned

Miao et al.⁽⁴³⁾

Letters to the Editor

26-year-old

woman

Severe vomiting, epigastric pain, and fever

CT scan: enlarged pancreas gland without any structural abnormality. Gastrointestinal endoscopy revealed unspecific pan gastritis.

At least 7days before confirming COVID-19

Discharged after treatment

Patnaik et al.⁽¹⁹⁾

Case report

29-year-old

man

Acute diffused abdominal

pain radiating to the back and progressively worsened, low-grade fever, tachypnea, abdominal tenderness, which was maximal in the umbilical region.

US: bulky pancreas with irregular edematous margins, some peripancreatic fluid.

CT scan confirmed these findings.

Two days after developing dyspnea

Discharged after treatment

Purayil et al.⁽⁴⁴⁾

Case report

58-year-old

man

Fever and vomiting for three days, epigastric pain, mild epigastric tenderness

US: unremarkable

Discharged after treatment

Rabice et al.⁽⁴⁵⁾

Case report

36-year-old pregnant woman

Asthma, cholecystectomy DM type 1, maternal obesity, pre-eclampsia in previous pregnancies,

Fever, nausea, vomiting,

, epigastric pain and epigastric tenderness

US: unremarkable

Six days after respiratory symptoms

Discharged after treatment

Schepis et al.⁽³³⁾

Case report

67-years-old woman

recent hospitalization for interstitial edematous acute Pancreatitis of unknown origin.

Upper quadrant abdominal pain, fever, and vomiting. Abdominal distention, slight tenderness, and pain in epigastric and mesogastric regions. The pancreatic pseudocyst sample resulted positive for all three target genes of SARS-CoV2 researched

CT scan: the presence of a large pancreatic pseudocyst

(16 cm _ 8 cm x 12 cm) causing a partial stomach outlet obstruction.

Presented as Pancreatitis

an endoscopic

ultrasound-guided trans gastric drainage of the pseudocyst using AXIOS™ Stent and Electrocautery Enhanced Delivery System was successfully performed.

Shinohara et al.⁽⁴⁶⁾

Letters to the Editor

58-year-old

man

HTN

Recurrent fever, intermittent abdominal pain

CT scan: enlargement of the pancreas with peripancreatic fat.

22^nd day after hospitalization

Discharged after treatment

Stevens et al.⁽⁴⁷⁾

Case report

10-year-old girl

Asthma, obesity

Diffuse abdominal pain radiating to back and right lower quadrant pain fever, non-bloody, non-bilious vomiting, watery diarrhea, and anorexia

CT scan: inflammatory change within the peripancreatic fat; pancreas appeared prominent

Five days before admission

Multisystem inflammatory

syndrome in children presented as acute Pancreatitis, treated with IVIG and discharged after stabilization

Szatmary et al.⁽⁴⁸⁾

Retrospective cohort

Five men

mean age:42

One of the patients had asthma

All patients had typical pain for Pancreatitis

CECT in all patients showed transient moderate to severe hepatic steatosis and mild pancreatic edema

US: unremarkable

On admission

Discharged after treatment

Wang, K et al.⁽²⁷⁾

Case report

42-year-old

man

Nausea, persistent upper abdominal pain with radiation to the back

CT scan: enlargement of the pancreas and peripancreatic fluid accumulation, without biliary dilatation or microlithiasis.

Four days before chest discomfort and shortness of breath.

Despite the use of different vasoactive drugs and fluid resuscitation, the patient expired on the 10^th day of admission.

Wang, K et al.⁽²⁷⁾

Case report

35-year-old

man

Upper abdominal pain with radiation to the back, nausea, and vomiting

CT scan: showed pancreatic swelling, peripancreatic fluid accumulation, and prerenal fascial thickening

Five days before confirming COVID-19.

Discharged after treatment

Zhao et al.⁽⁴⁹⁾

Case report

62-year-old

woman

HTN, DM type 1

Overweight

BMI: 26.67 kg/m2

Abdominal distension and epigastric pain after breakfast

Mild abdominal tenderness without rebound tenderness

CT scan: exudative changes in pancreatic uncinate process and infiltration along the perivascular.

15 days after fever, cough, and fatigue

14^th day of admission

Improved with treatment

N: not mentioned, US: Ultrasonography, CT: Computed Tomography

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COVID-19 Associated Pancreatitis: A Review of 66 Cases

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