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Acute Mesenteric Ischemia as a Complication of COVID-19 Infection: A Case Report and Review of the Literature

Ghazal Ghasempour Dabaghi1, Mehrdad Rabiee Rad1, Mohammad Eslamian2,* and Maryam Goharian3

  1. School of medicine, Isfahan University of Medical Science, Isfahan, Iran
  2. Department of Surgery, School of Medicine, Isfahan University of Medical Sciences, Isfahan, Iran
  3. Department of Obstetrics and gynecology, School of Medicine, Isfahan University of Medical Sciences, Isfahan, Iran

* Corresponding author: Mohammad Eslamian, Department of Surgery, Alzahra Educational Medical Hospital, Isfahan university of Medical Sciences, Isfahan, Iran. Tel: +983131091885; Email: mr.esl67@gmail.com

 

Received 2021 October 31; Revised 2022 March 29; Accepted 2022 March 31

 

Abstract

Background: Coronavirus disease 2019 (COVID-19) is a major health problem worldwide. Vascular thrombosis is increasingly observed in COVID-19 patients. This complication seems to be due to coagulopathy and endothelial damage. In this paper, we report a COVID-19 patient with superior mesenteric artery thrombosis and review of 27 COVID-19 cases with acute mesenteric ischemia (AMI).

Case presentation: A 59-years old man with confirmed COVID-19 readmitted to the hospital due to abdominal pain and diarrhea two days after discharge from the emergency department. He was diagnosed with acute mesenteric ischemia by abdominal CT scan with contrast. The patient underwent emergency laparotomy and the ischemic gangrenous bowel was resected. Unfortunately, the patient succumbed one month after the operation.

Conclusion: AMI is a life-threatening thrombotic event rarely seen in COVID-19 patients, so it is vital to diagnose it. Anticoagulant and anti-inflammatory prophylactic therapies might be useful in preventing AMI, especially in the patients with thrombosis risk factor. So, it is crucial to reduce its incidence in COVID-19 patients.

 

Keywords: COVID-19, Hypercoagulopathy, Mesenteric ischemia, SARS virus, Thrombosis


1. Background

Coronavirus disease 2019 (COVID-19) caused by SARS-CoV-2 is a respiratory infection observed in Wuhan, China, for the first time. Although most COVID-19 patients have mild symptoms, some critically ill cases may present severe symptoms like acute respiratory distress syndrome (ARDS), acute kidney injury, hepatic failure, cardiac injury, and might require admission to an intensive care unit (ICU) (1).

Thrombosis, including pulmonary embolism, deep venous thrombosis and acute mesenteric ischemia (AMI), has been reported increasingly in the COVID-19 patients in this pandemic (2). Its pathophysiology is not precisely determined, but researchers suggested that coagulopathy due to the imbalance in coagulation homeostasis with the elevation of fibrinogen, and D-dimers might lead to venous and atrial thrombosis in severe COVID-19 patients (3).

Mesenteric ischemia is a life-threatening emergency health condition that results from inadequate blood flow in the mesenteric circulation. If left untreated, might lead to intestinal necrosis (4). Due to AMI's devastating complications and its high mortality rate, early diagnosis and appropriate treatment is vital.

Here, we report a case of COVID-19 and AMI, besides 27 similar cases are reviewed in the literature.

 


2.Case Report

A 59-year-old man with a history of ten days of fever, shortness of breath, infrequent recurrent abdominal pain, headache, general pain, weakness, and nausea without vomiting was referred to our hospital emergency department. The patient's past medical history included opioid addiction and alcohol usage. His medication history included carbamazepine, chlordiazepoxide, and tranqopine. Initial examination revealed blood pressure of 140/70 mmHg, pulse rate of 100 beats/minute, O2 saturation of 84 %, axillary temperature of 38.5 °C, and body mass index (BMI) of 33kg/m2. The deatail of laboratory findings are shown in Table 1.

The Chest computed tomography (CT) scan showed ground-glass opacity in both lungs that were highly suggestive for the COVID-19 infection (Figure 1). This diagnosis was confirmed by real-time polymerase chain reaction (RT-PCR). Six days after hospitalization, clinical manifestations improved, and O2 saturation rose to 92%. Then, the patient was discharged with ciprofloxacin, aspirin, and famotidine. Two days later, the patient readmitted to the hospital with progressive, intermittent lower abdominal pain, watery diarrhea, and anorexia. The laboratory tests are summarized in Table 1. An  abdominal x-ray and an abdominal CT scan with IV contrast demonstrated multiple air-fluid levels in the small bowel and

 

Table 1. Laboratory values

Measure

First Admission

Second Admission

WBC (/μL)

4700

3800

Neutrophils%

30

80

Platelet (/μL)

140000

-

Ferritin (ug/L)

1650

1230

CPK (U/L)

367

633

LDH (U/L)

-

1213

PH

7.3

7.24

pCO2 (mmHg)

54.8

29

HCO3 (mEq/L)

26

23

ESR (mm/hr)

50

15

CRP (mg/L)

146

133

WBC: white blood cell; CPK: creatine phosphokinase; LDH: lactate dehydrogenase; ESR: erythrocyte sedimentation rate; CRP: C-reactive protein

 

Figure 1. The Chest computed tomography (CT) scan showed ground-glass opacity in both lungs, highly suggestive for COVID-19 pneumonia

 

complete obstruction of the superior mesenteric artery (SMA) with a calcified plaque at its origin (Figure 2 and ).

So, the intravenous heparin infusion was prescribed and the patient prepared for emergency laparotomy. During the operation, the pulseless SMA with small bowel gangrene in the terminal ileum and ischemia of the entire jejunum and colon was reported. Aortomesenteric bypass between SMA and the left common iliac artery, and resection of the gangrenous bowel was performed. The two ends of the intestine were closed temporarily. After 24 hours, a second-look operation was performed. Vascular grafts and the rest of the intestines had adequate blood flow, so side to side ileocolic anastomosis was made.

Fourteen days later, the patient readmitted with an anastomosis leak and enterocutaneous fistula without clinical sepsis. According to extensive pneumonia by COVID-19 (90% of both lungs) and superinfected with severe ventilator-associated pneumonia (VAP), unfortunately, the patient expired one month after surgery.

 

Figure 2. An abdominal x-ray shows multiple air-fluid levels in the small bowel

 

Figure 3. Abdominal CT scan with IV contrast. Axial (a) and coronal (b) section, white arrow revealed the complete thrombosis of SMA with the calcification at its origin. (A; aorta), SMA; superior mesenteric artery

 


3.Discussion

Acute mesenteric ischemia is a life-threatening health condition caused by a lack of blood flow in the mesenteric circulation. The mortality rate of AMI is reported at 5.3 per million each year (5). Moreover, post-surgical mortality rate without revascularization is about 80% (6). In this paper, we reported a 59 years old man with a ten-day history of COVID-19 infection. He had some atherosclerotic risk factors likewise smoking, alcohol consumption, and obesity. An abdominal CT scan with IV contrast demonstrated completed obstruction of the superior mesenteric artery (SMA). Although SMA and celiac trunk had calcified plaque at the location of branching from the aorta, it seems that the most important cause of complete occlusion of these two arteries was the hypercoagulopathy status caused by COVID-19 disease and its increased inflammation state in this patient.

We performed a literature review of PubMed, Scopus, Web of Science, and google scholar databases to retrieve COVID-19 associated AMI case reports and evaluate demographics, clinical presentations, and outcomes. We used keywords: “COVID-19”, “SARS-CoV-2”, “mesenteric”, “intestinal”, “bowel”, “ischemia”, and “thrombosis” for finding English language articles.

Our database search retrieved 27 reported COVID-19-AMI cases with a mean age of 57.4 (82 - 9) years old (7 - 26). The mean timing of AMI diagnosis was 8.1 days after admission. The clinical and laboratory characteristics of all cases are presented in Table 2. Twenty patients were male, and six were female, and the gender of one patient was not reported. The most common initial clinical presentations were fever (48%) and cough (48%) followed by abdominal pain (33%). Vomiting (22%), shortness of breath (18%), and diarrhea (7.4%) were other clinical features of these patients.

The most frequent comorbidities were diabetes mellitus (24%) and hypertension (23%). However, 23% of cases had no comorbidities. Eventually, ten patients were expired, while two cases passed  away

 

Table 2. Clinical features and laboratory findings of 27 previously reported cases of Covid-19 with acute mesenteric ischemia.

Author

N

Age

Sex

Clinical presentation

Timing of AMI diagnosis

WBC

(× 109 /L)

PLT

(×103/μL)

D-dimer (mg/L)

CRP

(mg/L)

Treatment of AMI

Outcome

Vartanoglu Aktokmakyan et al. (7)

5

Mean 61.2

5 Male

4 Cough, 3 Fever, 3 Dyspnea

NR

Mean 8.67

Mean 230 ( 73-359)

Mean 0.447 (0.321-675)

Mean 970 (200-1820)

NR

4 Discharged, 1 Died

Ignat et al.

(8)

3

Mean 50.3

2 Male, 1 Female

2 ARDS, 1 Abdominal Pain, 1 Vomiting,

Mean Day 6.6

NR

NR

NR

NR

2 Small Bowel Laparotomy and Resection, 1 Conservative Management

1 Died, 1 Discharged, 1 Still in Hospital

Al Mahruqi et al.

(9)

2

Both 51

1 Male, 1 NR

1 Shortness of Breath, 1 Fever, 1 Abdominal Pain, 1 Poor Oral Intake

Day 13

30,16

NR

2.5,10

NR

Both Laparotomy, 1 UFH

1 Discharged, 1 Died

Sehhat etl al.

(10)

1

77

Male

Shortness of Breath

Day 11

4.1

146

NR

86

Laparotomy

Died

Azouz etl al.

(11)

1

56

Male

Acute Ischemic Stroke

Day 2

NR

NR

NR

NR

Small Bowel Laparotomy and Resection

Discharged

Table 2. Continued

Cheung et al.

(12)

1

55

Male

Abdominal Pain, Diarrhea, Nausea

Day 12

12.46

100

3.4

(nmol/L)

NR

 

Exploratory Laparotomy and SMA Thromboembolectomy, Heparin Infusion

Discharged

Azhdeh et al.

(13)

1

54

Male

Cough, Shortness of Breath, Fever and Chills

NR

13.9

477

NR

+1

Small Bowel Laparotomy and Resection

Discharged

Kielty et al.

(14)

1

47

Male

Fever, Cough and Vomiting

Day 10

NR

NR

NR

NR

Therapeutic Heparin

Discharged

Mitchell et al.

(15)

1

69

Male

Abdominal Pain, Constipation, Eructation

Day 1

NR

NR

NR

NR

Small Bowel Resection and SMA Thromboembolectomy

Discharged

Beccara et al.

(16)

1

52

Male

Fever and Cough

Day 13

NR

NR

NR

44

Intestinal Resection

Discharged

Vulliamy et al.

(17)

1

75

Male

Abdominal Pain, Vomiting, Cough

Day 1

18.1

497

23.6

NR

Small Bowel Laparotomy and Resection

NR

Barry et al.

(18)

1

79

Female

Fever, Abdominal Pain

Day 1

12.6

NR

NR

125

SMA Thromboembolectomy and Laparotomy, Resection of Necrotic Ileum and Right Colon

Died

Khesrani et al.

(19)

1

9

Female

Fever, Abdominal Pain, Vomiting, Diarrhea

NR

1.14

4

NR

240

Resection of the Ischemic Bowel Loop With Double Ileostomy

Died

Norsa et al.

(20)

1

62

Male

Abdominal Pain and Bilious Vomiting

NR

elevated

NR

elevated

elevated

Small Bowel Resection

Died

Singh et al.

(21)

1

82

Female

Fever, Shortness of Breath, Cough

Day 18

22.8

146

1.3

308

Ileostomy

Discharged

English et al.

(22)

1

40

Male

Severe Dyspnea, Fever and Cough

Day 10

8.6

NR

13.7

NR

Small Bowel Laparotomy and Resection

Discharged

Krothapalli et al.

(23)

1

76

Female

Shortness of Breath

Day 14

9

NR

2.15

7.97

Conservative Management

Died

Soeselo et al.

(24)

1

65

Male

Fever, Cough, Dyspnea

Day 7

9

222

0.78

2

Small Bowel Laparotomy and Resection

Died

Hanif et al.

(25)

1

20

Female

Fever, Cough

Day 7

NR

633

2.34

620

Small Bowel Laparotomy and Resection

Discharged

Bagheripour et al. (26)

1

78

Male

Abdominal Pain, Cough, Dyspnea, Nausea, Vomiting

Day 1

11.2

146

301

Elevated

Conservative Management

Died

NR: not reported; UFH: unfractionated heparin; ARDS: Acute respiratory distress syndrome; CAD: coronary artery disease; HF: heart failure; AF: atrial fibrillation; SMA: superior mesenteric artery; WBC: white blood cell; PLT: platelet; CRP: C-reactive protein.

 

without any comorbidities. Treatment regimen of COVID-19 in most cases was not reported, but commonly the reported treatments regimens included azithromycin, hydroxychloroquine, dexamethasone, ceftriaxone, lopinavir, ritonavir, methylprednisolone, and enoxaparin.

Laparotomy and resection of the bowel as a common approach of mesenteric ischemia was performed in 13 cases (48%), however, in nine cases, bowel resection was not performed. Vartanoglu Aktokmakyan et al. reported that five out of six COVID-19 patients underwent emergency surgery for mesenteric ischemia (7) and ileostomy was created in of two these cases, and SMA thromboembolectomy was performed in three other cases.

In a case reported by Kielty et al. (14) therapeutic heparin was administrated and then the patient was discharged. In nine cases (64%), out of 14 patients, leukocytosis (WBC>11000), was reported and one patient had leukopenia (WBC<4000), the same as our case in the second admission. Fourteen patients (87%) had elevated CRP (CRP>10 mg/L), and D-dimer was elevated (D-dimmer > 0.4 mcg/ml) in all reported cases. Besides, in three patients thrombocytosis (PLT > 450000) was reported, but platelet count was not reported in many of the patients.

According to a study by Sogaard et al., the presence of intra-abdominal inflammation and systemic infections were the most important risk factors for portal vein thrombosis (27), however, two cases reported by Mitchell et al. (15) and English et al. (22) had a stroke and portal vein thrombosis, respectively, but most of the patients did not suffer from other thromboembolic events like PTE or stroke.

In the AMI, the key point is administration of life-saving treatment like revascularization (medical or surgical) before the progression of ischemia to intestinal gangrene and it depends on early diagnosis. If treatment be delayed more than six hours after the onset of mesenteric ischemia, it will be associated with a significant increased mortality rate (28).

Unfortunately, no specific criteria have already been proposed for the early diagnosis of mesenteric ischemia. Therefore, the best treatment for this disease is prevention by early diagnosis of the high risk patients. Hence, it was shown that all inflammatory markers were significantly elevated in the patients with mesenteric ischemic and COVID-19. Moreover, studies revealed that the pathogenicity of COVID-19 has been increasingly attributed to the systemic inflammatory response (SIR) leading to disseminated intravascular coagulation (3).

Yet, there is no consensus whether the coagulation disorders are a secondary response to the SIR or are developed directly by COVID-19 infection. Some studies revealed the incidence of peripheral ischemia and stroke are mediated by antiphospholipid antibodies (29). However, multiple factors seems to be responsible for development of AMI in COVID-19 patients. Foremost, COVID-19 enters the cell through the receptor of the angiotensin-converting enzyme two (ACE2) in the alveoli and, creates a severe form of infection with SIR expression n various organs, including vascular endothelial cells (30, 31). Hence, the entrance of SARS-CoV-2 to endothelial cells, can cause cellular damage and release Von-Willebrand Factor (VWF), which results in endothelial thrombosis.

Next, the cytokine-storm that is caused by increasing the blood level of interleukins one and six and interferon-g, have been reported in these patients (32). Diabetes mellitus, hypertension and atrial fibrillation are known as the main risk factors of AMI (, 34).

There are some signs and symptoms like abdominal distension, nausea, vomiting and diarrhea, when observed in patients with COVID-19, more evaluation like an abdominopelvic CT scan are necessary to rule out the AMI.

Consequently, it seems the use of preventive therapies for mesenteric ischemia in patients with COVID-19 is an important strategy. Prophylactic or therapeutic anticoagulation in patients with thromboembolic risk factors might be effective to reduce the incidence of such complications and improve the prognosis of AMI (35). According to the high worldwide prevalence of COVID-19 and its significant mortality, more studies about COVID-19 and AMI are recommended.

 


4.Conclusion

AMI is a critical health condition that its early diagnosis is crucial for life saving. Although, some studies have reported the relationship between AMI and COVID-19, but further studies are needed to understand this relationship more precisely and reach to proper approaches to prevent AMI in these patients.

 


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