key: cord-0805350-civbmhrg
authors: Tariq, Raseen; Saha, Srishti; Furqan, Fateeha; Hassett, Leslie; Pardi, Darrell; Khanna, Sahil
title: Prevalence and Mortality of COVID-19 patients with Gastrointestinal Symptoms: A Systematic Review and Meta-analysis
date: 2020-06-10
journal: Mayo Clin Proc
DOI: 10.1016/j.mayocp.2020.06.003
sha: 1267f44987a1e1102c7ef39e26f0f0fd0b319ed4
doc_id: 805350
cord_uid: civbmhrg

Abstract Objectives To perform a systematic review and meta-analysis evaluating the prevalence of gastrointestinal (GI) symptoms and mortality in patients diagnosed with coronavirus disease 2019 (COVID-19). Methods A systematic search of MEDLINE, Embase, Cochrane Central Register of Controlled Trials, Cochrane Database of Systematic Reviews and Scopus was performed from 2019 to May 7th, 2020. Observational studies including adults with COVID-19 infection and reporting GI symptoms were included. Primary outcome was assessing weighted pooled prevalence (WPP) of GI symptoms in patients with COVID-19. Secondary outcomes were WPP of overall mortality, and mortality in COVID-19 patients with GI symptoms. Results A total of 78 studies with 12797 patients were included. Among GI symptoms (at onset of illness in 6, at admission in 17, data given separately for both in 3, data unavailable in 52 studies), WPP of diarrhea was 12% (95% CI, 8%-17%), I 2 =94%, nausea and/or vomiting was 9.0% (95% CI, 5.5%-12.9%). I 2 =93%, loss of appetite was 22.3% (95% CI, 11.2%-34.6%, I 2 =94%, and that of abdominal pain was 6.2% (95% CI, 2.6%-10.3%, I 2 =92%. Mortality among patients with GI symptoms [0.4% (95% CI, 0%-1.1%), I 2 =74%] was similar to overall mortality [2.1% (95% CI, 0.2%-4.7%), I 2 =94%], p=0.15. Majority of studies had high risk of bias and overall quality of evidence was low to very low for all outcomes. Conclusions Gastrointestinal symptoms are seen in up to one in five patients with COVID-19. More high quality evidence is needed to confirm these findings and to explore factors causing mortality in these patients.

Coronavirus disease 2019 (COVID- 19) is an infection caused by the novel coronavirus, named severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2). The first case of was reported in December 2019 in Wuhan, China. Since then, the disease has been declared a pandemic, affecting over 4,700,000 people and causing over 300,000deaths globally, (as of May 21, 2020) 1, 2 . Similar to other coronaviruses, SARS-CoV-2 primarily affects the pulmonary system, but multi-system involvement has been reported. The spectrum of disease includes asymptomatic colonization, mild disease with fever, cough and fatigue, and severe disease characterized by dyspnea, hypoxemia, acute respiratory distress syndrome, need for mechanical ventilation, and death 3 .

The presence of gastrointestinal (GI) manifestations in COVID-19 patients has been noted in several reports recently, with 16%-50% of patients reporting one or more GI symptoms at presentation or during the illness 4 . Recognition of these symptoms has important implications for identification of individual cases, and would influence testing and isolation strategies, which are continually evolving based on emerging data. One recent meta-analysis of 4243 patients found the pooled prevalence of all gastrointestinal symptoms to be 17.6% 5 ; however, most of the data included in the analysis was from Asia, limiting is generalizability. Another meta analysis of 47 studies reported the symptoms of diarrhea and nausea/vomiting to be present in 7.7% and 7.8% patients with COVID 19 respectively. However, the study didn't report rates of mortality among these patients 6 .

Given the rapidly growing literature regarding gastrointestinal symptoms in COVID-19 patients, we conducted an updated systematic review and meta-analysis to assess the prevalence of GI symptoms in patients with COVID-19, and to determine if mortality is influenced by the presence of GI symptoms in these patients.

All procedures used in this meta-analysis were consistent with the Preferred Reporting Items for Systematic Reviews and Meta-Analyses (PRISMA) guidelines (Appendix 1) 7 .

The studies considered in this meta-analysis were observational studies that included adults with confirmed COVID-19 infection and reported clinical characteristics, including GI symptoms. Studies not reporting the presence or absence of GI symptoms (as non-reporting during this pandemic would not equate to lack of GI symptoms), and individual case reports were excluded. Two authors (R.T. and S.S.) independently reviewed the titles and abstracts of the identified studies, and those that did not answer the research question of interest were excluded.

The remaining articles were reviewed to determine inclusion criteria fulfillment. The reference lists of articles with information on the topic were also reviewed for additional pertinent studies.

A flow diagram of included studies is shown in Figure 1 .

Data were independently abstracted to a predetermined collection form by two investigators (R.T. and S.S.). Data collected for each study included study setting and design, month and year of publication, location, number of patients, patients with GI symptoms, symptom onset (symptoms assessed at onset of illness or at admission to the hospital), severity of COVID-19, duration of follow up and mortality. Severe infection was defined as admission to the intensive care unit (ICU) or need for mechanical ventilation. Conflicts in data abstraction were resolved by consensus, referring to the original article.

Majority of studies included were case series, hence an appropriate risk of bias tool was applied (Supplementary Table 2) 8 . Risk of bias was assessed based on four domains: selection, ascertainment, causality and reporting. An overall judgement of the risk of bias was made based on factors deemed to be most critical for the systematic review (selection criteria, ascertainment of outcome, follow up duration).

The GRADE framework was used to interpret the findings of the study. The principles of the GRADE system have been adopted by the Cochrane Collaboration for evaluating the quality of evidence for the outcomes reported in systematic reviews. For systematic reviews, the GRADE approach defines the quality of the body of evidence as the extent to which one can be confident that an estimate of effect or association is close to the quantity of specific interest. The GRADE framework classifies the quality of evidence in one of four levels-high, moderate, low, and very low. Quality of a body of evidence involves consideration of the study design of included studies, methodological quality, directness of evidence, heterogeneity, inconsistency of results and risk of publication bias 9,10 .

Data on symptom prevalence is expected to be of low quality, since the evidence primarily arises from observational studies. This is particularly true in the context of an ongoing pandemic.

Due to the clinical importance of the study question, such studies were included in the systematic review and meta-analysis.

Our primary analysis focused on assessing weighted pooled prevalence (WPP) of GI symptoms in patients with COVID-19 infection, occurring any time during the course of illness.

Secondary outcomes were WPP of mortality in all COVID patients and in patients with GI symptoms.

We calculated WPP with corresponding 95% confidence intervals (CI) for each symptom. We used the inverse variance heterogeneity (IVhet) model of meta-analysis with corresponding 95% CI for the overall and subgroup analyses. The IVhet model is a modification of the fixed-effects models that accounts for between-study heterogeneity, retains the individual weights of the studies and decreases the variance in estimates 11 . Freeman-Tukey double arcsine transformation was used to avoid giving more weight to studies with prevalence estimates that are too large or too small. We assessed heterogeneity within groups with the I 2 statistic, which estimates the proportion of total variation across studies that is due to heterogeneity in study patients, design, or interventions rather than chance; I 2 values greater than 50% suggest substantial heterogeneity 12 

The described database search strategy revealed 827 unique studies, 10 tudies were identified from other sources; titles and abstracts were screened and relevant articles were obtained. Of the potentially relevant articles, 759 were excluded for various reasons ( Figure 1 ) leaving 78 studies that were included in this meta-analysis (Table 1 ).

The risk of bias of included studies is shown in supplementary Table 2 . Risk of bias was high in 48 studies, medium in 24 studies and low in 6 studies.

The 78 included studies reported a total of 12767 patients 4,5,13-88 . Of these, 57 were performed in mainland China, 6 in United States, 1 in Australia, 1 in Europe, 1 in France, 1 in Germany, 1 in Netherland, 1 in Hong Kong, 2 in Italy ,1 in Spain, 1 in Japan, 2 in Korea, 1 in Taiwan and 2 in Singapore (Table 1) . Among the studies performed in China, 24 were from Wuhan City in Hubei province, four included data from the entire Hubei province, one from Jingzhou city, two from Beijing City, three from Chongqing city, three from Shanghai, three from Zhuahi City, two from Nanjing province, one from Anhai province, five from Zhejiang province, three from Guangdong province, one from Hunan province, one from Zhengzou province, one from Hunan province ,one from Jiangsu province, one from Shenzun province and one study included data from all provinces in China. The earliest study recruitment period started from December 11 th , 2019 and the last date of patient enrollment was April 16th 2020. Twelve studies were retrospective cohort studies, one was a prospective cohort study, one was a case control study and the remaining 64 were case series ( Table 1) .

The age distribution among the included patients ranged from 15-96 years, and 58.4% were female. Of the included studies, sixty four included only patients who were hospitalized (in one study, patients with mild symptoms were included, but they were hospitalized for monitoring and quarantine), ten studies included patients both from inpatients and outpatients, one included Table 3 ); 3 studies gave data separately for symptoms at illness onset and at hospitalization. Only one study reported data on how many patients had GI symptoms occurred with and without pulmonary symptoms. In this study, 23.3% patients had GI symptoms only, 43 .2% had pulmonary symptoms only and 33.5% had both.

Of the included studies, a total of 74 reported the prevalence of diarrheal symptoms in COVID-19 patients ranging from 0%-100%. Overall, of the 12688 patients, 1773 reported diarrhea; the WPP was 12% (95% CI, 8%-17%). There was significant heterogeneity among the studies with an I 2 =94% (Figure 2 ). Publication bias was seen on visual inspection of a funnel plot (Supplementary Figure 1) . There was one outlier study (Siegel et Among the 27 studies reporting on abdominal pain, prevalence ranged from 0%-50%; overall 418/5896 COVID-19 patients reported abdominal pain with a WPP of 6.2% (95% CI, 2.6%-10.3%, I 2 =92%, Supplementary Figure 4) . On performing sensitivity analyses by removing studies with high risk of bias, estimates did not change and heterogeneity did not decrease for any symptom (all p>0.05).

A total of 42 studies reported overall mortality among patients with COVID-19, which ranged from 0-100%. One study included only patients who had died of COVID-19, and hence was excluded from this analysis. Of the total of 8122 patients in the remaining 41 studies, 320 died with a WPP for an overall mortality of 2.1% (95% CI, 0.2%-4.7%). There was significant heterogeneity among the studies with an I 2 =94% (Figure 3 ). Cause of death (whether or not attributable to COVID-19) was not specified in any of the studies. Publication bias was seen on visual inspection of a funnel plot (Supplementary Figure 5) .

Twenty-one studies reported mortality as an outcome among patients with GI symptoms. Of a total of 4983 patients, 34 died with WPP of 0.4% (95% CI, 0%-1.1%). There was significant heterogeneity among the studies with an I 2 =74% (Figure 4 ).

Mortality among patients with GI symptoms was similar to overall mortality (p=0.15). On performing sensitivity analyses by removing studies with high risk of bias, estimates and between study heterogeneity did not decrease, neither for mortality in patients with GI symptoms nor for overall mortality.

Quality of evidencePer the GRADE framework, the quality of evidence for the prevalance of gastrointestinal symptom outcome was low because of study design (observational studies only), lack of consistency of methodology, presence of publication bias and significant heterogeneity in all effect estimates. The quality of evidence was considered very low for mortality outcome because of study design (observational studies only), lack of consistency of methodology, presence of publication bias, significant heterogeneity and inconsistency among reported results.

Additionally, none of the studies had adjusted for any potential confounding factors for mortality outcome (Supplementary Table 4 )

In this systematic review and meta-analysis, we found that gastrointestinal symptoms were present in up to one in five patients with COVID-19. The highest prevalence was for loss of appetite (~1/5th of patients), while the other symptoms occurred in up to 10% of patients.

Mortality among patients with GI symptoms was similar to overall mortality; this must be interepreted with caution, as variable follow up, lack of a uniform criteria for COVID-19 attributable mortality and lack of adjustment for cofounders would affect estimates of mortality.

WPP of diarrhea and nausea/vomiting were higher in the subgroup of studies conducted outside China compared to studies from China, likely due to increasing awareness and reporting of GI manifestations as the pandemic progressed. There was substantial heterogeneity for all estimates, and publication bias was present. Overall, the quality of evidence was low for outcomes of prevelance of GI symptoms and very low for mortality outcomes.

Several reports have described the occurrence of GI symptoms and possible feco-oral transmission in patients with COVID-19 4,28,68 . A previous systematic review of six studies reported diarrhea, nausea, vomiting and abdominal pain in less than 10% patients, which is similar to our results 89 . One recent meta-analysis of 47 studies with 10,890 patients estimated a pooled prevelanance of diarrhea to be 7.7%, nausea/vomiting 7.8% and abdominal pain 2.7%.

The study also pooled the prevalence of diarrhea among studies from countries other than China only and found that prevelance of diarrhea in non-China studies to be higher with pooled prevelance of 18.3% 6 . Another meta analysis of 29 studied reported a pooled prevalence of digestive symptoms of 15% with nausea or vomiting, diarrhoea, and loss of appetite being the three most common symptoms 90 . The prevalence of most GI symtoms in our study and the subgroup analyses by study location are similar to prior meta-analyses. Among all the GI symptoms, the prevalance of loss of appetite in our study was higher than the other GI symptoms. Loss of appetite is commonly seen with febrile illness, which could contribute to the higher rates. However, fewer included studies reported this symptom, which could affect our estimates.

Several important factors should be considered while interpreting results from our study. Until the date of this review, we are still in the mid-phase of the pandemic, with data reported predominantly being from China. Only a quarter of the included studies are from reports outside China. Additionally, the quality of data collection during pandemics is not robust due to the possibility of inadequate documentation of symptoms. The studies included in this meta-analysis primarily included hospitalized patients. Patients with mild disease who were not admitted to the hospital were not included. Patients with mild to moderate symptoms constitute a majority (81%) of those infected with SARS-CoV-2 virus 3 . Exclusion of these patients is likely to affect estimates of symptom prevalence. In the absence of published reports of symptom analyses in this cohort of patients, it is difficult to assess the direction in which our estimates would change, and therefore our results are not necessarily generalizable to outpatients.

Another important factor is that GI symptoms may be under-reported. Increasing awareness, comprehensive symptom questionnaires and prospective study design would likely provide more reliable estimates of GI symptoms in future studies. In the studies included, there was also limited information on GI specific laboratory tests, endoscopy reports, histopathology reports and imaging. Angiotensin-converting enzyme 2 (ACE2) is one of the receptors to which coronaviruses bind. ACE2 is expressed in the lung, and within the GI tract it is expressed in the small intestine, large intestine and cholangiocytes 91 . This may facilitate the spread of the virus through the GI tract, and could explain the occurrence of GI symptoms in COVID-19.Future studies should explore these aspects, which would shed light on the pathophysiology of GI involvement in COVID-19 infections.

We found mortality in patients with GI symptoms to be similar to overall mortality. Of note, mortality reported here is all-cause mortality. Deaths in COVID-19 could be due to the infection itself or due to underlying comorbid conditions. A uniform definition for COVID-19 attributable mortality and a standardized time frame (e.g., within 30 days) would be essential in assessing the impact of the infection and its differing presentations on mortality. Studies included in the systematic review did not assess the effect of different factors such as age and comorbid conditions on mortality. Moreover, several studies did not report, or had limited follow up, which would affect mortality estimates. By doing a sensitivity analysis based on risk of bias (which incorporates follow up duration as a quality indicator), we could partly adjust for limited follow up.

Strengths of this study include a comprehensive search strategy with studies from different countries and assessment of several GI symptoms. However, the study has several limitations.

Most of the included studies are retrospective, and are thus at high risk of bias. There is also evidence of significant heterogeneity and publication bias. Several included studies are from Wuhan, China, making it difficult to exclude the possibility of overlapping patients in different studies. As mentioned above, several factors affect mortality estimates. Only 12 included studies had information regarding comorbid GI conditions, which precluded assessment of whether symptoms were attributable to the infection or underlying disease. Only one study mentioned if patients had GI symptoms only or if they had both GI symptoms with respiratory symptoms, hence we couldn't assess if GI symptoms present alone or with other symptoms.

Finally, most of the studies were in the hospital setting, thus there was an under-representation of mild-moderate cases and cases within the community.

Up to one in five of patients with COVID-19 infection have gastrointestinal symptoms.

Clinicians should be aware of the possibility that patients with COVID-19 infection can have GI symptoms, and keep a low threshold for testing for the infection. Our study highlights the need for high quality prospectively collected data, with inclusion of patients in the community setting, and exploration of the causes underlying mortality. 

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