Keywords
mushroom poisoning - poisoning - coronavirus disease 2019 - toxic
Introduction
            More than 5,000 mushroom species have been classified in the world, and more than
               100 species have been found to be poisonous. Among these species, ∼10 are known to
               cause fatal poisoning.[1] Poisonous mushrooms contain different toxins that can cause different clinical manifestations.
               It has been reported that ∼2.5 to 7% of all poisoning cases in the world are due to
               the mushroom ingestion. This rate has been reported as 0.5 to 3% in studies conducted
               in Turkey. In the last decade, the number of mushroom poisoning cases has decreased
               due to the increase in the production of cultivated mushrooms, production of various
               species in the culture environment, and increased public awareness.[2]
               
            The World Health Organization (WHO) declared coronavirus disease 2019 (COVID-19) as
               a pandemic on March 11, 2020, and the first case was seen in Turkey on the same day.[3] Since then, measures taken by governments and individuals have affected the behavioral
               characteristics of societies. In the peak periods of the disease, the hospital admissions
               of all non-COVID-19 elective cases were postponed.[4]
               [5]
               [6] However, there was no significant increase in the number of non-COVID-19 emergency
               department admissions across the world.[7] In a study from China, Li et al reported an increase in mushroom poisoning cases
               in 2020.[8] Similarly, in a study from Israel, Lurie et al reported an increased number of mushroom
               poisoning cases compared with the fall/winter period in 2019 and noted an increase
               in the median annual rate between 2015 and 2019.[9] In light of this literature, we aimed to investigate the effect of the COVID-19
               pandemic on emergency department presentations with mushroom poisoning in a tertiary
               hospital in Turkey.
         Materials and Methods
            Study Design
            
            This study was conducted as a retrospective cohort study at Umraniye Training and
               Research Hospital, University of Health Sciences, a 795-bed tertiary education hospital
               with 1,110 daily emergency department presentations (annual average of the study period).
               The data of patients who presented to the emergency department between January 1,
               2018, and December 31, 2020, were retrospectively collected. To reveal the effect
               of COVID-19 pandemic on emergency department presentations with mushroom poisoning,
               the means of the pre-pandemic period (2018–2019) and the pandemic period (2020) were
               compared.
            
            Study Population
            
            The population of the study consisted of adult patients who presented to the emergency
               department with symptoms of mushroom poisoning during the study period. The patients
               who were diagnosed with the International Classification of Diseases (ICD)-10 code
               T62.0 of the WHO medical classification concerning the toxic effect of ingested mushrooms
               were identified through the computerized medical and laboratory record system of the
               hospital. Patients with missing data were excluded from the study. The flowchart of
               the study is shown in [Fig. 1].
            
             Fig. 1 Flowchart of the study.
                  Fig. 1 Flowchart of the study.
            
            
            
            Data Collection
            
            The patients' demographic data, presentation seasons, laboratory findings, emergency
               department outcomes, and mortality due to mushroom poisoning were obtained from the
               computer-based hospital system. The patient's files with the ICD-10 code T62.0 toxic
               effect of ingested mushrooms were obtained from the hospital computer-based data system
               in the electronic environment. Data were organized by the researchers (S.Ö. and İ.A.).
               The presentation season of the patients was recorded as winter (December, January,
               and February), autumn (September, October, and November), spring (March, April, and
               May), and summer (June, July, and August). The mean values for sodium, potassium,
               γ-glutamyl transpeptidase, total bilirubin, alanine aminotransferase (ALT), aspartate
               aminotransferase, indirect bilirubin, and direct bilirubin were calculated for 2 years
               preceding the pandemic (2018 and 2019). Emergency department outcomes were noted as
               discharge, hospitalization, and refusal of hospitalization or hemodialysis treatment.
            
            Statistical Analysis
            
            We used IBM SPSS Statistics for Mac, IBM Corp, Version 27.0, Armonk, New York, United
               States to perform statistical analyses. To evaluate the conformance of variables to
               the normal distribution, the Kolmogorov–Smirnov's test was conducted. The nonnormally
               distributed data were expressed as median and 25th to 75th percentile values, and
               the data that conformed to the normal distribution were presented with mean and standard
               deviation values. Categorical data were presented as the number of cases and percentages.
            
            Although the first case was seen in our country and the declaration of the pandemic
               was March 11, 2020, the effects of the government's reactions and measures on the
               social behavior began in January 2020.[3] For this reason, the first months of 2020 were also evaluated within the effects
               of the pandemic. To understand the impact of the pandemic, the data for 2020 and the
               average data for 2019 and 2018 were compared. For the comparison of qualitative and
               quantitative data between the two groups, the chi-square and Mann–Whitney's U tests were used. The p-value of 0.05 was considered as a cutoff point for statistical significance.
            Results
            Of the 171 patients included in the final analysis, 69 (42.3%) were male. The median
               age was 39 (25th–75th percentile: 28–53) years. The baseline characteristics of the
               enrolled patients are shown in [Table 1], and the seasonal distribution of the mushroom poisoning cases presenting to the
               emergency department from 2018 to 2020 is shown in [Fig. 2]. The number of patients hospitalized due to mushroom poisoning was 49 (51%) in 2018,
               28 (45.9%) in 2019, and 8 (57.1%) in 2020. Nineteen (19.9%) patients were discharged
               in 2018, 15 (24.5%) in 2019, and 1 (7.1%) in 2020. Twenty-eight (29.1%) patients in
               2018, 18 (29.5%) in 2019, and 5 (35.7%) in 2020 refused hospitalization or hemodialysis
               treatment. Hemodialysis was applied to 39 (39.5%) patients in 2018, 21 (34.4%) in
               2019, and 6 (42.8%) in 2020.
             Fig. 2 Seasonal distribution of mushroom poisoning cases presenting to the emergency department
                  from 2018 to 2020.
                  Fig. 2 Seasonal distribution of mushroom poisoning cases presenting to the emergency department
                  from 2018 to 2020.
            
            
            
               
                  Table 1 
                     Baseline characteristics of the enrolled patients according to years
                     
                  
                     
                     
                        
                        | Variables | 2018 (n = 96) | 2019 (n = 61) | 2020 (n = 14) | 
                     
                  
                     
                     
                        
                        | Age (y), median (25th–75th quarters) | 39 (28–53) | 40 (33–54.5) | 39 (27.75–28.25) | 
                     
                     
                        
                        | Gender, n (%) | 
                     
                     
                        
                        |  Male | 40 (41.7%) | 25 (41%) | 4 (28.6%) | 
                     
                     
                        
                        |  Female | 56 (58.3%) | 36 (59%) | 10 (71.4%) | 
                     
                     
                        
                        | Season, n (%) | 
                     
                     
                        
                        |  Winter | 12 (12.5%) | 17 (27.9%) | 5 (35.7%) | 
                     
                     
                        
                        |  Spring | 20 (20.8%) | 17 (27.9%) | 2 (14.3%) | 
                     
                     
                        
                        |  Summer | 12 (12.5%) | 12 (19.7%) | 3 (21.4%) | 
                     
                     
                        
                        |  Autumn | 52 (54.2%) | 15 (24.6%) | 4 (28.6%) | 
                     
                     
                        
                        | Laboratory findings, median (25th–75th quarters) | 
                     
                     
                        
                        |  Aspartate aminotransferase (U/L) | 23 (19–29.25) | 19 (16–25) | 20 (17.75–21.75) | 
                     
                     
                        
                        |  Alanine aminotransferase (U/L) | 19.5 (14–26) | 19 (13.5–28.5) | 14.5 (11–19) | 
                     
                     
                        
                        |  γ-glutamyl transpeptidase (U/L) | 18 (13–30) | 20.5 (14–35.75) | 16 (10–23) | 
                     
                     
                        
                        |  Total bilirubin (mg/dL) | 0.51 (0.33–0.79) | 0.51 (0.34–0.82) | 0.59 (0.43–1.49) | 
                     
                     
                        
                        |  Direct bilirubin (mg/dL) | 0.18 (0.13–0.26) | 0.19 (0.13–0.29) | 0.22 (0.15–0.45) | 
                     
                     
                        
                        |  Indirect bilirubin (mg/dL) | 0.35 (0.21–0.52) | 0.31 (0.21–0.53) | 0.37 (0.30–1.04) | 
                     
                     
                        
                        |  Sodium (mEq/L) | 138 (137–140) | 139 (138–141) | 139 (138–140) | 
                     
                     
                        
                        |  Potassium (mEq/L) | 4.4 (4.2–4.6) | 4.3 (4.1–4.6) | 4.3 (4.1–4.6) | 
                     
                     
                        
                        | Emergency department outcomes, n (%) | 
                     
                     
                        
                        |  Hospitalization | 49 (51%) | 28 (46%) | 8 (57.1%) | 
                     
                     
                        
                        |  Refusal of treatment | 28 (29.1%) | 18 (29.5%) | 5 (35.7%) | 
                     
                     
                        
                        |  Discharge | 19 (19.9%) | 15 (24.5%) | 1 (7.1%) | 
                     
                     
                        
                        | Hemodialysis, n (%) | 39 (39.5%) | 21 (34.4%) | 6 (42.8%) | 
                     
                     
                        
                        | Mortality, n
                               | 1 | 0 | 0 | 
                     
               
             
            
            Only one patient died due to the toxic effect of ingested mushrooms during hospitalization
               (in 2018). Transaminase levels were elevated in the initial tests in two patients
               in 2018 and in two patients in 2019. No elevation of transaminases was observed in
               initial test of the patients in 2020. The comparisons of the baseline characteristics
               between the pre-pandemic and pandemic periods are shown in [Table 2]. In the pre-pandemic period, the average number of patients presenting with mushroom
               poisoning per year was 78.5. In the pandemic period, 14 patients presented with mushroom
               poisoning annually. There was a 5.6-fold decrease in the number of patients presenting
               with mushroom poisoning during the pandemic.
            
               
                  Table 2 
                     Comparisons of baseline characteristics between the pre-pandemic and pandemic periods
                     
                  
                     
                     
                        
                        | Variables | 2018 and 2019 (n = 157) | 2020 (n = 14) | 
                              p-Value | 
                     
                  
                     
                     
                        
                        | Age (y), median (25th–75th quarters) | 39 (31–53) | 39 (27.75–28.25) | 0.616 | 
                     
                     
                        
                        | Gender, n (%) | 
                     
                     
                        
                        |  Male | 65 (41.4%) | 4 (28.6%) | 0.348 | 
                     
                     
                        
                        |  Female | 92 (58.6%) | 10 (71.4%) | 
                     
                     
                        
                        | Season, n (%) | 
                     
                     
                        
                        |  Winter | 29 (18.5%) | 5 (35.7%) | 0.343 | 
                     
                     
                        
                        |  Spring | 37 (23.6%) | 2 (14.3%) | 
                     
                     
                        
                        |  Summer | 24 (15.3%) | 3 (21.4%) | 
                     
                     
                        
                        |  Autumn | 67 (42.7%) | 4 (28.6%) | 
                     
                     
                        
                        | Laboratory findings, median (25th–75th quarters) | 
                     
                     
                        
                        |  Aspartate aminotransferase (U/L) | 21 (18–28) | 20 (17.75–21.75) | 0.283 | 
                     
                     
                        
                        |  Alanine aminotransferase (U/L) | 19 (14–27) | 14.5 (11–19) | 0.038 | 
                     
                     
                        
                        |  γ-glutamyl transpeptidase (U/L) | 19 (14–34) | 16 (10–23) | 0.179 | 
                     
                     
                        
                        | Total bilirubin (mg/dL) | 0.51 (0.33–0.80) | 0.59 (0.43–1.49) | 0.129 | 
                     
                     
                        
                        | Direct bilirubin (mg/dL) | 0.18 (0.13–0.26) | 0.22 (0.15–0.45) | 0.237 | 
                     
                     
                        
                        | Indirect bilirubin (mg/dL) | 0.33 (0.21–0.53) | 0.37 (0.30–1.04) | 0.124 | 
                     
                     
                        
                        | Sodium (mEq/L) | 139 (137–141) | 139 (138–140) | 0.776 | 
                     
                     
                        
                        | Potassium (mEq/L) | 4.4 (4.1–4.6) | 4.3 (4.1–4.6) | 0.555 | 
                     
               
             
            Discussion
            In this retrospective study, we evaluated the effect of the COVID-19 pandemic on emergency
               department presentations with mushroom poisoning. To this end, we compared the average
               number of presentations during the pre-pandemic and pandemic periods. According to
               our results, there was a 5.6-fold decrease in the number of patients presenting with
               mushroom poisoning. To the best of our knowledge, this was the first study to evaluate
               the effect of the COVID-19 pandemic on mushroom poisoning in Turkey. Contrary to the
               literature, we found a decrease in mushroom poisoning cases during the pandemic.
            We think that one of the logical explanations for the results of our study may be
               the change in people's hospital admission habits during the pandemic period. During
               the pandemic, there have been changes in the patient characteristics of emergency
               departments. While the number of patients presenting with COVID-19-like symptoms increased,
               presentations involving non-COVID-19-like symptoms have decreased considerably.[10] Another possible logical explanation for our results might be the changes in people's
               eating habits. The COVID-19 pandemic and its restrictive measures have also resulted
               in the modification of the eating habits of individuals. It has drastically changed
               food shopping behaviors, and the resulting economic recession has caused concerns
               over food availability. During lockdowns implemented, people have started to consume
               more pasta and canned goods than green vegetables, which has led to the increased
               incidence of nutritional disorders.[11]
               [12]
               
            Changes have also been reported in cases of mushroom poisoning due to altered nutritional
               habits and emergency patient characteristics. Li et al called mushroom poisoning cases
               in China mushroom poisoning outbreaks. They reported 24 new species of mushroom causes
               poisoning, a case of shiitake mushroom dermatitis, and mortality in one case due to
               Paxillus involutus. Li et al recommended promoting awareness concerning the safe consumption of mushrooms
               to reduce related poisoning, but they did not comment on the reasons for this change
               in mushroom poisoning cases.[8] In another study, Lurie et al investigated the effect of the COVID-19 pandemic on
               mushroom poisoning cases in Israel. They showed a 5-fold increase compared with the
               same fall/winter period in 2019, as well as a 2.5-fold increase in the median annual
               rate from 2015 to 2019. They suggested that this might be due to favorable increased
               outdoor activities of the public and climate conditions in response to restrictions
               on other relaxation activities obligatory during the pandemic as an explanation of
               their results.[9] Contrary to these two studies, our sample indicated a 5.6-fold decrease in the median
               annual rate of mushroom poisoning cases during the pandemic compared with the pre-pandemic
               2-year period. An explanation for this discrepancy may be that we used emergency department
               data in our study, while the other two studies evaluated data obtained from national
               poisoning information centers. Lurie et al reported that most cases had minor or no
               symptoms and signs.[9] We consider this particular patient group may not have presented to the emergency
               department due to the fear of contracting COVID-19. Another possible explanation is
               our study being conducted in a metropolitan city and not including national data and
               individuals' changing dietary habits in favor of storable foods, such as pasta and
               canned food.
         Limitations
            The main limitation of our study was its retrospective nature. First, there may have
               been other risk factors that could not be measured due to the retrospective design.
               Retrospective studies cannot determine causation; they only evaluate association.
               Second, we only evaluated data obtained from an emergency department of a tertiary
               hospital located in a metropolitan city and did not include national data. The situation
               may be different in the countryside. Third, the poisonous mushroom species were not
               evaluated in our study; therefore, we were not able to determine whether there was
               a change in the poisoning characteristics similar to the previous study conducted
               in China.[8] Fourth, in our country, clinicians are obliged to report mushroom poisoning cases
               to law enforcement in accordance with local legal policies. The data of these cases
               are considered forensic data. Therefore, clinicians are careful while recording the
               data of mushroom poisoning cases. On the other hand, this legal obligation may have
               encouraged patients to give incorrect information. Another limitation of our study
               was the high number of patients who refused treatment. Due to the clinical practices
               of our hospital, we follow up the patients by hospitalizing them more. Before hospitalization,
               patients are told that applications such as hemodialysis will be performed. Patients
               who have already become asymptomatic with symptomatic treatment in the emergency department
               refuse hospitalization and hemodialysis. Another explanation for about one-third of
               patients' refusal to receive treatment may be the low level of health literacy in
               our country, as in the rest of the world.[13] Finally, our study had a single-center design, and therefore, our results cannot
               be generalized to other health care institutions.
         Conclusion
            In conclusion, our results indicated a 5.6-fold decrease in the number of patients
               presenting to the emergency department with mushroom poisoning. This may be due to
               the changes in the eating habits of individuals during the pandemic and our study
               being conducted in a metropolitan city. We recommend that multicenter studies be performed
               to verify the data obtained from our study and increase their generalizability.