Impact of the COVID‐19 pandemic on pathological autopsy practices in Japan
Coronavirus disease 2019 (COVID‐19) is an emerging infectious disease caused by severe acute respiratory syndrome coronavirus 2 (SARS‐CoV‐2), which was first reported in Wuhan, China, in December 2019 and has rapidly spread worldwide. In the first year of the pandemic, more than one million people died, and since then, the global public health crisis has continued. It is important to understand the pathophysiology and pathogenesis of these emerging infectious diseases to develop preventive and therapeutic methods. Therefore, it is essential to perform pathological autopsies on patient cadavers and evaluate the post‐mortem tissue samples obtained from autopsies to determine the histopathological changes due to infection of the pathogens for elucidating the pathogenesis of the infections. In addition, pathological autopsies are also considered an important quality assessment tool in healthcare through the diagnosis of the cause of death and concurrent diseases. Then, even during a pandemic of an emerging infectious disease, pathological autopsies should be carried out without hindrance in order to maintain and improve the standard of normal healthcare. Various guidelines regarding personal protective equipment (PPE) and autopsy procedures for deceased patients with SARS‐CoV‐2 infection were published by the Centers for Disease Control and Prevention (CDC), USA, and other national public health agencies. Based on these guidelines, numerous autopsies have been performed in various countries since early in the pandemic, and many important findings, including characteristic pulmonary findings and occurrence of thrombosis, have been obtained. Guidelines , for pathologists doing autopsy on COVID‐19 patients were released in Japan by the National Institute of Infectious Diseases (NIID) through the Japanese Society of Pathology as early as February 2020. However, unlike other countries that have conducted many autopsies, only a few autopsies were reported from Japan in the beginning of the pandemic, suggesting that pathological autopsies might not be sufficiently performed for COVID‐19 patients. Moreover, even under these circumstances, pathological autopsies should be performed for patients who do not have SARS‐CoV‐2 infection or who exhibit similar symptoms but lack a diagnosis of the virus. However, few reports have considered autopsies of non‐COVID‐19 patients during this pandemic. Similarly, there is no information on whether each medical facility has restrictions on autopsies in these cases. Herein, we conducted a questionnaire survey to understand the actual status of pathological autopsies in Japan during the first year of the COVID‐19 pandemic when the cumulative number of infections in Japan was limited to less than 1% of the total population and before a useful COVID‐19 vaccine was clinically available. Based on the survey, we report the status of pathological autopsies performed in Japan during the early stages of the COVID‐19 pandemic and the arrangements for conducting autopsies at each medical facility to evaluate the exact impact of this pandemic on pathological autopsy practices for cases including non‐COVID‐19 patients in Japan. 

An e‐mail containing a link to the online questionnaire was sent to all 422 accredited facilities and 418 registered facilities of the Japanese Society of Pathology on December 15, 2020. A total of 678 email‐receiving facilities were chosen to participate in the survey. The response deadline was January 22, 2021. A questionnaire was used to investigate the status of pathological autopsy practices at each facility from the beginning of the COVID‐19 pandemic (for the survey about the non‐COVID‐19 autopsy, April 7, 2020, when the state of emergency was declared, was assigned as the start date of the survey period) to the date of reply from the facility. The Ethics Committee of Chiba University School of Medicine, to which one of the principal investigators (HS) who conducted this e‐mail questionnaire survey belongs, has determined that this survey is not subject to review by the Ethics Committee because it does not involve human subjects. Furthermore, in conducting the survey, we disclosed the contents of the questionnaire to the Japanese Society of Pathology and obtained their permission and cooperation to conduct the survey. In this study, a portion of the data acquired via survey questionnaire responses was utilized. The other sections of the data from the survey questionnaire responses have previously been reported. For statistical analysis, Wilcoxon matched‐pairs signed rank test or Mann–Whitney test were used to compare values. 

Autopsy status of patients with confirmed or suspected COVID‐19, and decision‐making algorithm for conducting autopsies of confirmed or suspected COVID‐19 We sent e‐mails requesting survey completion to 678 medical facilities in Japan, 227 (34%) of which responded. Of the hospitals that responded, 13 facilities (5.7%) had 199 or fewer beds, 70 (31%) had 200–399 beds, and 144 (63%) had 400 beds or more. Among them, 197 facilities (87%) accepted COVID‐19 patients for hospitalization and 71 (31%) answered that they had experienced the death of COVID‐19 patients (Table ). In order to understand the actual status of pathological autopsy practices involving non‐COVID‐19 cases during the early phase of the pandemic, we classified patient cadavers that were candidates for pathological autopsy into confirmed COVID‐19, suspected COVID‐19, and non‐COVID‐19 cases, and investigated procedures for each case at each medical facility. Of all 227 facilities that responded, autopsies of patients with a confirmed diagnosis of COVID‐19 at the time of the autopsy were performed in 10 facilities (4.4%, 10/227), for a total of 21 cases (Table ). The median case number (interquartile range [IQR]) of confirmed COVID‐19 autopsy at these 10 facilities was 1 (1–2.75) during the first year of the pandemic. Of these cases, 8 were full‐body autopsies (including craniotomy), 12 were torso (thorax and abdomen)‐only autopsies, and one case was a thorax‐only autopsy. There were no cases of abdomen‐only autopsies, cranium‐only autopsies, or autopsies at other dissection sites. Notably, confirmed COVID‐19 cases did not allow to be subjected to autopsy in 180 facilities (79%, 180/227) (Table ). Among these 180 facilities, most facilities (46%, 104/227) did not allow the confirmed COVID‐19 autopsies due to inadequate infection control systems such as equipment in the autopsy room. Autopsies of suspected COVID‐19 cases without test confirmation by the time of autopsy were performed at 19 facilities (8.3%) for a total of 55 cases (Table ). The median case number (IQR) of suspected COVID‐19 autopsy in these 19 facilities was 2. , , , Of these cases, 24 were full‐body autopsies (including craniotomy), and 31 were torso (thorax and abdomen)‐only autopsies. There were no cases of thorax‐only, abdomen‐only, cranium‐only autopsies, or autopsies of other specific anatomical sites. Then, all 227 facilities responded about the decision‐making algorithm for conducting autopsies of suspected COVID‐19 cases without test confirmation of SARS‐CoV‐2 infection before their decease (Table ). These cases were not allowed to be subjected to autopsy in 110 facilities (49%). By contrast, these cases were allowed to be subjected to autopsy with negative pre‐autopsy SARS‐CoV‐2 RNA or antigens test results in 88 facilities (39%), and without a pre‐autopsy test in four facilities (1.8%). No specific decision‐making algorithm for conducting autopsies of suspected COVID‐19 cases was provided in 25 facilities (11%). For a pre‐autopsy test, SARS‐CoV‐2 RNA PCR tests or SARS‐CoV‐2 antigen rapid diagnostic tests for suspected cases were used in 67 (76%) or 19 (22%) facilities, respectively. For the handling of suspected COVID‐19 cases, the criteria for defining a suspected COVID‐19 case are important. We received responses from 100 facilities on how to define cases where COVID‐19 had not been diagnosed at the time of autopsy as suspected COVID‐19 cases at each facility (Table ). In each facility, suspected COVID‐19 cases were defined as follows (with some overlaps): defined based on clinical findings such as fever, respiratory symptoms, pneumonia, taste/smell disturbance, and gastrointestinal symptoms (87, 87%), defined based on epidemiological links to confirmed COVID‐19 cases such as “COVID‐19 close contact” (25, 25%), all deceased patients were defined (14, 14%), defined based on unknown medical history (5, 5%). Additionally, in four facilities (4%), cases with fever symptoms with or without respiratory symptoms were classified as suspected COVID‐19 cases. Autopsy status of non‐COVID‐19 patients A total of 21 confirmed, and 55 suspected COVID‐19 autopsies were performed at 227 institutions during the first year of the pandemic (Table ), but this result alone does not allow us to assess the impact of the COVID‐19 pandemic on overall pathological autopsy practices. Therefore, we also investigated the status of non‐COVID‐19 autopsies during the study period (April 2020–January 2021). The average number of autopsies per year in the pre‐pandemic period was obtained for all 227 facilities, and for 226 facilities, the total number of autopsies of patients without suspected COVID‐19 from April 7, 2020, to the date of response was also obtained. The mean number of autopsies of non‐COVID‐19 patients per month at each facility during the pandemic period was found to decrease significantly (1.7‐fold decline, about 60% reduction) compared to the pre‐pandemic period (Figure ). Notably, there was no clear difference in the extent of the reduction in the number of non‐COVID‐19 autopsies in facilities that did not permit all suspected COVID‐19 autopsies and those that performed autopsies only after confirming a SARS‐CoV‐2 negative test (Figure ). This suggests that differences in decision‐making algorithms for performing suspected COVID‐19 autopsies did not affect the reduction in the number of non‐COVID‐19 autopsies. On the other hand, large facilities with more than 500 beds showed a larger decrease in the number of autopsies than those with fewer than 500 beds (Figure ), indicating that larger facilities with higher numbers of autopsies normally are more severely affected during the pandemic. PPE at autopsy during COVID‐19 pandemic The COVID‐19 pandemic has affected not only the autopsies of COVID‐19 cases but also the entire practice of pathological autopsies. Since the most important difference in the autopsy practices among confirmed COVID‐19, suspected COVID‐19, and non‐COVID‐19 cases were thought to be about the PPE used, the general policy regarding the PPE use at autopsy of non‐COVID‐19 cases was evaluated compared to confirmed and suspected COVID‐19 cases. Notably, in 8 (4.5%) out of 178 facilities, they would use the maximum level of PPE for non‐COVID‐19 autopsies, equivalent to that used at autopsy in confirmed COVID‐19 cases. For non‐COVID‐19 autopsies, N95 respirators were used or considered for use in 79 (50%) out of 158 facilities, and protective clothing covering the whole body (e.g., Tyvek suit) was used or considered for use in 4 (2.5%) out of 158 facilities (Table ). For suspected COVID‐19 autopsies, N95 respirators were used or considered for use in 32 (73%) out of 44 facilities, and protective clothing covering the entire body was used or considered for use in 10 (23%) out of 44 facilities (Table ). For cases in which COVID‐19 was confirmed by the time of autopsy, N95 respirators were used or considered for use in 34 (94%) out of 36 facilities, and protective clothing covering the entire body was used or considered for use in 21 (58%) out of 36 facilities (Table ). In addition, in 13 out of 44 facilities (30%), they would use the same PPE for suspected COVID‐19 autopsies as for confirmed COVID‐19 autopsies. Of the facilities that did not list N95 respirators, one facility listed surgical masks and another listed Powered Air Purifying Respirators (PAPR). 

We sent e‐mails requesting survey completion to 678 medical facilities in Japan, 227 (34%) of which responded. Of the hospitals that responded, 13 facilities (5.7%) had 199 or fewer beds, 70 (31%) had 200–399 beds, and 144 (63%) had 400 beds or more. Among them, 197 facilities (87%) accepted COVID‐19 patients for hospitalization and 71 (31%) answered that they had experienced the death of COVID‐19 patients (Table ). In order to understand the actual status of pathological autopsy practices involving non‐COVID‐19 cases during the early phase of the pandemic, we classified patient cadavers that were candidates for pathological autopsy into confirmed COVID‐19, suspected COVID‐19, and non‐COVID‐19 cases, and investigated procedures for each case at each medical facility. Of all 227 facilities that responded, autopsies of patients with a confirmed diagnosis of COVID‐19 at the time of the autopsy were performed in 10 facilities (4.4%, 10/227), for a total of 21 cases (Table ). The median case number (interquartile range [IQR]) of confirmed COVID‐19 autopsy at these 10 facilities was 1 (1–2.75) during the first year of the pandemic. Of these cases, 8 were full‐body autopsies (including craniotomy), 12 were torso (thorax and abdomen)‐only autopsies, and one case was a thorax‐only autopsy. There were no cases of abdomen‐only autopsies, cranium‐only autopsies, or autopsies at other dissection sites. Notably, confirmed COVID‐19 cases did not allow to be subjected to autopsy in 180 facilities (79%, 180/227) (Table ). Among these 180 facilities, most facilities (46%, 104/227) did not allow the confirmed COVID‐19 autopsies due to inadequate infection control systems such as equipment in the autopsy room. Autopsies of suspected COVID‐19 cases without test confirmation by the time of autopsy were performed at 19 facilities (8.3%) for a total of 55 cases (Table ). The median case number (IQR) of suspected COVID‐19 autopsy in these 19 facilities was 2. , , , Of these cases, 24 were full‐body autopsies (including craniotomy), and 31 were torso (thorax and abdomen)‐only autopsies. There were no cases of thorax‐only, abdomen‐only, cranium‐only autopsies, or autopsies of other specific anatomical sites. Then, all 227 facilities responded about the decision‐making algorithm for conducting autopsies of suspected COVID‐19 cases without test confirmation of SARS‐CoV‐2 infection before their decease (Table ). These cases were not allowed to be subjected to autopsy in 110 facilities (49%). By contrast, these cases were allowed to be subjected to autopsy with negative pre‐autopsy SARS‐CoV‐2 RNA or antigens test results in 88 facilities (39%), and without a pre‐autopsy test in four facilities (1.8%). No specific decision‐making algorithm for conducting autopsies of suspected COVID‐19 cases was provided in 25 facilities (11%). For a pre‐autopsy test, SARS‐CoV‐2 RNA PCR tests or SARS‐CoV‐2 antigen rapid diagnostic tests for suspected cases were used in 67 (76%) or 19 (22%) facilities, respectively. For the handling of suspected COVID‐19 cases, the criteria for defining a suspected COVID‐19 case are important. We received responses from 100 facilities on how to define cases where COVID‐19 had not been diagnosed at the time of autopsy as suspected COVID‐19 cases at each facility (Table ). In each facility, suspected COVID‐19 cases were defined as follows (with some overlaps): defined based on clinical findings such as fever, respiratory symptoms, pneumonia, taste/smell disturbance, and gastrointestinal symptoms (87, 87%), defined based on epidemiological links to confirmed COVID‐19 cases such as “COVID‐19 close contact” (25, 25%), all deceased patients were defined (14, 14%), defined based on unknown medical history (5, 5%). Additionally, in four facilities (4%), cases with fever symptoms with or without respiratory symptoms were classified as suspected COVID‐19 cases. 

A total of 21 confirmed, and 55 suspected COVID‐19 autopsies were performed at 227 institutions during the first year of the pandemic (Table ), but this result alone does not allow us to assess the impact of the COVID‐19 pandemic on overall pathological autopsy practices. Therefore, we also investigated the status of non‐COVID‐19 autopsies during the study period (April 2020–January 2021). The average number of autopsies per year in the pre‐pandemic period was obtained for all 227 facilities, and for 226 facilities, the total number of autopsies of patients without suspected COVID‐19 from April 7, 2020, to the date of response was also obtained. The mean number of autopsies of non‐COVID‐19 patients per month at each facility during the pandemic period was found to decrease significantly (1.7‐fold decline, about 60% reduction) compared to the pre‐pandemic period (Figure ). Notably, there was no clear difference in the extent of the reduction in the number of non‐COVID‐19 autopsies in facilities that did not permit all suspected COVID‐19 autopsies and those that performed autopsies only after confirming a SARS‐CoV‐2 negative test (Figure ). This suggests that differences in decision‐making algorithms for performing suspected COVID‐19 autopsies did not affect the reduction in the number of non‐COVID‐19 autopsies. On the other hand, large facilities with more than 500 beds showed a larger decrease in the number of autopsies than those with fewer than 500 beds (Figure ), indicating that larger facilities with higher numbers of autopsies normally are more severely affected during the pandemic. 

The COVID‐19 pandemic has affected not only the autopsies of COVID‐19 cases but also the entire practice of pathological autopsies. Since the most important difference in the autopsy practices among confirmed COVID‐19, suspected COVID‐19, and non‐COVID‐19 cases were thought to be about the PPE used, the general policy regarding the PPE use at autopsy of non‐COVID‐19 cases was evaluated compared to confirmed and suspected COVID‐19 cases. Notably, in 8 (4.5%) out of 178 facilities, they would use the maximum level of PPE for non‐COVID‐19 autopsies, equivalent to that used at autopsy in confirmed COVID‐19 cases. For non‐COVID‐19 autopsies, N95 respirators were used or considered for use in 79 (50%) out of 158 facilities, and protective clothing covering the whole body (e.g., Tyvek suit) was used or considered for use in 4 (2.5%) out of 158 facilities (Table ). For suspected COVID‐19 autopsies, N95 respirators were used or considered for use in 32 (73%) out of 44 facilities, and protective clothing covering the entire body was used or considered for use in 10 (23%) out of 44 facilities (Table ). For cases in which COVID‐19 was confirmed by the time of autopsy, N95 respirators were used or considered for use in 34 (94%) out of 36 facilities, and protective clothing covering the entire body was used or considered for use in 21 (58%) out of 36 facilities (Table ). In addition, in 13 out of 44 facilities (30%), they would use the same PPE for suspected COVID‐19 autopsies as for confirmed COVID‐19 autopsies. Of the facilities that did not list N95 respirators, one facility listed surgical masks and another listed Powered Air Purifying Respirators (PAPR). 

Our study revealed the actual situation of pathological autopsy practices during the COVID‐19 pandemic at 227 medical facilities in Japan. The number of confirmed and suspected COVID‐19 autopsies was limited to 76; notably, a significant decrease was observed even in the number of the non‐COVID‐19 autopsy. In many facilities, patients with clinical symptoms consistent as COVID‐19 were managed as suspected COVID‐19 cases when the SARS‐CoV‐2 test was not performed prior to death, and autopsies of those cases were avoided in about half of the facilities. In addition, confirmed COVID‐19 cases were not permitted to be subjected to autopsy due to inadequate infection control equipment in about 90% of facilities without experience with confirmed COVID‐19 autopsies. These findings suggested that pathological autopsies of cases with confirmed or possible SARS‐CoV‐2 infection were avoided at many facilities due to inadequate autopsy room equipment. The importance of autopsies for COVID‐19 cases has been strongly recognized worldwide. In February 2020, the first autopsy report of a COVID‐19 patient was issued in China, and many autopsies have since been performed in other countries. While there have been several reports of autopsy series exceeding 20 cases from the early stage of the pandemic, , , including 80 autopsy reports in Hamburg, only 21 autopsies of COVID‐19 cases from 10 facilities in Japan were identified in this study. In the majority of the facilities in our study, deceased cases with typical symptoms including fever and respiratory symptoms were treated as suspected COVID‐19 cases. In addition, some facilities managed all deathswithout SARS‐CoV‐2 test positive prior to death as suspected COVID‐19 cases, which may have made it particularly difficult to perform autopsies. Although difficulties and restrictions in conducting autopsies of COVID‐19 cases due to lack of material and human resources have been reported, there have been no reports about the impact of the pandemic on the overall number of pathological autopsies, including non‐COVID‐19 cases. While the COVID‐19 pandemic has affected the diagnosis and treatment of a variety of other diseases in clinical practice, , our study revealed that pathological autopsy practices on non‐COVID‐19 cases have been also affected by the pandemic. There were some differences in PPE used for the autopsy practices among confirmed COVID‐19, suspected COVID‐19, and non‐COVID‐19 cases. Notably, as the probability of SARS‐CoV‐2 infection in deceased patients decreases, the number of facilities utilizing N95 respirators and full‐body protective clothing has decreased. However, several facilities used the same PPE at autopsies for non‐COVID‐19 and suspected COVID‐19 cases as for confirmed COVID‐19 cases. In addition, suspected COVID‐19 cases were subjected to autopsy only after confirmation of negative SARS‐CoV‐2 test results prior to autopsy in many facilities. While seroprevalence was only about 1%–2%, even in Tokyo, where the COVID‐19 case notification rate had been one of the highest during the first year of the pandemic. Taken together, these suggest that even in situations where the probability of SARS‐CoV‐2 infection in decedents is considered very low, substantial resources were devoted to preventing SARS‐CoV‐2 infection from autopsy practices at many medical facilities, which may have resulted in a decrease in the number of autopsies of non‐COVID‐19 cases in Japan. This study has several limitations. First, this survey could not obtain responses from all facilities conducting pathological autopsies; thus, some autopsies, particularly those of confirmed COVID‐19 cases, could not be captured. Second, some questions were not answered by all facilities that responded to the survey. To capture the complexity of each facility, the questionnaire has an open‐ended format, which is may have resulted in missing data. Third, it should also be noted that since the survey was about the situation in the early stage of the pandemic, before effective treatments, vaccines, and other medical countermeasures were available, some facilities may have changed their policies over the course of the pandemic. However, the evaluation of pathological autopsy practices in Japan at the time of an emerging infectious disease crisis, for which no effective medical countermeasure exists, yields valuable findings for optimizing infection prevention and control strategies in pathological autopsies. In conclusion, the COVID‐19 pandemic affected pathological autopsies generally, even in cases that weren't COVID‐19 cases. Although autopsies are on the decline worldwide, they are useful in evaluating the cause of death and in elucidating the pathogenesis of infectious diseases. Therefore, we need to ensure that autopsies are not impeded during emerging infectious disease pandemics. To maintain overall pathological autopsy activity during a pandemic, it is desirable to develop the human and material resources essential for a system to conduct pathological autopsies during emerging infectious diseases pandemic under the non‐pandemic phase. The aversion to performing autopsies due to the presence of infectious diseases should also be removed by improving education on pathological autopsy protocols with infectious diseases in mind, such as the selection and use of PPE, and by proposing decision‐making algorithms that do not impede the performance of autopsies. In order to see the effect of these efforts, we suggest that surveys such as this report should be continued in the future. 

The author contributions of this study are as follows. Conception and design, conducting the survey; TS, SA and HS. Analysis of data; YH, SI and TS. Drafting the manuscript or figures: YH, SI and TS. Final approval of manuscript: All authors. 

None declared. 

