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Preplanned Studies: Mushroom Poisoning Outbreaks — China, 2019

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  • Summary

    What is already known about this topic?

    Mushroom poisoning is becoming one of the most serious food safety issues in China, which is responsible for nearly a half of all oral poisoning deaths.

    What is added by this report?

    In China, many mushrooms were previously “recorded” as poisonous. In this study, about 70 species obtained from mushroom poisoning incidents including several new records were confirmed accurately by morphological and molecular evidence in 2019, and spatial and temporal distribution characters of 13 lethal mushrooms were summarized systematically.

    What are the implications for public health practice?

    Precise and timely species identification is of pivotal importance in mushroom incidents. More efforts and cooperation are continued to be needed urgently for the governments, CDC staff, doctors and mycologists in future.

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  • The median number of cases was two.
    Supplementary Table S1 (available in http://weekly.chinacdc.cn) summarized their spatial and temporal distribution.
  • [1] Wu F, Zhou LW, Yang ZL, Bau T, Li TH, Dai YC. Resource diversity of Chinese macrofungi: edible, medicinal and poisonous species. Fungal Divers 2019;98:1 − 76. http://dx.doi.org/10.1007/s13225-019-00432-7CrossRef
    [2] White J, Weinstein SA, de Haro L, Bédry R, Schaper A, Rumack BH, et al. Mushroom poisoning: a proposed new clinical classification. Toxicon 2019;157:53 − 65. http://dx.doi.org/10.1016/j.toxicon.2018.11.007CrossRef
    [3] Zhou J, Yuan Y, Lang N, Yin Y, Sun CY. Analysis of hazard in mushroom poisoning incidents in China mainland. Chin J Emerg Med 2016;25(6):724 − 8. http://dx.doi.org/10.3760/cma.j.issn.1671-0282.2016.06.008 (In Chinese)CrossRef
    [4] Dadpour B, Tajoddini S, Rajabi M, Afshari R. Mushroom poisoning in the northeast of Iran; a retrospective 6-year epidemiologic study. Emergency 2017;5(1):e23. http://dx.doi.org/10.22037/emergency.v5i1.13607CrossRef
    [5] Diaz JH. Evolving global epidemiology, syndromic classification, general management, and prevention of unknown mushroom poisonings. Crit Care Med 2005;33(2):419 − 26. http://dx.doi.org/10.1097/01.CCM.0000153530.32162.B7CrossRef
    [6] Chen ZH, Yang ZL, Bau T, Li TH. Poisonous mushrooms: recognition and poisoning treatment. Beijing: Science Press. 2016. (In Chinese).
    [7] Guzmán G, Ramírez Guillén F, Hyde KD, Karunarathna SC. Psilocybe s.s. in Thailand: four new species and a review of previously recorded species. Mycotaxon 2012;119:65 − 81. http://dx.doi.org/10.5248/119.65CrossRef
    [8] Yang ZL. Atlas of the Chinese species of Amanitaceae. Beijing: Science Press. 2015. (In Chinese).
    [9] Cui YY, Cai Q, Tang LP, Liu JW, Yang ZL. The family Amanitaceae: molecular phylogeny, higher-rank taxonomy and the species in China. Fungal Divers 2018;91:5 − 230. http://dx.doi.org/10.1007/s13225-018-0405-9CrossRef
    [10] Li CR, Hywel-Jones N, Cao YP, Nam S, Li ZZ. Tolypocladium dujiaolongae sp. nov. and its allies. Mycotaxon 2018;133(2):229 − 41. http://dx.doi.org/10.5248/133.229CrossRef
    [11] Bau T, Zhang H. Strophariaceae of China (VI): Galerina. J Fungal Res 2012; 10(2): 72 − 96. http://mall.cnki.net/onlineview/MagaView.aspx?fn=yjjw201202*1*. (In Chinese).http://mall.cnki.net/onlineview/MagaView.aspx?fn=yjjw201202*1*
    [12] Yang ZL. Flora fungorum sinicorum. Vol. 52. Fungi lepiotoidei (Agaricaceae). Beijing: Science Press. 2019. (In Chinese).
    [13] Zhang YZ, Zhang KP, Zhang HS, Sun J, Yin Y, Li HJ, et al. Lepiota subvenenata (Agaricaceae, Basidiomycota), a new poisonous species from southwestern China. Phytotaxa 2019;400(5):265 − 72. http://dx.doi.org/10.11646/phytotaxa.400.5.2CrossRef
    [14] Li GJ. The taxonomy of Russula in China. Beijing: University of Chinese Academy of Science; 2013. http://www.wanfangdata.com.cn/details/detail.do?_type=degree&id=Y2746994. (In Chinese).http://www.wanfangdata.com.cn/details/detail.do?_type=degree&id=Y2746994
    [15] Cervellin G, Comelli I, Rastelli G, Sanchis-Gomar F, Negri F, de Luca C, et al. Epidemiology and clinics of mushroom poisoning in Northern Italy: a 21-year retrospective analysis. Hum Exp Toxicol 2018;37(7):697 − 703. http://dx.doi.org/10.1177/0960327117730882CrossRef
  • FIGURE 1.  Monthly distribution of mushroom poisoning in China, 2019.

    TABLE 1.  Toxic mushroom species causing poisoning incidents in China, 2019

    Mushroom speciesNumber of incidentsNumber of patientsDeathsMortality (%)
    Acute liver failure
     Amanita exitialis8251352.00
     Amanita fuliginea4900
     Amanita cf. fuliginea25120.00
     Amanita fuliginea or Amanita rimosa41417.14
     Amanita pallidorosea49111.11
     Amanita rimosa2400
     Amanita subjunquillea1300
     Amanita subpallidorosea711327.27
     Galerina sulciceps49111.11
     Lepiota brunneoincarnata51100
    Rhabdomyolysis
     Russula subnigricans155411.85
    Acute renal failure
     Amanita neoovoidea1200
     Amanita oberwinklerana91800
     Amanita pseudoporphyria1300
    Gastroenteritis
     Agaricus cf. arvensis*1100
     Agaricus subrufescens*1400
     Other Agaricus spp.41000
     Baorangia pseudocalopus2200
     Chlorophyllum globosum2800
     Chlorophyllum hortense1100
     Chlorophyllum molybdites5412600
     Chlorophyllum molybdites and Chlorophyllum hortense1700
     Entoloma omiense83100
     Entoloma quadratum1200
     Entoloma strictius1200
     Entoloma sp.1300
     Gerhardtia sinensis2600
     Lactarius atrobrunneus1100
     Lactarius torminosus and Megacollybia clitocyboidea1400
     Lactifluus vellereus1700
     Omphalotus guepiniformis31900
     Porphyrellus cf. holophaeus1200
     Russula cf. emetica1300
     Russula foetens3800
     Russula grata1200
     Russula illota and Entoloma cf. abortivum1200
     Russula japonica266800
     Russula cf. japonica104300
     Russula japonica and Amanita sepiacea1300
     Russula japonica and Entoloma omiense1100
     Russula japonica and Russula foetens3700
     Russula sp.1400
     Scleroderma cepa4800
     Scleroderma sp.1100
     Suillus pictus1500
     Sutorius flavidus1100
     Sutorius sp.1300
     Tricholoma terreum*3600
     Tylopilus neofelleus1100
    Psycho-neurological disorder
     Amanita concentrica4600
     Amanita melleiceps1500
     Amanita rufoferruginea24125.00
     Amanita subglobosa31000
     Amanita cf. subglobosa1200
     Amanita cf. virgineoides1100
     Boletus cf. bicolor1900
     Butyriboletus roseoflavus1700
     Clitocybe sp.41400
     Gymnopilus dilepis2300
     Gymnopilus lepidotus1100
     Gymnopilus sp.2200
     Inocybe rimosa2400
     Inocybe serotina 1200
     Inocybe squarrosolutea1100
     Panaeolus fimicola and Conocybe sp.1200
     Psilocybe cubensis1500
     Psilocybe cubensis and Panaeolus papilionaceus1600
     Psilocybe samuiensis2700
     Psilocybe thaiaerugineomaculans1400
    Photosensitive dermatitis
     Cordierites frondosus2300
    Unclassified
     Amanita citrinoannulata1400
     Amanita clarisquamosa1300
     Amanita fritillaria2800
     Amanita hamadae1100
     Lepista sordida*1100
     Macrocybe gigantea*1100
     Scleroderma yunnanense*1100
     Tolypocladium dujiaolongae*3900
     Other mushrooms124600
    * Species recorded as edible mushrooms.
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    沈阳化工大学材料科学与工程学院 沈阳 110142

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Mushroom Poisoning Outbreaks — China, 2019

View author affiliation

Summary

What is already known about this topic?

Mushroom poisoning is becoming one of the most serious food safety issues in China, which is responsible for nearly a half of all oral poisoning deaths.

What is added by this report?

In China, many mushrooms were previously “recorded” as poisonous. In this study, about 70 species obtained from mushroom poisoning incidents including several new records were confirmed accurately by morphological and molecular evidence in 2019, and spatial and temporal distribution characters of 13 lethal mushrooms were summarized systematically.

What are the implications for public health practice?

Precise and timely species identification is of pivotal importance in mushroom incidents. More efforts and cooperation are continued to be needed urgently for the governments, CDC staff, doctors and mycologists in future.

  • 1. National Institute of Occupational Health and Poison Control, Chinese Center for Disease Control and Prevention, Beijing, China
  • Corresponding author:

    Chengye Sun, suncy@chinacdc.cn

    doi: 10.46234/ccdcw2020.005
  • Macrofungi, commonly known as mushrooms, are important sources of foods and medicines especially in China (1). But with the utilization of wild edible and medicinal mushrooms, many poisoning incidents occur every year. At least 100 estimated people die every year worldwide, which is likely underestimated given the approximate 50–100 deaths separately reported each year in both Europe and China (2-5). Mushroom poisoning is a major cause of death by oral poisoning in China and is characterized by typical space-time clustering (in South areas of China, from summer to autumn), high mortality (about 20%), and high risk to farmers (3,6). After mushroom poisoning events, mushroom poisoning information is systematically collected by a technical support network including professional staff of CDC, doctors and mycologists, and an epidemiological investigation is immediately conducted. In 2019, 276 independent mushroom poisoning incidents from 17 provinces involving 769 patients and 22 deaths were investigated and the overall mortality was 2.86%.

    Currently, 480 varieties of poisonous mushrooms have been recorded in China (1) that result in seven different kinds of clinical syndromes including acute liver failure, acute renal failure, rhabdomyolysis, gastroenteritis, psycho-neurological disorder, hemolysis, and photosensitive dermatitis (2,6). Among these clinical syndromes, poisonous mushrooms resulting in acute liver failure and rhabdomyolysis are responsible for almost all deaths.

    Information from epidemiological investigations was systematically recorded and analyzed, and the information focused primarily on location, poisoning time, incubation, complaints, number of patients and deaths, mushroom species, method of acquisition (including self-harvested, market purchase), and syndromic classification. The patients’ number of a few incidents resulting gastroenteritis or psycho-neurological disorder were not accurately obtained, they were treated as one patient for each incident. Following poisoning events, mushroom specimens were obtained by local CDC, China CDC, or hospital professionals from the venue where the mushrooms were consumed or from the field and confirmed by the patients. Almost all specimens were processed and deposited in the National Institute of Occupational Health and Poison Control (NIOHPC) of China CDC. Some were also deposited in Cryptogamic Herbarium of Kunming Institute of Botany, Chinese Academy of Sciences (HKAS), Herbarium of College of Life Sciences, Hunan Normal University (MHHNU), and other local CDCs. All mushroom specimens were identified by morphological and molecular analyses, DNA gene fragment internal transcribed spacer (ITS) was selected for species recognition. Related clinical symptoms data were summarized from the hospital records.

    In 2019, a total of 276 independent mushroom poisoning incidents from 17 provinces involving 769 patients and 22 deaths were investigated and the overall mortality was 2.86%. Among them, the mushroom species could accurately be identified in 264 incidents (95.65%). There were 26 patients from 9 incidents with 1 death who had eaten poisonous mushrooms purchased from market. Ten patients from five incidents had been poisoned after eating dried Russula spp. or boletes. Patients from 33 incidents had consumed mixed wild mushrooms. Mushroom poisoning happened every month all year round and centered from June to October with its peak in July, which involved 85 incidents including 200 patients and 4 deaths (Figure 1).

    Figure 1.  Monthly distribution of mushroom poisoning in China, 2019.

    In terms of geographical distribution, the provincial-level administrative division with the most incidents was Hunan, which involved 77 incidents and 221 patients, followed by Yunnan, Zhejiang, Guizhou, and Chongqing. The number of incidents and patients in the top 5 provinces accounted for more than 80% of the total (82.61% and 80.49%) and 95.45% (21/22) of the total death toll. The number of cases ranged from 1 to 23, and 6 outbreaks involved more than 10 patients. Yunnan had 14 patients die after eating poisonous mushrooms, followed by Guizhou (5 deaths), Zhejiang (2 deaths), and Sichuan (1 death).

    In addition, There were 12 patients from Burma who had been involved in 3 incidents with 6 deaths. There was one patient who had eaten Chlorophyllum molybdites, which causes gastroenteritis, four patients who had consumed Psilocybe thaiaerugineomaculans, which leads to hallucinations, and the other seven patients had eaten the lethal mushroom Amanita exitialis.

    About 70 species of poisonous mushroom causing 6 different kinds of clinical syndromes were successfully identified by morphological and molecular studies (Table 1). Seven species (Entoloma strictius, Gymnopilus lepidotus, Inocybe serotina, I. squarrosolutea, Lactarius atrobrunneus, Lactifluus vellereus, and Psilocybe thaiaerugineomaculans) were newly recorded as poisonous mushrooms in 2019 and were added to the Chinese poisonous mushroom list. This is the first report of I. serotina and P. thaiaerugineomaculans in China. Gerhardtia sinensis and Tolypocladium dujiaolongae were treated as highly suspected poisonous species and further investigations will be continued to certify their edibility or toxicity.

    Mushroom speciesNumber of incidentsNumber of patientsDeathsMortality (%)
    Acute liver failure
     Amanita exitialis8251352.00
     Amanita fuliginea4900
     Amanita cf. fuliginea25120.00
     Amanita fuliginea or Amanita rimosa41417.14
     Amanita pallidorosea49111.11
     Amanita rimosa2400
     Amanita subjunquillea1300
     Amanita subpallidorosea711327.27
     Galerina sulciceps49111.11
     Lepiota brunneoincarnata51100
    Rhabdomyolysis
     Russula subnigricans155411.85
    Acute renal failure
     Amanita neoovoidea1200
     Amanita oberwinklerana91800
     Amanita pseudoporphyria1300
    Gastroenteritis
     Agaricus cf. arvensis*1100
     Agaricus subrufescens*1400
     Other Agaricus spp.41000
     Baorangia pseudocalopus2200
     Chlorophyllum globosum2800
     Chlorophyllum hortense1100
     Chlorophyllum molybdites5412600
     Chlorophyllum molybdites and Chlorophyllum hortense1700
     Entoloma omiense83100
     Entoloma quadratum1200
     Entoloma strictius1200
     Entoloma sp.1300
     Gerhardtia sinensis2600
     Lactarius atrobrunneus1100
     Lactarius torminosus and Megacollybia clitocyboidea1400
     Lactifluus vellereus1700
     Omphalotus guepiniformis31900
     Porphyrellus cf. holophaeus1200
     Russula cf. emetica1300
     Russula foetens3800
     Russula grata1200
     Russula illota and Entoloma cf. abortivum1200
     Russula japonica266800
     Russula cf. japonica104300
     Russula japonica and Amanita sepiacea1300
     Russula japonica and Entoloma omiense1100
     Russula japonica and Russula foetens3700
     Russula sp.1400
     Scleroderma cepa4800
     Scleroderma sp.1100
     Suillus pictus1500
     Sutorius flavidus1100
     Sutorius sp.1300
     Tricholoma terreum*3600
     Tylopilus neofelleus1100
    Psycho-neurological disorder
     Amanita concentrica4600
     Amanita melleiceps1500
     Amanita rufoferruginea24125.00
     Amanita subglobosa31000
     Amanita cf. subglobosa1200
     Amanita cf. virgineoides1100
     Boletus cf. bicolor1900
     Butyriboletus roseoflavus1700
     Clitocybe sp.41400
     Gymnopilus dilepis2300
     Gymnopilus lepidotus1100
     Gymnopilus sp.2200
     Inocybe rimosa2400
     Inocybe serotina 1200
     Inocybe squarrosolutea1100
     Panaeolus fimicola and Conocybe sp.1200
     Psilocybe cubensis1500
     Psilocybe cubensis and Panaeolus papilionaceus1600
     Psilocybe samuiensis2700
     Psilocybe thaiaerugineomaculans1400
    Photosensitive dermatitis
     Cordierites frondosus2300
    Unclassified
     Amanita citrinoannulata1400
     Amanita clarisquamosa1300
     Amanita fritillaria2800
     Amanita hamadae1100
     Lepista sordida*1100
     Macrocybe gigantea*1100
     Scleroderma yunnanense*1100
     Tolypocladium dujiaolongae*3900
     Other mushrooms124600
    * Species recorded as edible mushrooms.

    Table 1.  Toxic mushroom species causing poisoning incidents in China, 2019

    Nine species (A. exitialis, A. fuliginea, A. cf. fuliginea, A. pallidorosea, A. rimosa, A. subjunquillea, A. subpallidorosea, Galerina sulciceps, and Lepiota brunneoincarnata) causing acute liver failure resulted in 41 incidents involving 100 patients and 20 deaths and thus, A. exitialis had been recognized as the most dangerous mushroom in 2019 (Table 1). Russula subnigricans which leads to rhabdomyolysis resulted in 15 incidents involving 54 patients and 1 death (Table 1). Three species (A. neoovoidea, A. oberwinklerana, and A. pseudoporphyria) from the genus Amanita causing acute renal failure were identified, leading to 11 incidents involving 23 patients and no deaths (Table 1). As almost all deaths for mushroom poisoning were attributed to acute liver failure, rhabdomyolysis, and acute renal failure, and these species have drawn the most attention and been regarded as the most dangerous mushrooms.

    As displayed in Table 1, about 30 species causing gastroenteritis were identified. Chlorophyllum molybdites is the most common poisonous mushroom followed by Russula japonica, Russula cf. japonica, and Entoloma omiense. This study also confirmed that several recorded poisonous mushrooms were involved in poisoning incidents including Entoloma quadratum, E. strictius, Lactarius atrobrunneus, L. torminosus, Lactifluus vellereus, Megacollybia clitocyboidea, and Suillus pictus.

    The 18 species from 8 genera causing psycho-neurological disorder were also identified (Table 1). Amanita concentrica, Gymnopilus lepidotus, Inocybe serotina, I. squarrosolutea and P. thaiaerugineomaculans were confirmed involving in poisoning incidents in China. Inocybe serotina and P. thaiaerugineomaculans were the first time recorded in China (7). Cordierites frondosus appeared from Yunnan and Guizhou provinces resulted in 2 incidents with photosensitive dermatitis.

    The 8 species resulting in 11 incidents had been still not clear about their clinical classification (Table 1). Amanita clarisquamosa and A. fritillaria were previously recorded as poisonous mushrooms although their clinical classification remains poorly understood (1). Moreover, toxicity of Amanita citrinoannulata and A. hamadae had been not recorded (1,8-9). Lepista sordida and Macrocybe gigantea were deemed as edible mushrooms, but two people ate these two mushrooms and then exhibited gastrointestinal symptoms, which indicated that some edible mushrooms are toxic to some humans in certain circumstances (1). Tolypocladium dujiaolongae, a new species seen in China, was used as medicine (10), and nine patients from three independent incidents after eating this species showed gastrointestinal and psycho-neurological disorder symptoms. In one incident from Yunnan, left-over mushroom samples were identified as Scleroderma yunnanense, which is edible and often consumed in large quantities by local residents. This may possibly be due to a mixture of Scleroderma mushrooms being sold in the market and real poisonous mushroom samples not being obtained.

  • Mushroom poisoning is becoming one of the most serious food safety issues in China. Mushroom poisonings are reported every month and concentrated from summer to autumn peaking in July. Southwestern and Central China are the most seriously affected areas, followed by Eastern and Southern China with noticeably lower levels in Northern, Northeastern and Northwestern China. Notably, Zhejiang in Eastern China has been viewed as the region with the fastest growing threat. About 70 species, including 7 newly recorded species causing 6 different clinical syndromes, were successfully confirmed. This study accumulated first-hand information of mushroom poisoning, which is considerably valuable for mushroom poisoning control, diagnosis, and treatments for patients and for popular science education for thousands of people who are potentially threatened by poisonous mushrooms.

    Most mushroom poisoning incidents have favorable outcomes, only presenting with gastrointestinal or psycho-neurological disorder complaints and needing symptomatic treatments. Almost all deaths were caused by lethal mushrooms companied by acute liver failure and rhabdomyolysis (6). Lethal mushroom species causing acute liver failure were mainly concentrated in the genera of Amanita, Galerina, and Lepiota (1,6). The 12 species from Amanita section Phaloideae were discovered in China (1,8-9), and 6 recorded species and 1 species currently identified as A. cf. fuliginea were involved in mushroom poisoning in 2019 (Table 1, Supplementary Table S1). The 14 poisonous Galerina species were recorded in China (1,11), and the most common species was G. sulciceps which caused 4 incidents in 2019 (Table 1, Supplementary Table S1). Eight poisonous Lepiota species were recorded in China (1,12-13), and the most common species was L. brunneoincarnata (Table 1, Supplementary Table S1). Russla subnigricans and Tricholoma equestre could cause rhabdomyolysis, and the former species is the most common resulting in at least 50 deaths in the last 2 decades in China (6,14).

    Accurate and timely species identification is of pivotal importance in mushroom incidents. Unfortunately, previous studies suggested that the rate of correct species identification in mushroom incidents was considerably low, between 5% and 27%, or even lower (15). Of the 212 reported incidents from 2010 to 2014 in China, the mushrooms were scientifically identified only in 2 incidents (3). In recent years, a large number of mycologists have begun participating in mushroom poisoning in China, which has greatly benefitted mushroom poisoning control. Beginning in 1996, a 24 hour/365 day on-call mycological service became available in northern Italy, which has helped with the identification of poisonous mushroom in 89.6% of incidents (15). A similar poisoning-counselling service (010-83132345) became available in China in 1999 and plays a crucial role in mushroom poisoning control.

    In Europe, mushroom poisoning risk dramatically increased and was ascribed to recent mass immigrations to Europe (2). Likewise, thousands of foreigners come to China every year and the three mushroom poisoning incidents involving Burmese people in 2019 drew attention to the need for targeted science and health education for foreigners in addition to local residents.

    The incidents investigated in this report only represent a portion of the variety of mushroom poisonings happening every year. More effort and continued cooperation are needed urgently from local and national governments, CDC staff, doctors, and mycologists to properly control mushroom poisoning events.

  • We gratefully acknowledge Profs. Zuohong Chen, Ping Zhang (Hunan Normal University); Drs. Xianghua Wang, Gang Wu, Hong Luo, Zaiwei Ge, Yanchun Li (Kunming Institute of Botany, Chinese Academy of Sciences); Profs. Taihui Li, Wangqiu Deng, Dr. Ming Zhang (Guangdong Institute of Microbiology); Prof. Tolgor Bau (Jilin Agricultural University); Prof. Junfeng Liang, Dr. Jie Song (Research Institute of Tropical Forestry, Chinese Academy of Forestry); Profs. Yucheng Dai, Baokai Cui, Shuanghui He (Beijing Forestry University, China); Dr. Chuanhua Li (Shanghai Academy of Agricultural Sciences); Profs. Haisheng Yuan, Yulian Wei (Institute of Applied Ecology, Chinese Academy of Sciences); Dr. Yuguang Fan (Hainan Medical University); Prof. Tiezhi Liu (Chifeng University); and Prof. Wenfei Lin (Zhejiang University) for species identification of poisonous mushrooms. Many people from CDC and hospitals are acknowledged for collecting specimens, and offering data on mushroom poisoning and clinical symptoms. Special thanks to Dr. Jing Si (Beijing Forestry University, China) for improving the manuscript. This study was supported by the National Science Foundation of China (No. 31501814). The study was approved by the National Institute of Occupational Health and Poison Control Ethics Committee, Chinese Center for Disease Control and Prevention (NIOHP201904).

  • The median number of cases was two.
    Supplementary Table S1 (available in http://weekly.chinacdc.cn) summarized their spatial and temporal distribution.
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