Mushroom Poisoning Outbreaks — China, 2019

Abstract

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.

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,^① 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.

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

Mushroom species	Number of incidents	Number of patients	Deaths	Mortality (%)
* Species recorded as edible mushrooms.
Acute liver failure
Amanita exitialis	8	25	13	52.00
Amanita fuliginea	4	9	0	0
Amanita cf. fuliginea	2	5	1	20.00
Amanita fuliginea or Amanita rimosa	4	14	1	7.14
Amanita pallidorosea	4	9	1	11.11
Amanita rimosa	2	4	0	0
Amanita subjunquillea	1	3	0	0
Amanita subpallidorosea	7	11	3	27.27
Galerina sulciceps	4	9	1	11.11
Lepiota brunneoincarnata	5	11	0	0
Rhabdomyolysis
Russula subnigricans	15	54	1	1.85
Acute renal failure
Amanita neoovoidea	1	2	0	0
Amanita oberwinklerana	9	18	0	0
Amanita pseudoporphyria	1	3	0	0
Gastroenteritis
Agaricus cf. arvensis*	1	1	0	0
Agaricus subrufescens *	1	4	0	0
Other Agaricus spp.	4	10	0	0
Baorangia pseudocalopus	2	2	0	0
Chlorophyllum globosum	2	8	0	0
Chlorophyllum hortense	1	1	0	0
Chlorophyllum molybdites	54	126	0	0
Chlorophyllum molybdites and Chlorophyllum hortense	1	7	0	0
Entoloma omiense	8	31	0	0
Entoloma quadratum	1	2	0	0
Entoloma strictius	1	2	0	0
Entoloma sp.	1	3	0	0
Gerhardtia sinensis	2	6	0	0
Lactarius atrobrunneus	1	1	0	0
Lactarius torminosus and Megacollybia clitocyboidea	1	4	0	0
Lactifluus vellereus	1	7	0	0
Omphalotus guepiniformis	3	19	0	0
Porphyrellus cf. holophaeus	1	2	0	0
Russula cf. emetica	1	3	0	0
Russula foetens	3	8	0	0
Russula grata	1	2	0	0
Russula illota and Entoloma cf. abortivum	1	2	0	0
Russula japonica	26	68	0	0
Russula cf. japonica	10	43	0	0
Russula japonica and Amanita sepiacea	1	3	0	0
Russula japonica and Entoloma omiense	1	1	0	0
Russula japonica and Russula foetens	3	7	0	0
Russula sp.	1	4	0	0
Scleroderma cepa	4	8	0	0
Scleroderma sp.	1	1	0	0
Suillus pictus	1	5	0	0
Sutorius flavidus	1	1	0	0
Sutorius sp.	1	3	0	0
Tricholoma terreum *	3	6	0	0
Tylopilus neofelleus	1	1	0	0
Psycho-neurological disorder
Amanita concentrica	4	6	0	0
Amanita melleiceps	1	5	0	0
Amanita rufoferruginea	2	4	1	25.00
Amanita subglobosa	3	10	0	0
Amanita cf. subglobosa	1	2	0	0
Amanita cf. virgineoides	1	1	0	0
Boletus cf. bicolor	1	9	0	0
Butyriboletus roseoflavus	1	7	0	0
Clitocybe sp.	4	14	0	0
Gymnopilus dilepis	2	3	0	0
Gymnopilus lepidotus	1	1	0	0
Gymnopilus sp.	2	2	0	0
Inocybe rimosa	2	4	0	0
Inocybe serotina	1	2	0	0
Inocybe squarrosolutea	1	1	0	0
Panaeolus fimicola and Conocybe sp.	1	2	0	0
Psilocybe cubensis	1	5	0	0
Psilocybe cubensis and Panaeolus papilionaceus	1	6	0	0
Psilocybe samuiensis	2	7	0	0
Psilocybe thaiaerugineomaculans	1	4	0	0
Photosensitive dermatitis
Cordierites frondosus	2	3	0	0
Unclassified
Amanita citrinoannulata	1	4	0	0
Amanita clarisquamosa	1	3	0	0
Amanita fritillaria	2	8	0	0
Amanita hamadae	1	1	0	0
Lepista sordida *	1	1	0	0
Macrocybe gigantea *	1	1	0	0
Scleroderma yunnanense *	1	1	0	0
Tolypocladium dujiaolongae *	3	9	0	0
Other mushrooms	12	46	0	0

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.^②

As displayed in Table 1, about 30 species causing gastroenteritis were identified. Chlorophyllum molybdites is the most common poisonous mushroom followed by Russula japonica, Russulacf. 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.

Discussion

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.