A. Kalashnikov1, N. Kurdil1, O. Lutsenko2, H. Voitenko1, А. Bohomol3
1 State Enterprise “L. I. Medved’s Research Center of Preventive Toxicology, Food and Chemical Safety”, Ministry of Health of Ukraine, Kyiv
2 Scientific Center of Radiation Medicine, Academy of Medical Sciences of Ukraine, Laboratory of Food Hygiene and Food Safety, Kyiv, Ukraine
3 Kiev City Clinical Hospital for Emergency Medicine, Toxicology Department Kyiv, Ukraine
ABSTRACT. Unsettling statistics of poisoning resulting from the use of wild-growing mushrooms necessitates a more detailed study of the life-threatening causes in human and determination of preventive measures.
Objective. Analysis of the structure, changes over time and causes of poisoning by wild-growing mushrooms among the population of Kyiv and the Region of Kyiv in recent years.
Materials and Methods. Cases of mushroom poisoning (ICD–T62.0) among the adult population of Kyiv; statistic data from the Ministry of Health of Ukraine, the State Emergency Service of Ukraine and the toxicological centre of the Kyiv City Clinical Emergency Hospital. Study methods used: analytical, systemic and comparative analysis.
Results and Discussion. In the general structure of acute poisoning, cases of mushroom poisoning account for 3%. The average hospital mortality rate is 9.3%. Among the aetiological factors, poison amanita prevails, conditionally edible mushrooms are in the second place, and edible mushrooms, which acquired toxic properties due to anthropogenic pollution of the environment are in the third place. The following abnormal conditions were found in poisoned persons: toxic gastroenterocolitis (81.4%), toxic neuropathy (2.1%), toxic hepatonephropathy (16.2%). It was established that the risk groups for poisoning associated with mushrooms are the population with a lack of understanding of the possible danger of eating mushrooms: unskilled workers, unemployed, school and preschool children and inhabitants of large cities who have no stranger in picking mushrooms (mainly men). In general, poisoned persons showed a low level of awareness of the danger and lack of knowledge about the means of preventing poisoning at the stages of picking, sorting and preparation of mushrooms and the rules of primary health care. Low efficacy of prevention against seasonal mushroom poisoning remains one of the factors of high morbidity and mortality.
Conclusion. The study revealed that seasonal poisoning with wild-growing mushrooms remains an important medical and social problem in most regions of Ukraine. In recent years, measures of sanitary supervision and control in the field of prevention of seasonal mushroom poisoning have been significantly worsened. The situation requires the restoration of an integrated approach to preventive actions to prevent harm to life and health when eating wild-growing mushrooms.
Key Words: sanitary and hygienic monitoring, mushroom poisoning.
Introduction. Ukraine is one of the countries where eating wild-growing mushrooms is a tradition, but despite the awareness about their dangers, the massive picking of mushrooms every year makes up the disappointing statistics of poisoning among the population of Ukraine. However, it is important to remember that out of 2,000 species of mushrooms that grow in Ukraine, at most 500, i.e. only one third, are considered edible [1]. Mushrooms are a balanced natural complex of biologically active substances: glycans, chitin, terpenes, proteins, lipids, carotenoids, melanin, polyphenols, polysaccharides, enzymes. Their spread in areas of ecological and anthropogenic loading, high yields and traditional consumption by locals determine the intake of various pollutants through the food chains by the human body.
Recently, the consistently high specific ratio of mushroom poisoning is associated with the difficult socio-economic situation and is caused by the decline of the system, which previously covered all stages of prevention of this group of poisoning and minimized the fatal effects caused by mushroom poisoning due to therapeutic measures. Unfortunately, the reforms in the work of the sanitary and epidemiological service that have taken place in recent years do not encourage optimism in this regards. Today, there is virtually no regulatory impact on the problem of poisoning with edible wild-growing mushrooms, taking into account the ecological and anthropogenic load on the environment, which is typical for industrial regions, and sanitary and hygienic supervision at all stages of contact with mushroom raw materials and cooked meals has been eliminated. There is no clear comprehensive system of treatment and prevention measures. It is necessary to improve and implement a preventive action algorithm to prevent mushroom poisoning.
Thus, the sanitary and hygienic aspects of the prevention of mushroom poisoning are an important socio-economic problem of public health, the system of which is now only emerging in Ukraine.
Objective. Analysis of the structure changes over time and causes of poisoning by wild-growing mushrooms among the population of Kyiv and the Region of Kyiv in recent years.
Materials and methods. Cases of mushroom poisoning (T62.0) among the adult population of Kyiv; statistic data from the Ministry of Health of Ukraine (MoH), the State Emergency Service of Ukraine (SES) and the toxicological centre of the Kyiv City Clinical Emergency Hospital (KCCEH). Study methods used: an analytical, systemic and comparative analysis.
Results and discussion. In Ukraine, the tradition of consuming wild-growing mushrooms has a deep cultural and historical basis. However, picking mushrooms is a high-risk activity. Among the huge variety of mushrooms, there are many species that a dangerous to human health, mushroom poisoning is recorded in all regions where they are picked and consumed. According to statistic data, poisoning by pileate mushrooms by a number of victims occupy the second place among lesions of non-bacterial nature after poisonings by organophosphorus insecticides [1, 2].
In Ukraine, the toxicology of wild-growing mushroom poisoning generally corresponds to global and European levels in terms of prevalence and mortality. Thus, according to the summary data of the Ministry of Health of Ukraine, over the period from 2011 to 2018, over 1,800 people were treated due to acute poisoning by wild-growing mushrooms, of which at least 150 died (hospital mortality 8%). A longs tending to monitor of mushroom poisoning shows that, on average, during the seasonal mushroom picking (August to September), one person dies daily in Ukraine [3‒5]. Changes in the number of cases of poisoning by wild-growing mushrooms in Ukraine over time according to the SES and the Center for Medical Statistics of the Ministry of Health of Ukraine for 2005–2018 is presented in Fig. 1.
Fig. 1. Changes in the number of cases of wild-growing mushroom poisoning over time in Ukraine in 2005–2018 (according to the annual analytical reports of the SES, Center for Medical Statistics of the MoH of Ukraine). Data for 2018 are provided as for 01.10.2018.
According to the emergency classifier (Decree of the CMU No. 368 as of March 24, 2004 “On Approval of the Procedure for Classification of Emergency Situations by Their Levels”) mushroom poisoning in Ukraine periodically acquires emergency status. In recent years, the highest number of cases was registered in the region of Kharkiv, Donetsk, Vinnytsia, Kirovohrad, Mykolaiv, Luhansk, Chernihiv, and Kyiv [5].
According to Order of the Main Directorate of Health and Medical Supply of Kyiv as of 1986, KCCEH (where Toxicological Department is functioning) is a specialised facility involved in the treatment of acute poisoning in Kyiv. In particular, under this Order, Toxicology Department is a specialized centre for the provision of medical care due to mushroom poisoning in adults. Annually, more than 2.5 thousand patients with acute poisoning are delivered to the hospital by emergency teams, of which about 3% are affected by mushroom poisoning [6–8].
During 1995 to 2018, 1,680 patients with the diagnosis “Mushroom poisoning” (ICD-T62.0) were treated at KCCEH, among treated ones, 985 (58.6%) were men, 695 (41.4) — women. The summary data on the number of mushroom poisonings (N = 1,680) during the study period from 1995 to 2018 and the rates of hospital mortality throughout the observation period and the structure of the main pathological syndromes are presented in Fig. 2.
Fig. 2 Changes in mushroom poisoning (N = 1,680) overtime during the study period from 1995to 2018 and the rates of hospital mortality (according to the Toxicological Department of the KCCEH).
The data show that there are significant fluctuations in the number of mushroom poisonings and in the rates of in-patient mortality, respectively. Throughout the study period, in-patient mortality rates were within 4.5 to 9.5%.
There are different classifications of mushroom poisoning, however, most of them divide mushrooms into three groups, depending on the clinical manifestations caused by the systemic organotropism of the mushroom toxins. Therefore, mushrooms of gastroenterotropic action, neurotropic action and hepatonephrotropic action are classified [9].
In general, in the structure of the aetiological factors of mushroom poisoning poison amanita prevails, the second place is taken by conditionally edible mushrooms and the third — by edible mushrooms that have acquired toxic properties due to man-made pollution of the biosphere. The summary structure of the main pathological syndromes is presented in Fig. 3.
At the same time, it should be noted that due to a quit large number of mushrooms, the first symptom of poisoning is acute gastroenteritis, complicating the early diagnosis of life-threatening poisoning by poison amanita. The data in Fig. 3 show the distribution of the directions of toxic action throughout the observation period; on average, gastroenterotropic effect was observed in 81.4% of persons, neurotropic — in 2.1%, and hepatonephrotropic — in 16.2%.
Fig. 3. Structure of acute poisoning by wild-growing conditionally edible mushrooms by the main toxic syndromes and its changes over time during 1995–2018 (according to Toxicological Department of KCCEH). Note: GETA, gastroenterotropic; NTA, neurotropic action; HNTA, hepatonephrotropic action.
It has been established that the main groups at risk of mushroom poisoning are: socially disadvantaged groups of population with a low level of sanitary education (workers of unskilled professions, unemployed, children of school and preschool age), residents of large cities without mushroom picking skills (mainly older men).
A separate negative factor for the Region of Kyiv is the radiation contamination of part of the districts, which have traditionally been places of picking wild-growing edible and conditionally edible mushrooms. Radioactive contamination of wild-growing mushrooms is an important cause that increases the risk to humans, although it does not cause acute toxic effects.
During 30 years after the Chornobyl disaster, the level of radioactivity due to 137Cs accumulation in forest cover and forest soils has decreased due to degradation and leaching with water and now accounts for approximately 56% of the initial activity. However, through the root system, radioactive 137Cs continues to penetrate wood, leaves, berries, and especially mushrooms. That is why, unlike agricultural products, the level of contamination of which has sharply decreased over time and been systematically controlled, the activity level of 137Cs in mushrooms can still reach several tens of Bq/kg.
The table provides data of the Laboratory of Radioecology of Agrarian, Forestry and Natural ecosystems of the Institute of Agroecology and Environmental Management of the National Academy of Sciences of Ukraine in terms of quantitative parameters of exceed of the maximum acceptable levels (MALs) of 137Cs in samples of wild-growing mushrooms from the territory of the Ukrainian Polissia over the 20 years (1991–2010).
Table 1
Changes in radioactive contamination of wild-growing mushrooms with 137Cs by separate years in state forestry enterprises of Polissia
According to the data, the radioactivity of wild-growing mushrooms of the Ukrainian Polissia after the Chornobyl NPP accident is still a significant obstacle to the use of these “forest gifts”. The Region of Zhytomyr remains a particularly dangerous area for mushroom picking (not including the Exclusion Zone).
Monitoring studies conducted by the State Institution “Zhytomyr Regional Laboratory Centre of the State Sanitary Service of Ukraine” show that in 2014 in the District of Korosten the excess of 137Cs in mushrooms was 54.5% from the number of tested samples, in the District of Narodychi — 66.6%, in the District of Olevsk — 47.3%, in the District of Malyn — 26.6%, in the District of Ovruch — 47.2%.
Studies conducted in 2015 within the northern regions of the Region of Zhytomyr have shown that the contamination of the fruiting bodies of wild-growing forest mushrooms was on average 1,230 Bq/kg, exceeding the established acceptable level by 146%, ranging from 47 to 3,780 Bq/kg. The specific activity of 137Cs and 40K radionuclides in macromycetes shows that the belonging of mushrooms to different ecological groups influences the accumulation of radionuclides in their fruiting bodies, which grow in one territory [10, 11, 12].
Thus, the production of forest phytocenoses, even with their small fraction in the human diet, is one of the main in forming the internal radiation dose of the population of both adjacent territories and the part of the population of Ukraine that consumes these products through their uncontrolled transportation from radioactively contaminated territories.
To reduce the level of radionuclide intake by the human body, it is necessary to strengthen the radiological control of forest products before sale and consumption, as well as to inform the population of the possible threat to health through the use of radioactively contaminated forest products.
The last comprehensive chemical safety studies of wild-growing mushrooms were conducted in the south-eastern region of Ukraine in the late 1990s and early 2000s. For example, when carrying out laboratory tests by the chemical safety parameters of the fruiting bodies of edible mushrooms, which were collected in “environmentally unfavourable places” — along traffic roads, in the areas of runways of aerodromes and industrial enterprises, on lawns of large cities, etc., it was found that 20.0%, 12.9%, 9.6% and 7.2% of the tested samples, respectively, exceeded the regulatory requirements by Pb, Cd, Cu, Zn. It was found that the quota of conditionally edible mushrooms (xenobiotics within 1.0–2.0 MAL) ranged from 4.4% for zinc to 12.9% for the lead with intermediate values of 5.9% for copper and 8.4% cadmium. Non-edible mushrooms (the content of toxic elements > 2.0 MAL) were found in 7.1% of tests. The degree of contamination of mushrooms with toxic elements reaches maximum values for copper and zinc in loamy soil, and for lead and cadmium — in sandy soil [13].
The above data show that in the conditions of anthropogenic environmental pollution there is a quit intense contamination of higher macromycetes by foreign chemicals.
In 2015, other authors investigated the content of heavy metals and other elements in the fruiting bodies of Carpathian mushrooms. It is found that the average content of Ca, Mn, Mg, Al, Ni, as well as the toxic elements Pb and Cd in the studied myxomycetes exceeds the average values accepted for a living substance; on the other hand, the concentration of Si, Zn and Cr in myxomycetes is lower than in most living organisms, and Fe and Cu are identical to their average percentage for other biological objects [14].
Studies conducted within rural settlements located in the Polissia part of the Region of Zhytomyr identified risks to the health of the population due to intake of chemical substances — carcinogens as result of consumption of the most polluted macromycetes species. The studies were conducted during 2011–2013 on the territory of rural settlements of The District of Radomyshl, Korostyshiv, Olevsk and Ovruch. The content of Cd, Cu, Pb, Zn in the fruiting bodies of mushrooms was measured by atomic absorption spectrophotometry after dry mineralization. Among the tested chemicals, substances with proven carcinogenic effect — lead and cadmium were selected. The evaluation of carcinogenic risk, which means the likelihood of increased incidence of neoplasms in humans due to oral intake of chemical carcinogens, was carried out by calculating the values of individual, total and population carcinogenic risks [15].
Data from other studies also confirm that macromycetes growing within the natural ecosystems of the Polissia part of the Region of Zhytomyr are not environmentally safe, and their consumption causes an increase in carcinogenic and non-carcinogenic risk of population morbidity, which necessitates the creation of a state system for monitoring the quality of mycological products [15, 16, 17].
The above features of mushrooms to accumulate xenobiotics cause a variety of pathological conditions observed in the poisoned persons.
The analysis of available clinical observations suggests that the Region of Kyiv is characterized by several pathological conditions that differ depending on the aetiological factor:
- fatal poisoning with highly toxic mushrooms — poison amanita Amanita phalloides, some types of amanita fly agarics;
- multisymptom poisoning with conditionally edible mushrooms that have not undergone sufficient cooking and retained toxins; symptoms of poisoning depend on the properties of the pollutant;
- poisoning with mushrooms that grow in places contaminated with various toxins, due to their high adsorption activity, mushrooms accumulate them;
- food toxic infections that develop due to the consumption of mushrooms infected with pathogenic microflora, especially cases of botulism are distinguished;
- symptoms of exacerbation of chronic diseases of the digestive organs (gastritis, pancreatitis, hepatitis, colitis, peptic ulcer and others).
In this case, the most dangerous are poisonings with mushrooms, which belong to the group of so-called amanita mushrooms (poison amanita, some species of amanita fly agarics).
It is also important to note that the content and ratio of toxic compounds in mushrooms is not constant since it depends on many factors, in particular, the type and age of mushrooms, place where they grow, air temperature, etc. Thus, in humus-rich lands, mushroom poisoning properties increase in the warm wet year and decrease in poor soils and in dry years.
Long-standing observations show that spring mushrooms form a mainly gastroenterotropic group of poisonings; mushrooms growing in summer cause hepatonephrotropic and neurotropic groups of poisoning; autumn mushrooms mainly have hepatotropic action. At the same time, the diversity and variability of symptoms of acute mushroom poisoning require careful differential diagnosis with a number of somatic and infectious diseases.
Therefore, the following situations should be clinically distinguished due to acute poisoning:
- poisoning with highly toxic mushrooms (poison amanita and certain types of amanita fly agarics);
- cases of toxic infection and botulism;
- cases of acute poisoning with pesticides, metals, other toxicants contained in mushrooms in high concentrations (typical for poisoning in the territories of the Regions of Donetsk, Dnipropetrovsk, Mykolaiv, Kirovohrad).
The clinical experience suggests that the following should be considered in the differential diagnosis of acute poisoning by wild-growing mushrooms:
- the fact of mushroom consumption by the poisoned person (in the form of any mushroom dish);
- presence of a positive epidemic history (the presence of signs of poisoning in most people who consumed suspicious food together);
- the onset of the initial symptoms of poisoning (gastroenteritis, gastroenterocolitis) 6 hours after consuming mushroom (usually 8‒12 hours);
- the course of gastroenteritis without raising the body temperature in the first 1–2 days; phase of “well-being”, which manifests itself with the cessation of enterocolitis and lasts for 1–2 days, after which jaundice appears.
For timely response to development of hepatic and renal failure, especially in patients whose condition is regarded as moderate or severe, immediate hospitalization is advisable only to intensive care units with experienced medical staff; provided with antidotes, sufficient supplies of infusion solutions, pharmacological means of symptomatic therapy; equipped with apparatuses for emergency application of extracorporeal detoxification procedures (plasmapheresis, haemodialysis, haemodiafiltration).
In cases of the group and mass poisoning, especially in families, the following should generally be done:
- hospitalize poisoned persons from mushroom poisoning focus (even in the absence of signs of poisoning) to in-patient departments for up to 3 days under medical supervision with obligatory laboratory tests;
- if necessary, ensure the active detection and search of persons who consumed the mushrooms together with the hospitalized but did not seek medical assistance in order to ensure an emergency clinical and laboratory workup and monitoring.
In the system of public health of Ukraine, due to the elimination of the sanitary and epidemiological service, in order to prevent damage to the population health in mushroom poisoning (especially group and mass), it is necessary to provide comprehensive epidemiological, hygienic and toxicological studies, which consist of the following stages:
Stage 1. Fieldwork. This is conducted in different regions to determine the species composition and growing season of higher macromycetes.
Stage 2. Routine and retrospective epidemiological analysis, which involves investigating the characteristics of poisoning with wild-growing mushrooms by methods of epidemiological analysis. This is conducted according to a specially designed program by the following criteria: number of poisoned, the rate of cases, aetiological structure (botanical species of mushroom), seasonality, location of places of picking mushrooms, age and gender of poisoned, their social origin and place of residence, duration of incubation period (development of outbreak in time), clinical pattern and degree of course of poisoning, mortality. The distribution of poisoning by symptom groups (gastroenterotropic, hepatonephrotropic, neurotropic and hepatotropic) and seasons of macromycetes fruiting is analysed in parallel with the analysis of toxicological and hygienic features of cases of mushroom poisoning.
Stage 3. Toxicological studies. They are conducted to detect toxins contained in mushrooms via biological testing in laboratory animals using specific chemical methods of rapid diagnosis.
Stage 4. Investigation of ecological and anthropogenic load on the environment. Laboratory studies of the fruiting bodies of edible mushrooms are performed according to the chemical safety parameters (GOST 26927-86, GOST 26930-86, GOST 26931-86, GOST 26932-86, GOST 26933-86, GOST 26934-86, MU 01-19/47-11-92). In parallel — chemical tests of soil where mushrooms have been growing.
Stage 5. Development of a comprehensive regional program of measures to prevent poisoning by wild-growing mushrooms. It should be noted that edible mushrooms under adverse environmental conditions can acquire toxic properties near industrial objects, especially involved in chemical production, motorways, in the presence of release of toxic substances (mercury, lead, cadmium, etc.) into the atmosphere, their discharge in the water.
Regular monitoring and analysis of cases of mushroom poisoning, which should result in a comprehensive system of measures to prevent poisoning by wild-growing mushrooms, will allow for preventive measures and reduce the likelihood of mushroom poisoning, and timely recognition of the aetiologic factor (species of mushroom) will allow to provide appropriate medical care for poisoned and reduce mortality due to poisoning in such a way.
The modern paradigm for the prevention of mushroom poisoning should be developed in accordance with the guidelines of the International Life Sciences Institute ILSI) and basic nutrition principles provided in the Codex Alimentarius, and it should involve three branches Codex [18, 19].
The first branch involves the dominant factors in the occurrence of poisoning. At this stage, the most important is a range of measures aimed at the person of the mushroom picker, since all cases of mushroom poisoning are related to the unstructured picking of mushrooms. An important component of this branch is awareness of the basic requirements at the stages of mushroom picking, processing, storage and consumption.
The second branch regulates measures concerning the level of preparation of healthcare facilities for the provision of medical care in case of poisoning.
The third branch includes the main areas of activity of sanitary and epidemiological surveillance for the prevention of mushroom poisoning, which may be related to the acquisition of mushrooms in food markets and enterprises producing mushroom products.
When controlling the sale of mushrooms in the markets, the main goal is to eliminate the possibility of erroneous purchase and consumption of poisonous mushrooms instead of edible ones.
Currently, in Ukraine, some functions of state sanitary supervision and control in the field of food hygiene (Decree of the CMU No. 442 as of September 10, 2014 “On Optimization of the System of Central Executive Authorities”) are entrusted to the body created during the reorganization of central executive bodies, State Service of Ukraine on Food Safety and Consumer Protection [20].
When creating a public healthcare system, this problem should be taken into account, in particular, the implementation of measures to prevent mushroom poisoning.
Conclusion
1. Seasonal poisoning with wild-growing mushrooms in Ukraine is an important medical and social problem. The main risk groups of mushroom poisoning are socially disadvantaged groups of population with a low level of sanitary education (workers of unskilled professions, unemployed, children of school and preschool age), residents of large cities without mushroom picking skills. Poisoning in males prevails.
2. In the structure of the aetiological factors of mushroom poisoning poison amanita prevails, the second place is taken by conditionally edible mushrooms and the third — by edible mushrooms that have acquired toxic properties due to man-made environmental pollution. The most common pathological poison syndromes are: gastroenterotropic (81.4%), neurotropic (2.1%), hepatonephrotropic (16.2%). In industrial regions, toxic elements (lead, cadmium, copper and zinc, radioactive elements) give toxic properties to edible mushrooms.
3. Currently in Ukraine the measures of sanitary supervision and control in the field of prevention of seasonal mushroom poisoning are scaled down. The situation requires the restoration of comprehensive preventive actions in public health system in order to avoid mushroom poisoning.
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Надійшла до редакції 23.09.2019 р.