Food Safety
Online ISSN : 2187-8404
ISSN-L : 2187-8404
Original article
Development of a Tool for Evaluating the Risk of Health Damage by Meat-borne Parasite Infection
Hiroshi YamasakiKyoko ArakawaTakeo OhashiKenji YagitaYasuyuki MorishimaHiromu SugiyamaKisaburo NagamuneMichiru KakinumaYuko OsadaDaihi OushikiAtsushi Hasegawa
Author information

2014 Volume 2 Issue 4 Pages 151-159


In this study, we developed a semi-quantitative risk mapping tool to assess the risk of damage to human health resulting from infection by meat-borne parasites. The developed method is based on the R-Map methodology, which is widely used in industrial settings to assess hazards in Japan. The risk of damage to health due to parasite infection was determined by two main criteria: the annual number of patients and the extent of damage to health. The former criterion was subdivided into four categories and the latter was evaluated based on severity of illness and period required to obtain a cure (hereafter, period to cure). The four categories for extent of damage to health were calculated by multiplying the scores assigned for severity of illness by the period to cure. Each parasite could then be mapped to this 4 × 4 matrix depending on the annual number of patients and the extent of damage to health. Three risk-level zones were then superimposed on the matrix to determine the priority of implementing risk management measures. In this way, the risk to human health associated with each parasite and the priority associated with implementing control measures could be visualized. Toxoplasma gondii infection in human immunodeficiency virus-infected patients and newborn babies was mapped to the unacceptable risk zone due to the severity of the disease in these patients. Emerging parasites, such as Sarcocystis fayeri, Kudoa septempunctata and Taenia asiatica, were mapped to the zone in which the risk of parasitic infections should be reduced by implementing urgent control measures, since doing so would prevent any further increase in infections. The risk assessment tool developed in this study can be employed to evaluate previous and potential risks of parasite infection and is useful for assessing the efficacy of risk control measures.

1. Introduction

Food-borne diseases can arise from the consumption of food that has been contaminated by pathogenic microbes and parasites, and by chemical substances or natural toxins. In Japan, the “Ordinance for Enforcement of the Food Sanitation Act,” which is based on the Food Sanitation Law, stipulates that food-borne parasitic diseases should be treated the same as food poisoning.

The eating habits of Japanese people have become increasingly diversified as their lifestyles have changed, with more processed and ready-to-eat foods being consumed in recent years. In addition to traditional foods, the importation of both exotic food and food cultures from foreign countries has also had a marked impact on their lifestyle. These changes have affected food poisoning patterns by increasing the frequency of incidents and the number of patients and fatalities1). Indeed, food poisoning attributed to emerging parasites2,3), i.e., parasites that previously did not occur in Japan, is becoming an increasingly important issue in the area of food sanitation and public health.

Meat products that are distributed and consumed in Japan are derived from livestock (cattle, pig, horse, sheep, and goat) and game animals (wild boar, deer, bear etc.). In the case of meat products from livestock, inspections of animals that have been sent to slaughter are routinely performed in abattoirs and meat inspection centers, as this is prescribed by the Slaughterhouse Act. By conducting these inspections, data on contamination by parasites can be estimated. However, since the act does not extend to game meat, very little information is currently available on the contamination of game meat products by parasites.

It is therefore necessary to implement effective risk assessment methods to carefully manage the risk associated with meat-borne parasitic infections. In Japan, a risk assessment methodology for zoonotic diseases including parasites has already been reported4). In that study, the risk associated with approximately 100 zoonotic diseases was quantified using a hierarchical analytical process that ranked each disease and assigned a risk factor. The results revealed that the majority of the 30 parasitic diseases examined had low risk scores, which made it difficult to prioritize the risks associated with a particular parasitic disease. However, the reason for the low scores was because the assessment items were biased toward human-to-human transmission. Consequently, parasitic diseases were assigned a relatively low-risk status if there was no human-to-human transmission and/or if transmissibility was low, unlike bacterial and viral infections which would score highly, since they are typically spread by human-to-human transmission.

Outside of Japan, risk-assessment studies on parasite infections have been performed for Cryptosporidium parvum5,6,7), Giardia intestinalis (syn. G. lamblia)7), Toxoplasma gondii8,9), Anisakis spp.10), Trichinella spiralis11,12), Taenia solium cysticercus13), and Taenia saginata14). In these studies, most of the risk assessments employed quantitative approaches, such as probabilistic analysis using Monte Carlo modeling5,14), hazard impact analysis6,7,9), scoring risks8), risk profiling10,11,13), and exposure assessment12).

The present study aimed to develop a risk assessment tool for assessing the potential damage to human health resulting from infection by meat-borne parasites based on currently available epidemiological and enzootic information in Japan, and to prioritize the identification of parasitic diseases for which control measures should be implemented.

2. Materials and Methods

2-1. Profiling of Meat-borne Parasites Targeted for Risk Assessment

A total of 14 parasites, including two protozoa, myxozoa, and 11 helminths associated with meat and fish, were selected for this assessment (Table 1). Table 1 also shows the sources of infection for each parasite. Two fish-borne parasites, Kudoa septempunctata and Anisakis spp., were included for comparing the risk associated with infection to the risk associated with meat-borne parasites. The data on livestock meat contaminated with any of these parasites were obtained from meat inspection statistics provided by the Ministry of Health, Labour and Welfare (MHLW), Japan15). The annual number of patients infected with these 14 parasites was estimated based on 1) Food Poisoning Statistics from the MHLW1), 2) a literature search of material held by the Japan Medical Abstracts Society, 3) PubMed, 4) annual reports of the National Institute of Infectious Diseases (2007 to 2013)16), and 5) medical insurance data from the Japan Medical Data Center17). To select the most suitable assessment items for estimating the risk of damage to human health due to infection by the target parasites, each parasite was profiled by considering the following items: annual number of food poisoning cases, annual number of patients, clinical symptoms, severity of illness, presence or absence of treatment and preventive methods, high-risk groups, presence or absence of secondary infection, seasonality, regionality, and current estimates of the proportion of meat products contaminated by parasites in Japan.

Table 1. Parasites and sources of infection considered for the risk mapping method.
Parasite Food product as source of infection
Sarcocystis fayeri Horse meat
Toxoplasma gondii Pork, beef, mutton, goat meat
Kudoa septempunctata Flounder
Toxocara canis and Toxocara cati Beef liver, free-range chicken liver
Trichinella spp. Bear meat
Anisakis spp. Mackerel, squid, Pacific saury (=samma in Japanese)
Paragonimus westermani Wild boar meat, Japanese mitten crab, Japanese freshwater crab
Paragonimus miyazakii Japanese freshwater crab
Fasciola spp. Beef liver
Taenia asiatica Pork liver
Taenia saginata Beef
Taenia solium (adult) Pork
Taenia solium (larval cysticercus) Food and drinking water contaminated with T. solium eggs
Spirometra erinaceieuropaei Snakes, frogs, free-range chicken

2-2. Selection of Risk Assessment Method

The profiling procedure revealed that it was difficult to employ quantitative risk assessment methods. The reasons for this were that the incidence of human cases infected by the target parasites was generally low, and epidemiological and enzootic information on meat-borne parasites was difficult to obtain. The R-Map risk assessment tool, which was originally developed to quantitatively assess the hazards associated with industrial products, is widely used in Japan18). Briefly, the R-Map method involves mapping the “frequency of occurrence” and “extent of damage” on a two-dimensional matrix (6 × 5) to visualize the associated risk and to evaluate the appropriate level of risk management.

In the present study, we developed a semi-quantitative method for evaluating risks associated with parasitic infections based on the R-Map methodology; this method was referred to as a risk mapping method.

2-3. Development of the Risk Mapping Method

Prior to developing the risk mapping method, two assessment items—annual number of patients and extent of damage to health—were selected to evaluate the risk of damage to health from the items used for initial profiling. The first item, annual number of patients, was subdivided into four categories (<10, 10 to 99, 100 to 999 and ≥1,000 cases) according to the number of reported cases per year. The second item, extent of damage to health, was evaluated based on the severity of illness and the period required to obtain a cure (hereafter referred to as period to cure). The severity of illness was also subdivided into four categories according to the Disability Weights (DW) defined by WHO19) (Table 2), with each subcategory assigned a score of 1 to 4 in order of increasing severity (Table 3). The period to cure was subdivided into three categories: short (<1 month), medium (1 to <3 months) and long (≥3 months), with each category assigned a score of 1 to 3, respectively (Table 3). In this way, a total score representing the extent of damage to health could be expressed by multiplying the scores assigned for severity of illness by the period to cure (Table 4). Any potentially lethal parasites were assigned a score of 12, because death was considered to be the most severe form of health damage. Similarly, emerging parasites, such as Sarcocystis fayeri, K. septempunctata and Taenia asiatica, which have become increasingly prevalent in recent years, were also assigned a score of 12, despite only having a severity of illness score of 1. The reason emerging parasites were assigned such high scores was because urgent control measures and management initiatives need to be implemented to prevent further infection by these parasites (Table 5). Total scores of 1 to 3, 4 and 6, 8 and 9, and 12 were assigned as very low, low, moderate, and high, respectively. Consequently, a risk map, which consisted of a 4 × 4 matrix based on the annual number of patients on the vertical axis and the extent of damage to health on the horizontal axis, was compiled. The risk associated with target parasites was assessed based upon profiled data from 2000 to 2013 and the risk was then compared with that for the period from 1960s to 1980s.

Table 2. Main symptoms associated with parasitic diseases and their severities.
Slight* Mild** Moderate*** Severe****
Symptoms Diarrhea Liver abscess Bloody sputum Meningitis
Bloody stool Jaundice Pneumothorax Blindness
Abdominal pain Hepatomegaly Pleural effusion
Cough Liver hypertrophy Epileptic attacks
Anemia Gastrointestinal disorder Pernicious anemia
Wandering mass Ileus Ascites
Myalgia Dizziness/vertigo
Creeping disease Lymphangitis
Pyrexia Central nervous system

* Disability Weights (DW)<0.03, ** 0.03≤DW <0.1,*** 0.1≤DW <0.3, **** DW ≥0.3

Table 3. Assessment items for evaluating the extent of damage to health.
Items Assessment Score Definition
Severity of illness Slight 1 See Table 2.
Mild 2
Moderate 3
Severe 4
Period to cure Short 1 <1 month. Patient recovers to original condition relatively
soon after treatment.
Medium 2 1 month to <3 months. Recovery (including complications)
takes long but does occur.
Long 3 ≥3 months. Disease often becomes chronic and results in
permanent impairment.
Table 4. Scores representing extent of damage to health.
Severity of illness
Period to cure Short (1) 1 2 3 4
Medium (2) 2 4 6 8
Long (3) 3 6 9 12

Scores 1-3 (very low), 4 and 6 (low), 8 and 9 (moderate) and 12 (high). Numbers in the parenthesis indicate scores assigned for each subcategory of severity of illness and period to cure.

Table 5. Results of risk assessment for 14 parasitic diseases.
No. Parasites Annual number
of patients
Extent of health damage
(A) (B) (C) (D) Score
(A x B)
Risk assessment
Main symptoms Severity
of illness
Score (A) Period
to cure
Score (B) Any deaths in
past 10 years
Any occurrence
in the last 2–3 years
1 Sarcocystis fayeri* 10–99 Diarrhea Slight 1 Short 1 None Yes 12 High
2-H Toxoplasma gondii 100–999 Encephalitis Severe 4 Long 3 Unknown Yes 12 High
2 T. gondii ≥1,000 Lymphadenitis Slight 1 Short 1 None Yes 1 Very low
3 Kudoa septempunctata* 100–999 Diarrhea Slight 1 Short 1 None Yes 12 High
4-H Toxocara canis and T. cati <10 Blindness Severe 4 Long 3 None Yes 12 High
4 T. canis and T. cati 10–99 Hepatomegaly Mild 2 Short 1 None Yes 2 Very low
5 Trichinella spp. <10 Fever, muscle pain Mild 2 Medium 2 None No 4 Low
6 Anisakis spp. ≥1,000 Gastric pain Slight 1 Short 1 None Yes 1 Very low
7 Paragonimus westermani 10–99 Bloody sputum Moderate 3 Medium 2 None Yes 6 Low
8 Paragonimus miyazakii <10 Pleural effusion Moderate 3 Medium 2 None Yes 6 Low
9 Fasciola spp. <10 Liver abscess Mild 2 Short 1 None Yes 2 Very low
10 Taenia asiatica* <10 Abdominal discomfort Slight 1 Short 1 None Yes 12 High
11 Taenia saginata <10 Abdominal discomfort Slight 1 Short 1 None Yes 1 Very low
12 Taenia solium (adult) <10 Abdominal discomfort Slight 1 Short 1 None Yes 1 Very low
13 T. solium (larval cysticercus) <10 Central nervous system manifestations Moderate 3 Long 3 None Yes 9 Medium
14 Spirometra erinaceieuropaei <10 Central nervous system manifestations Moderate 3 Medium 2 None Yes 6 Low
14 S. erinaceieuropaei <10 Creeping disease Slight 1 Short 1 None Yes 1 Very low

*emerging parasites

3. Results and Discussion

3-1. Risk Assessment of 14 parasites Based on Data for the Period 2000 to 2013.

Fig. 1 shows 14 parasites mapped to a matrix to visualize the risk of health damage associated with parasite infection. Due to differences in susceptibility to infection, T. gondii was mapped to different positions in human immunodeficiency virus (HIV)-infected patients and newborn babies, and healthy adults. Toxocara canis and Toxocara cati, and Spirometra erinaceieuropaei were also mapped to different positions in the matrix due to differences in severity associated with the site infected by the parasite.

Fig. 1.

Risk map for 14 parasites based on data from 2000 to 2013.

1, Sarcocystis fayeri: 2-H, Toxoplasma gondii (HIV/neonate): 2, T. gondii (adult): 3, Kudoa septempunctata: 4-H, Toxocara canis and Toxocara cati (blindness): 4, T. canis and T. cati (visceral larva migrans): 5, Trichinella spp.: 6, Anisakis spp.: 7, Paragonimus westermani: 8, Paragonimus miyazakii: 9, Fasciola spp.: 10, Taenia asiatica: 11, Taenia saginata: 12, Taenia solium: 13, T. solium (neurocysticercosis due to larval cysticercus): 14-H, Spirometra erinaceieuropaei (meningitis): 14, S. erinaceieuropaei (cutaneous larva migrans). Dark grey, light gray and white cells indicate unacceptable risk zone, zone in which the risk should be reduced, and socially-acceptable risk zone, respectively.

The R-Map method, in which a 6 × 5 matrix is divided into 3 risk level zones for purposes of risk management18), is the risk mapping method developed in this study; it employed three risk zones to determine the need for risk management measures: i) unacceptable risk, ii) risk that should be reduced, and iii) socially acceptable risk. Thus, T. gondii infections in HIV-patients and congenital neonates were mapped to the unacceptable risk zone due to the high severity of the illness and absence of an effective therapy, indicating the highest priority for risk management and urgent need to implement control measures. Emerging parasites, such as S. fayeri, K. septempunctata and T. asiatica, were mapped to the zone in which a risk should be reduced. The reason urgent control measures need to be implemented against emerging diseases is to promote the establishment of diagnostic methods and methods for preventing the expansion of infection. Toxoplasma gondii infection in adults, Anisakis spp., and T. canis and T. cati infections were mapped to the zone in which the risk should be reduced due to the moderate severity of illness associated with infection by these parasites. Other parasites were mapped to the socially acceptable risk zone because of the very low severity or mild nature of the symptoms and the presence of effective therapy. This risk mapping method facilitates risk assessments by visually representing the annual number of patients and the extent of damage to health in two dimensions.

3-2. Application of the Risk Mapping Method

The risk mapping method developed in this study was used to compare the risk of parasite infection for the period from 1960s to 1980s (Fig. 2). During this period, parasites such as T. solium (larval cysticercus), T. canis and T. cati, and S. erinaceieuropaei were mapped to the zone in which the risk should be reduced (Fig. 2). However, these parasites would now be reassigned to the socially acceptable zone (Fig. 1). Although it is possible to estimate which factors were likely to be effective in reducing the risk of parasite infections20), doing so with absolute certainty is difficult. It is generally considered that the adoption of national control measures combined with improved sanitation conditions21). In particular the abolishment of latrine facilities adjoined to pigsties was very effective for reducing T. solium infection22). Further, advances in diagnostic and therapeutic methods have also contributed to a reduction in the severity of illness caused by parasite infections23,24). On the other hand, a preference among Japanese people for eating raw and undercooked meat has contributed to an increase the risk of the emerging parasites such as S. fayeri2), K. septempunctata2) and T. asiatica3).

Fig. 2.

Risk map for 11 parasites based on data from 1960s to 1980s.

Symbols and risk zones are the same as those in Fig. 1. Note different positions of several parasites, such as T. canis and T. cati, T. solium, S. erinaceieuropaei, Trichinella spp., Fasciola spp. and T. saginata.

Thus, the risk mapping method described here is considered to be a useful tool, not only for assessing extant parasite infection risks, but also for assessing previous or potential risks, both of which have been affected by changes in the international food trade, diversification of food cultures, and advances in medical technologies and control measures.

In addition, while the present study focused on risk assessment within the context of damage to personal health due to infection by meat-borne parasites, the developed method could also be used to assess the risk of epidemics, as well as social and economic losses arising from parasite infections. Given these potential threats, it is considered important to develop alternative risk assessment items to extend the potential application of the methods described here. More detailed description of the developed method can be found elsewhere25). A part of the contents reported here has been published in Food Sanitation Research26).


The authors thank Drs. T. Nozaki, H. Ohmae, S. Izumiyama, K. Tsukui and Y. Nakano at the Department of Parasitology, National Institute of Infectious Diseases, for their critical comments and suggestions regarding this study.

This study was supported by a grant from the Food Safety Commission, Cabinet Office, Government of Japan (Research Program for Risk Assessment Study on Food Safety, No. 1202).

© 2014 Food Safety Commission, Cabinet Office, Government of Japan