Foodborne parasitic diseases in China:A scoping review on current situation,epidemiological trends,prevention and control

Langui Song,Qingxing Xie,Zhiyue Lv

1The Eighth Affiliated Hospital,Sun Yat-sen University,Shenzhen,Guangdong,China

2Key Laboratory of Tropical Translational Medicine of Ministry of Education,Hainan Medical University,Haikou,China

3NHC Key Laboratory of Control of Tropical Diseases,the First Affiliated Hospital,Hainan Medical University,Haikou,China

4Key Laboratory of Tropical Disease Control,Sun Yat-sen University,Ministry of Education,Guangzhou,China

ABSTRACT Objective:Foodborne parasitic diseases,although with a declining overall incidence rate,are still endangering local public safety.This review aims to describe the current situation and epidemiological trends of foodborne parasitic diseases in China in order to explore possible reasons contributors to its high prevalence in some areas,and propose strategies for prevention and control accordingly.Methods:A scoping review was conducted by searching PubMed,CNKI,Wanfang,CQVIP,Embase,and the Cochrane Library using search formula “foodborne parasitic diseases (or foodborne parasites)” AND “China”.Studies on foodborne parasitic diseases in China were considered,but only articles in English or Chinese published between January 1980 and June 2020 were retrieved.Included studies were screened according to the eligibility criteria:1)diseases consistent with the WHO definition of foodborne parasitic diseases;2) the food carriers were included in the WHO food classification;3) data related to epidemiology,pathogenicity,and prevention and control;4) Foodborne parasitic diseases cases or outbreaks in China.Results:A total of 111 out of 665 records were included and summarized.The prevalence of clonorchiasis,angiostrongyliasis,echinococcosis,trichinellosis and cysticercosis was still increasing although the infection rate of soil-transmitted nematodes has substantially decreased in recent years.Diverse eating habits,close contact with animals,and urbanization were contributing factors to the increase.Conclusions:Foodborne parasitic diseases remain an important public health issue in China with the progress of economic globalization and food diversification.We should manage to raise public awareness about the prevention and control of foodborne parasitic diseases,improve health and safety inspections,as well as public health practice.

KEYWORDS:Foodborne diseases;Parasitic diseases;China;Preventive medicine

Significance

Foodborne parasitic diseases are transmitted by contaminated food.This article comprehensively reviews and summerizes the clinical and epidemic characteristics of foodborne parasitic diseases in China.This review amis to provide information to health care administrators and clinicians for a better control and prevention of parasitic diseases.

1.Introduction

Foodborne parasitic diseases are acquired through the ingestion of food or drinking water contaminated with the infective stage of parasites.The diseases present some unique challenges and are often referred to as neglected diseases,which might result in major public health and socioeconomic problems[1].The World Health Organization (WHO) found in 2006 that 7% of foodborne diseases in the world are caused by parasites[2];meanwhile,in China,approximately 150 million people were reported to suffer from foodborne parasitic zoonoses in 2005 and more people were at risk[3].Transmission and prevalence are mainly associated with human behavior patterns of preparing food and dietary habits.The populations in endemic areas usually have formed related dietary traditions and customs of eating raw or undercooked food[4].However,their habits and traditions are difficult to change.In addition,the life cycles of parasites might be extremely complicated,which may include multiple intermediate hosts and definite hosts,and some of them may become food.In addition,the parasites themselves might contaminate food or water.The WHO classifies food causing foodborne parasitic diseases into five categories:land animals (

i.e.

,beef,pork and poultry),aquatic animals (

i.e.

,marine fish,freshwater fish,shellfish and aquatic mammals),dairy products,plants (

i.e.

,berries,fruits,leafy greens and vegetables) and others (

i.e.

,snakes,frogs and insects) (Figure 1)[5].To date,a ninety-three foodborne parasites have been identified,and some of them may lead to severe illness and even death[5].In this paper,the classification,prevalence and prevention and control strategies for foodborne parasitic diseases are reviewed to provide new insights for better control of foodborne parasitic diseases in China.

Figure 1.Five food categories and related foodborne parasitic diseases.

Figure 2.PRISMA flow diagram showing the scoping review process.

2.Materials and methods

2.1.Search strategy

We searched the term “foodborne parasitic diseases (or foodborne parasites)” AND “China” in three English and three Chinese electronic databases,including PubMed (https://www.ncbi.nlm.nih.gov/pubmed/),Embase (www.embase.com/),Cochrane Library(www.cochranelibrary.com/),CNKI (www.cnki.net),Wanfang(www.wanfangdata.con.cn) and CQVIP (http://www.cqvip.com/).After reading the title/abstract or the full article if necessary,we summarized the current situation,epidemiological trend and its characteristics,and the prevention and control of foodborne parasitic diseases in China.Then,we searched every genus we found in the first step (such as

Clonorchis

,

Opisthorchis

,

etc.

) AND epidemiology(or infection or pathogenicity) AND China.Finally,we searched every genus we mentioned (such as

Anisakis

,

Gongylonema

,

etc.

)AND case report (or misdiagnosis) from 1980 to 2020 in China.Manual searching was not performed,and the gray literature was not searched neither.

2.2.Eligibility criteria

Papers were included if they fulfilled the following criteria:1)consistent with the WHO definition of foodborne parasitic diseases;2) the food carriers were included in the WHO food classification;3) presented information related to epidemiology,pathogenicity,and prevention and control;4) written in English or Chinese;5)published during January 1,1980,to June 10,2020;and 6) the case or outbreak occurred in China.

2.3.Data extraction,summary and data charting process

We extracted information from the included studies under the following categories:1) the classification,prevalence and pathogenicity of foodborne parasitic diseases;2) the epidemiological trends and characteristics of foodborne parasitic diseases;and 3) the prevention and control strategies for foodborne parasitic diseases.Two authors independently assessed eligibility,extracted data and cross-check results with disagreements resolved by consensus.

3.Results

3.1.Search findings

Six hundred sixty-five records were retrieved.After excluding 21 records due to lack of full text,4 records due to duplication,and 529 records that met the exclusion criteria mentioned above,111 records were eventually included in this review.Figure 2 presents a flowchart of the selection process.

3.2.The classification,prevalence and pathogenicity of foodborne parasitic diseases in China

The foodborne parasitic diseases that have been identified or posed a potential threat in China are summarized and listed in Table 1-4.The pathogens are divided based on the biological classification of parasites (trematodes,nematodes,cestodes and protozoa) and are further classified according to the five major food sources mentioned above.Under each classification,the distribution,parasitic site and pathogenicity are recorded.Among them,foodborne trematode and cestode infections are numerous,widely distributed,closely related to diseases,and diverse in pathogenicity,thus attracting the most widespread attention.However,relatively few epidemiological investigations have been conducted on foodborne nematode and protozoan diseases in China.

Regarding the epidemiological distribution,information on the spatial distribution is relatively complete.However,few studies have examined the temporal and population distributions.For the study of pathogenicity,the location of the parasite and the possible symptoms and signs or pathological changes have been clearly documented,but few studies have investigated the specific pathogenic mechanism.

Foodborne trematode diseases are mainly transmitted by the consumption of raw or undercooked food such as fish,crustaceans and vegetables that harbor the larval stages of the parasites[6].A national survey conducted in 2005 showed that human clonorchiasis is endemic in 27 provinces,with the largest number of infected people (～5.5 million) in Guangdong;human paragonimiasis is prevalent in 24 provinces,with the highest prevalence in Shanghai(5.1%) and Chongqing (4.1%),respectively.Fasciolopsiasis was formerly one of the most dominant trematodes,as revealed by the first national survey between 1988 and 1992,and was distributed across 16 provinces with 9 531 infections;148 people were infected with

Fasciola

(

F.

)

hepatica

,and 9 people were infected with

F.gigantica

[7].The types,distribution and pathogenicity of common foodborne trematode infections in China are listed in Table 1,which includes trematodes carried by aquatic animals such as

Clonorchis

and

Opisthorchis

[8,9],

Heterophyes

[10],

Echinostoma

[11],

Gymnophalloides seoi

and

Paragonimus

[12-14],and trematodes carried by plants such as

Fasciolopsis

and

Fasciola

[15,16].

Table 1.Types,distribution and pathogenicity of foodborne trematode infections in China.

Human parasitic nematodes are widely distributed in nature and are found in water and soil.Most of them are free-living,but a small proportion parasitize the human body and cause disease[17].Although comprehensive data on the prevalence of foodborne nematodes in China are still lacking,we can retrieve information on some common nematodes separately.Human trichinellosis is serious in several provinces,such as Yunnan and Inner Mongolia,where it has a mean prevalence of 8.3% and 6.3%,respectively in 2005[7].Approximately 400 cases of human angiostrongyliasis have been reported in China[7].The types,distribution and pathogenicity of common foodborne nematode infections in China are listed in Table 2,which includes nematodes transferred by aquatic animals such as

Gnathostoma

[18],

Anisakis

[19],

Angiostrongylus

[20,21],and

Dioctophyme

[22];nematodes transferred by land animals such as

Trichinella

[23];nematodes transferred by plants such as

Trichostrongylus

[24];and nematodes transferred by other contaminated food or water such as

Dracunculus

[25],

Ascaris

[26],

Toxocara

[27],

Enterobius

[28],

Gongylonema

[29],

Trichuris

[30],

Capillaria

[31],

Syngamus

and

Rhabditis

[17,32].Most cestode adults live in the digestive tract of vertebrates,and their larvae can migrate throughout the body,resulting in visceral and cutaneous larval migrants[17].Cysticercosis is one of the most serious foodborne parasitic diseases,and people might acquire an infection by eating food or drinking water contaminated with the eggs of

Taenia (T.) solium

or self-infection caused by eggs entering the stomach with vomiting.It was reported in 29 provinces of China with～550 thousand infections according to a national survey conducted in 2005[7].Echinococcosis is another important parasitic disease that is now becoming the key parasitic disease in China,with 380 thousand infections,and～50 million individuals are at risk of infection based on a report published in 2005.In addition,～1 000 cases of human sparganosis were reported in 22 provinces due to the ingestion of raw frogs or snakes or drinking water contamininated with eggs in 2006[7].The types,distribution and pathogenicity of common foodborne cestode infections in China are listed in Table 3,which includes cestodes transferred by aquatic animals such as

Spirometra

and

Diphyllobothrium

[33,34];cestodes transferred by land animals such as

Taenia

[35-37];and cestodes transferred by other contaminated food or water such as

Echinococcus

[38,39],

Hymenolepis

[40],

Dipylidium

[41] and

Bertiella studeri

[42].

Table 3.Types,distribution and pathogenicity of foodborne cestode infections in China.

Although we included

Taenia

in the category of land animals,we should always remember that cysticercosis is acquired by eating food contaminated with eggs of

T.solium

[35],and thus we listed it separately in Table 3.Additionally,in rare cases,humans can be accidentally infected with

T.taeniaeformis

and

T.hydatigena

by inadvertently eating their eggs and infected with

Mesocestoides lineatus

by ingesting the muscles or organs of animals such as frogs and snakes that contain tetrathyridium[17].Approximately forty protozoan species are able to infect humans.Due to the lack of effective vaccines and difficulties in vector control,many protozoal infections are still a global public health problem[17].Human infection with

Giardia

lamblia

and

Toxoplasma gondii

has been documented in every mainland province of China.The mean infection rate of the latter is 7.9% nationwide.Human cases of cryptosporidiosis have been recorded in 14 provinces,and according to a survey conducted in Zhejiang Province in 2000,

Cryptosporidium

oocysts were detected in 57 of 548 children with diarrhea (10.4%)[7].The types,distribution and pathogenicity of foodborne protozoan infections in China are listed in Table 4,which includes protozoa carried by land animals such as

Sarcocystis

[43],protozoa carried by plants such as

Trypanosoma

[44],and protozoa carried by other contaminated food or water such as

Trichomonas hominis

[45],

Giardia

[46],

Lophomonas

[17],

Entamoeba histolytica

,

Entamoeba coli

[47],

Toxoplasma

[48],

Cryptosporidium

[49],

Isospora belli

[50],

Balantidium

and

Blastocystis

[51,52].

Studeis on typical cases of common foodborne parasitic diseases reported in China and their diagnosis and treatment are listed in Table 5[68-110],which helps us learn lessons and propose better control strategies.

Table 4.Types,distribution and pathogenicity of foodborne protozoan infections in China.

4.Discussion

4.1.The epidemiological trends and characteristics of foodborne parasitic diseases in China

From 1980 to the present,China conducted three national surveys on the distribution of human parasites ranging from 1988-1992,2001-2004,and,most recently,2014-2016.In the three surveys,the total infection rates of human parasites were 55.27%,21.38%and 3.41%,respectively[96].The infection rate of soil-transmitted nematodes across the country has been substantially reduced in recent years[96],which is closely related to the social and economic development and the adoption of scientific prevention measures in China.However,the prevalence of food-transmitted parasitic diseases such as trichinellosis,clonorchiasis,paragonimiasis,cysticercosis,and echinococcosis has increased significantly[97].The third survey of parasitic infections in China showed that the leading causes of foodborne parasitic disease (infection rate) in China were

Ascaris lumbricoides

(1.36%),followed by

Trichuris trichiura

(1.02%) and

Clonorchis sinensis

(0.23%).The overall infection rates of intestinal protozoa and cestodes were 0.99% and 0.06%,respectively[96].The fastest-growing foodborne parasitic diseases in China included clonorchiasis,angiostrongyliasis,echinococcosis,trichinellosis and cysticercosis[97].In recent years,some new changes in the prevalence of foodborne parasitic diseases in China have occurred,which merit attention.

China has 56 ethnic groups and 34 provinces (autonomous regions,municipalities and special administrative regions).Each region has its own unique food culture,leading to the prevalence of different types of foodborne parasitic diseases.For example,in Shunde,Guangdong,local people like to eat sashimi,and a survey conducted in 2014-2015 showed that the infection rate of

Clonorchis sinensis

among local residents was up to 42.38%[98].In Tibet,nomads have more contact with sheep,dogs,and wolves,and thus their food is more likely to be contaminated with the eggs of

Echinococcus

.Inspections conducted from 2012 to 2016 estimated that the prevalence of echinococcosis in the Tibetan population was 1.66%[99].People in Yunnan have the habit of eating raw or half-raw pork.Since 2000,21 outbreaks of human trichinosis have been reported in Yunnan Province,with 2 256 cases and 3 deaths[100].Freshwater snails are widely distributed in Hainan Province,and locals have the habit of eating

Ampullaria gigas

.An epidemiological survey conducted in Hainan Province indicated that the positive rate of

Angiostrongylus cantonensis

IgG antibody in the serum was 20.3%[101].In recent years,with the rapid development of tourism and the catering industry,food culture exchanges between various regions have increased rapidly,thus these so-called local diseases are no longer confined to the previous epidemic areas in China,which might lead to sporadic cases or even outbreaks.For example,Hubei and Henan reported cases of trichinosis caused by eating undercooked pork[102].From June to September 2006,a hospital in Beijing treated 141 patients with angiostrongyliasis,all of whom dined at a restaurant in Beijing.They all ate uncooked

Ampullaria gigas

from Guilin,Guangxi[103].Second,with the increase in economic globalization,an increasing amount of foreign food appears on the Chinese table.If these foods are not properly processed,they are likely to carry some parasites that are not available in China or have been controlled,causing the spread or even outbreaks of new or recurring foodborne parasitic diseases.For example,in June 1998,an outbreak of imported paragonimiasis occurred in Dandong City,Liaoning Province.Among the 676 people who consumed imported river crabs,623 had the disease,with an incidence rate of 92.2%[104].In 1994,the Ruili Animal and Plant Quarantine Bureau of Yunnan found 12

Anisakis

larvae in imported hairtails from the Bay of Bengal[105].Currently,an increasing number of Chinese people are gradually accepting Japanese sushi or sashimi,which might lead to

Anisakis

infection[106].Most foodborne parasitic diseases are zoonotic diseases,such as echinococcosis,trichinosis and toxoplasmosis.As the economy develops,keeping a pet is becoming a new hobby of the new generation[107],and thus the number of people keeping pets obviously increases,which leads to increased contact with animals,and the infective stages of parasites from these animals might contaminate the food,thereby resulting in infection.For example,an epidemiological survey of cat toxoplasmosis conducted in Beijing showed that the apparent prevalence rate was 2.0% in 2014 and increased to 7.2% in 2015[108].Another survey carried out in areas including Heilongjiang,Jilin,Liaoning and Inner Mongolia,where residents form a habit of breeding dogs and cats,revealed a high overall parasitic infection rate in animal fecal and serum samples (20.77%),and many common foodborne parasites were detected,such as

Toxocara canis

(28.23% in dogs) and

Toxocara cati

(5.29% in cats)[109].

The current parasitic infection rate in rural areas is higher than that in urban areas in China[96].However,as the process of urbanization accelerates,an increasing number of rural populations enter cities,which may cause an increase in the infection rate of foodborne parasites in cities.For example,in the past,paragonimiasis was presumed to occur in areas with poor sanitation conditions in Jiangsu,Zhejiang,Guangdong and Guangxi and rarely in cities.However,in recent years,paragonimiasis has continued to appear in cities,and the incidence is increasing annually,even showing outbreaks in families.Due to the particularity of the disease,it was called “urban paragonimiasis”[110].

4.2.Prevention and control strategies for foodborne parasitic diseases in China

Due to the diseases themselves (mild or nonspecific symptoms and diverse clinical symptoms),low public awareness,neglect of medical personnel and lack of sensitive and specific detection methods[4],misdiagnosis and missed diagnosis of foodborne parasitic diseases in the clinic occur frequently,further aggravating their harmfulness and people in the rural regions were more infected than those living in the urban areas[111].As shown in Table 5,eating raw fish or meat accounted for 32.6% of the observed infection routes,drinking raw water or eating plants accounted for 13.9%,contacting animals accounts for 18.6%,and others and unknown account for 34.9%.Among all cases reported in China,many researchers have overlooked the importance of investigating the route of infection,and mostly only cases characterized by severe or chronic symptoms would be published,which may not represent the most common cases.

The basic principle of infectious disease control is to manage the three links of parasitic disease epidemics,namely,the source of infection,transmission route and susceptible people[17].In addition to increasing awareness of prevention,strengthening health education,reinforcing the vigilance of medical staff,and comprehensively applying laboratory inspection methods[4],food hygiene inspections and supervision are important.The eating habits and customs of humans are difficult to change,but further improvements in food safety could solve this problem,such as the development of a

Bacillus subtilis

-based fish vaccine against

Clonorchis sinensis

infection[112].In addition,efforts to restrict the contamination of food with infective stages is another solution.For instance,the detection of parasite infections in pets,livestock and wild animals should be strengthened.We can also control the source of infection by controlling the animal host.For example,if dogs were prevented from eating raw offal or were wormed,the control of

Echinococcus granulosus

might improve.

In addition,the prevention and control of foodborne parasitic diseases is a global issue.In countries around China,the problem of parasites remains severe[113].In the mainstream of globalization,we cannot preserve our dignity as a nobody.Therefore,we should pay attention to the prevalence of parasitic diseases in the countries around China and provide them with assistance to reduce the burden of foodborne parasitic diseases.

The limitations of this article are listed below.1) The included literature was limited to studies published in English and Chinese,and the gray literature was not searched,which may lead to the loss of data from some areas in studies written in the local language or that has not been formally published.2) Reports and research on parasitic infections and foodborne parasitic diseases are constantly being updated,and the cases and epidemiological data in this article have temporal validity.

With the progress of economic globalization and food diversification,foodborne parasites are becoming increasingly common in both developing and developed countries,endangering human health and imposing great challenges in public health,including China.From the current situation presented above,we concluded that the diverse eating habits,closely contact with animals,and urbanization are increasing the risk of foodborne parasitic diseases in China.Although effective drugs are available for many foodborne parasitic diseases,they remain an important public health issue that merits further attention,and the emphasis should be placed on raising the awareness of prevention,strengthening health education and food hygiene inspections,reinforcing the vigilance of medical staff,and comprehensively applying laboratory inspection methods for their prevention and control.

Conflict of interest statement

We declare that we have no conflict of interest.

Funding

This work was supported by the Major Science and Technology Program of Hainan Province (Grant No.ZDKJ202003),Grants from the Key Research and Development Program of Hainan Province(Grant No.ZDYF2020120),the National Natural Science Foundation of China (Grant Nos.81572023 and 81371836),the Guangdong Natural Science Foundation (Grant No.2019A1515011541),the Science and Technology Planning Project of Guangdong Province(Grant No.2019B030316025),the National Parasitic Resources Center of China (Grant No.NPRC-2019-194-30),the Open Foundation of Key Laboratory of Tropical Translational Medicine of the Ministry of Education,Hainan Medical University (Grant No.2020TTM007),the 111 Project (Grant No.B12003),and the Teaching Reform Project of Guangdong Province (Grant No.2017001).

Authors' contributions

LS and QX were responsible for study selection and data extraction and drafted the manuscript.LS and ZL designed the study and revised the manuscript.All authors read and approved the final manuscript.