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From 1 January 2018 came into force Regulation (EU) 2015/2238 of the European Parliament and of the Council of 25 November 2015, introducing the concept of “novel foods”, including insects and their parts. One of the most commonly used ...
www.ncbi.nlm.nih.gov
Published online 2019 Jul 8. doi:
10.1371/journal.pone.0219303
PMCID: PMC6613697
PMID:
31283777
A parasitological evaluation of edible insects and their role in the transmission of parasitic diseases to humans and animals (edited see website for complete article)
Abstract
From 1 January 2018 came into force Regulation (EU) 2015/2238 of the European Parliament and of the Council of 25 November 2015, introducing the concept of “novel foods”, including insects and their parts. One of the most commonly used species of insects are: mealworms (
Tenebrio molitor), house crickets (
Acheta domesticus), cockroaches (Blattodea) and migratory locusts (
Locusta migrans). In this context, the unfathomable issue is the role of edible insects in transmitting parasitic diseases that can cause significant losses in their breeding and may pose a threat to humans and animals. The aim of this study was to identify and evaluate the developmental forms of parasites colonizing edible insects in household farms and pet stores in Central Europe and to determine the potential risk of parasitic infections for humans and animals.
The experimental material comprised samples of live insects (imagines) from 300 household farms and pet stores, including 75 mealworm farms, 75 house cricket farms, 75 Madagascar hissing cockroach farms and 75 migrating locust farms.
Parasites were detected in 244 (81.33%) out of 300 (100%) examined insect farms. In 206 (68.67%) of the cases, the identified parasites were pathogenic for insects only; in 106 (35.33%) cases, parasites were potentially parasitic for animals; and in 91 (30.33%) cases, parasites were potentially pathogenic for humans. Edible insects are an underestimated reservoir of human and animal parasites.
Our research indicates the important role of these insects in the epidemiology of parasites pathogenic to vertebrates. Conducted parasitological examination suggests that edible insects may be the most important parasite vector for domestic insectivorous animals. According to our studies the future research should focus on the need for constant monitoring of studied insect farms for pathogens, thus increasing food and feed safety.
Introduction
The growing demand for easily digestible and nutritious foods has contributed to the emergence of new food sources in agricultural processing. Edible insects are one such category of under-utilized foods with a high nutritional value [
1]. Insects are farmed for direct consumption and for use in the production of foods and feeds [
2]. The concept of “novel foods”, including insects and their parts, has been introduced by Regulation (EU) 2015/2238 of the European Parliament and of the Council of 25 November 2015 on novel foods, which came into force on 1 January 2018.
The growing popularity of exotic pets has also increased the demand for novel foods. However, edible insects are often infected by pathogens and parasites which cause significant production losses [
3]. These pathogens also pose an indirect threat for humans, livestock and exotic animals.
The majority of insect farming enterprises in the world are household businesses, and in Europe edible insects are rarely produced on a large scale. In European Union, entomophagy is rare, and it is regarded as a cultural taboo [
4]. More than 1900 species of insects are considered to be edible. The most popular edible insects include mealworms (
Tenebrio molitor) [
5], house crickets (
Acheta domesticus) [
4], cockroaches (Blattodea) [
6] and migratory locusts (
Locusta migrans) [
4].
Mealworms are beetles of the family Tenebrionidae. Adult beetles are generally 13-20 mm in length, and larvae have a length of around 30 mm. During their short life cycle of 1-2 months, females lay around 500 eggs. One of the largest mealworm suppliers in the world is HaoCheng Mealworm Inc. which produces 50 tons of live insects per month and exports 200,000 tons of dried insects per year [
7]. Mealworms are used in human and animal nutrition, and they are a popular food source for exotic pets, including reptiles and insectivores. The nutritional value of mealworm larvae is comparable to that of meat and chicken eggs [
8]. Mealworms are easy to store and transport. They are abundant in highly available nutrients and are regarded as a highly promising source of feed in poultry and fish breeding. Mealworms can also be administered to pets and livestock [
4]. The popularity of mealworms consumption by humans is on the rise especially in Europe. Mealworms effectively degrade biological waste and polystyrene foam [
9]. The most common mealworm parasites include
Gregarine spp.,
Hymenolepis diminuta and mites of the family Acaridae. Mealworms are model insects in parasitological research [
10–
12].
The house cricket (
A. domesticus) has a length of up to 19 mm, and its life cycle spans 2-3 months. It is a source of food for reptiles, amphibians and captive bred arachnids, including spiders of the family Theraphosidae. House crickets are consumed by humans in powdered form or as protein extracts [
13,
14]. Whole crickets are consumed directly in Thailand [
1]. These insects are frequently infested by
Nosema spp.,
Gregarine spp. and
Steinernema spp.
Cockroaches of the order Blattodea include the German cockroach (
Blattella germanica), American cockroach (
Periplaneta americana), Cuban burrowing cockroach (
Byrsotria fumigata), Madagascar hissing cockroach (
Gromphadorhina portentosa), speckled cockroach (
Nauphoeta cinerea), Turkestan cockroach (
Shelfordella lateralis) and oriental cockroach (
Blatta orientalis). Cockroaches can live for up to 12 months, and the largest individuals reach up to 8 cm in length. Cockroaches are increasingly popular in human nutrition, and they are a part of the local cuisine in various regions of the world [
15].
Migratory locusts are members of the family Acrididae, order Orthoptera. Insects have up to 9 cm in length and live for up to 3 months. Locusts are consumed by amphibians, reptiles and humans, mainly in Africa and Asia. Locusts contain up to 28% protein and 11.5% fat, including up to 54% of unsaturated fats [
16].
Nosema spp. and
Gregarine spp. are the most prevalent locust parasites [
17].
The aim of this study was to identify and evaluate the developmental forms of parasites colonizing edible insects in household farms and pet stores in Central Europe and to determine the potential risk of parasitic infections for humans and animals.
experimental material comprised samples of live insects (imagines) from 300 household farms and pet stores, including 75 mealworm farms, 75 house cricke
Results
Prevalence
Parasitic developmental forms were detected in 244 (81.33%) out of 300 (100%) examined insect farms. In 206 (68.67%) of the cases, the identified parasites were pathogenic for insects only; in 106 (35.33%) cases, parasites were potentially parasitic for animals; and in 91 (30.33%) cases, parasites were potentially pathogenic for humans.
Nosema spp. spores were detected in 27 (36.00%) cricket farms and 35 (46.67%) locust farms. The presence of
Cryptosporidium spp. was observed in 12 (16%) mealworm farms, 5 (6.67%) cricket farms, 13 (17.33%) cockroach farms and 4 (5.33%) locust farms. Forty-four (58.67%) mealworm farms, 30 (40.00%) cricket farms, 57 (76%) cockroach farms and 51 (68.00%) locust farms were infested with
Gregarine spp., including
Steganorhynchus dunwodyii,
Hoplorhynchus acanthatholius,
Blabericola haasi,
Gregarina blattarum,
G. niphadrones,
Gregarina cuneata and
Gregarina polymorpha.
Isospora spp. were detected in 7 (9.33%) mealworm farms, 4 (5.33%) cricket farms, 9 (12.00%) cockroach farms and 8 (10.67%) locust farms.
Eleven (14.67%) mealworm farms, 13 (17.33%) cockroach farms and 9 (12.00%) locust farms were infested with
Balantidium spp. including
B. coli and
B. blattarum. The presence of
Entamoeba spp., including
E. coli,
E. dispar,
E. hartmanii and
E. histolytica, was determined in 9 (12%) mealworm farms, 14 (18.67%) cockroach farms and 4 (5.33%) locust farms.
Seventeen (22.67%) cockroach farms were colonized by
Nyctotherus spp., including
N. ovalis and
N. periplanetae. Tapeworm cysticercoids, including
Hymenolepis nana,
H. diminuta and
Raillietina spp., were detected in 9 (12%) mealworm farms, 3 (4%) cricket farms, 4 (5.33%) cockroach farms and 3 (4.00%) locust farms. Nematodes of the order Gordiidea colonized 6 (8.00%) cricket and locust farms.
Hammerschmidtiella diesigni was detected in 35 (46.67%) cockroach farms.
Steinernema spp. was identified in 22 (29.33%) cricket farms, and
Pharyngodon spp.—in 14 (18.67%) locust farms. The presence of
Physaloptera spp. was observed in 4 (5.4%) mealworm farms, 2 (2.67%) cricket farms, 9 (12.00%) cockroach farms and 7 (9.33%) locust farms. Five (6.67%) mealworm farms and 7 (9.33%) cockroach farms were infested with Spiruroidea.
Thelastomidae spp. was detected in 10 (13.33%) cricket and locust farms.
Thelastoma spp. was identified in 58 (77.33%) cockroach farms. Acanthocephala were observed in 2 (2.67%) mealworm farms and 3 (4.00%) cockroach farms. Two (2.67%) cockroach farms were infested with Pentastomida.
The presence of Acaridae, including house dust mites, was observed in 35 (46.67%) mealworm farms, 15 (20.00%) cockroach farms and 7 (9.33%) locust farms. In the group of samples collected from mealworm farms,
Cryptosporidium spp. were noted in 37 (12.33%) samples,
Gregarine spp. were detected in 99 (33.00%) samples,
Isospora spp.—in 12 (4%) samples,
Entamoeba spp.—in 12 (4.00%) samples,
Balantidium spp.—in 14 (4.67%) samples, cysticercoids—in 18 (6.00%) samples,
Pharyngodon spp.—in 10 (3%) of samples,
Physaloptera spp.—in 15 (5.00%) samples,
Spiruroidea—in 6 (2.00%) samples, Acanthocephala spp.—in 2 (0.67%), and Acaridae in 80 (26.67%) samples. In the group of samples collected from cricket farms,
Nosema spp. were identified in 74 (24.67%) samples,
Cryptosporidium spp.—in 5 (1.67%) samples
Isospora spp.—in 8 (2.67%) samples,
Gregarine spp.—in 72 (24.00%) samples, cysticercoids—in 4 (1.33%) samples,
Physaloptera spp.—in 4 (1.33%) samples,
Steinernema spp.—in 11 (3.67%) samples, and nematodes of the order Gordiidea—in 19 (6.33%) samples. In the group of samples obtained from cockroach farms, the presence of
Cryptosporidium spp. was determined in 89 (11.87%) samples,
Gregarine spp.—in 236 (31.47%) samples,
Isospora spp.—in 16 (2.13%) samples,
Nyctotherus spp.—in 57 (7.60%) samples,
Entamoeba spp.—in 34 (4.53%) samples,
Balantidium spp.—in 35 (4.67%) samples, cysticercoids—in 4 (0.53%) samples,
Pharyngodon spp.—in 20 (2.67%) samples,
Physaloptera spp.—in 23 (3.07%) samples, Spiruroidea—in 14 (1.87%) samples,
Thelastoma spp.—in 270 (36.00%) samples,
H. diesigni—in 143 (19.07%) samples, Acanthocephala spp.—in 5 (0.67%) samples, Pentastomida spp.—in 5 (0.67%) samples, and Acaridae—in 29 (3.87%) samples. The following parasites were identified in locust farms:
Nosema spp.—in 125 (16.67%) samples,
Cryptosporidium spp.—in 13 (1.73%) samples,
Gregarine spp.—in 180 (24.00%) samples,
Isospora spp.—in 15 (2.00%) samples,
Entamoeba spp. in 9 (1.20%) samples,
Balantidium spp.—in 14 (1.87%) samples, cysticercoids—in 15 (2.00%) samples,
Physaloptera spp.—in 17 (2.27%) samples,
Steinernema spp.—in 31 (4.13%) samples, nematodes of the order Gordiidea—in 7 (0.93%) samples, and Acaridae—in 31 (4.13%) samples. Detailed results of the parasitological examination have been placed in
Table 1.
(See website for the rest of this nasty report)