Parasitic contamination in vegetables for human consumption: a systematic review and meta-analysis

Santomauro, Rafael Alves; Pinto-Ferreira, Fernanda; Pimont, Nathália Miasato; Marques, Mariana da Silva; Lemos, Maria Clara Soares; Ladeia, Winni Alves; Balbino, Letícia Santos; Navarro, Italmar Teodorico

doi:10.1590/S1984-29612024040

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Revista Brasileira de Parasitologia Veterinária

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Original Article • Rev. Bras. Parasitol. Vet. 33 (3) • 2024 • https://doi.org/10.1590/S1984-29612024040 copy

Parasitic contamination in vegetables for human consumption: a systematic review and meta-analysis

Contaminação parasitária em vegetais para consumo humano: uma revisão sistemática e meta-análise

Authorship SCIMAGO INSTITUTIONS RANKINGS

Abstract

The study conducted a review of the parasitological profile of vegetables from 2001 to 2021, considering the type, consumption, and cultivation, globally. The databases searched included MEDLINE, SciELO, Web of Science, Science Direct, and Scopus using the terms "Detection OR Prevalence OR Incidence OR occurrence OR contamination AND vegetable OR fruit AND Helminth OR egg OR Parasite OR cysts OR protozoa". A total of 16,600 articles were found, 117 of which were reviewed. Of the 391,291 samples, 3.85% (15,095) were contaminated by parasites. Among those positive, 30.10% (4,543/15,095) contained enteroparasites commonly of human origin and 58.78% (8,873/15,095) came from markets. Few articles mentioned the cultivation type, but among those, conventional cultivation showed more contamination (42.34%; 224/529). Herbaceous vegetables were the most contaminated (56.84%; 8,580/15,095. Ascaris lumbricoides was found in 10.16% (1,535/15,095) of the samples. Lettuce was the most contaminated (20.43%; 3,084/15,095).

Keywords:
Lettucce; helminths; kitchen gardens; meta-analyses; parasites; protozoa

Parasite	Positive	Total of analysis	Positives/analyses	Positives/total of positives
Ascaris lumbricoides	1535	26186	5.86%	10.17%
Giardia lamblia	1022	23069	4.43%	6.77%
Hookworms	833	11452	7.27%	5.52%
Entamoeba spp.	746	3323	22.45%	4.94%
Ascaris spp.	697	7705	9.05%	4.62%
Entamoeba coli	697	19849	3.51%	4.62%
Strongyloides stercoralis	695	20744	3.35%	4.60%
Cryptosporidium spp.	658	8263	7.96%	4.36%
Entamoeba histolytica	657	16517	3.98%	4.35%
Fasciola hepatica	568	16674	3.41%	3.76%
Taenia spp.	533	20700	2.57%	3.53%
Toxocara spp.	483	17406	2.77%	3.20%
Hymenolepis nana	420	23025	1.82%	2.78%
Giardia spp.	380	5822	6.53%	2.52%
Toxocara cati	355	3111	11.41%	2.35%
Trichuris trichiura	348	19611	1.77%	2.31%
Toxocara canis	316	4151	7.61%	2.09%
Blastocystis hominis	281	14662	1.92%	1.86%
Cryptosporidium parvum	279	17227	1.62%	1.85%
Dicrocoelium dendriticum	272	2873	9.47%	1.80%
Enterobius vermicularis	266	3556	7.48%	1.76%
Balantidium coli	261	13284	1.96%	1.73%
Endolimax nana	214	1851	11.56%	1.42%
Cyclospora cayetanensis	197	15556	1.27%	1.31%
Nematodes	180	996	18.07%	1.19%
Trichomonas hominis	162	578	28.03%	1.07%
Ancylostoma duodenale	150	13753	1.09%	0.99%
Toxoplasma gondii	146	5147	2.84%	0.97%
Entamoeba histolytica/dispar	141	1816	7.76%	0.93%
Trichostrongylus spp.	120	3404	3.53%	0.79%
Strongyloides spp.	119	2190	5.43%	0.79%
Microsporidia spp.	116	519	22.35%	0.77%
Trichuris spp.	105	1942	5.41%	0.70%
Cystoisospora spp.	100	12969	0.77%	0.66%
Fasciola spp.	94	1815	5.18%	0.62%
Ancylostoma spp.	94	3364	2.79%	0.62%
Taenia/Echinococcus	85	704	12.07%	0.56%
Hymenolepis diminuta	78	900	8.67%	0.52%
Others^* * Toxascaris leonina, Dicrocoelium spp., nematode larvae, Cyclospora spp., ascarids, unsporulated oocyst, Enterocytozoon bieneusi, Blastocystis spp., Hymenolepis spp., Ascaridia gali, Cystoisospora belli, helminths, Iodamoeba butschlii, Taenia saginata, Trichostrongylidae, Echinococcus multilocularis, Echinococcus spp., Entamoeba complex, Hydatigera taeniformis, Paramphistomum spp., Eimeria spp., Enterocytozoom spp., Enterobius spp., Haemonchus contortus, Taenia hydatigena, cestodes, coccidia, Cryptosporidium andersoni, Iodamoeba spp., Oxyuridae, Iodamoeba spp., Amoeba, Dipylidium caninum, Echinococcus granulosus, Trichuris ovis, Ascaris suum, Diphyllobothrium latum, Physaloptera spp. Schistosoma haematobium, Schistosoma mansoni, Strongylida, Taenia polyacantha, Trichostrongylus colubriformes, Acanthamoeba spp., Dipylidium spp., Heterophyes heterophyes, Schistosoma japonicum, Taenia crassiceps, Toxocara vitulorum, Necator americanus.	692	24577	2.82%	4.58%

Food	Positives	Total of analyzes	(Positives/analyzes)	Positivos/ total of Positives
Lettuce	3084	45135	6.83%	20.43%
Cress	864	24583	3.51%	5.72%
Leek	858	24027	3.57%	5.68%
Parsley	603	23782	2.54%	3.99%
Cabbage	595	7415	8.02%	3.94%
Arugula	495	4498	11.00%	3.28%
Carrot	432	7965	5.42%	2.86%
Tomato	429	22852	1.88%	2.84%
Radish	382	25917	1.47%	2.53%
Scallion	348	7561	4.60%	2.31%
Mint	331	9029	3.67%	2.19%
Cucumber	329	4931	6.67%	2.18%
Celery	297	17950	1.65%	1.97%
Cilantro	293	5875	4.99%	1.94%
Basil	236	6332	3.73%	1.56%
Spinach	229	5570	4.11%	1.52%
Roots	225	1749	12.86%	1.49%
Fennel	215	17100	1.26%	1.42%
Strawberry	203	804	25.25%	1.34%
Turnip	203	16545	1.23%	1.34%
Beet	184	17389	1.06%	1.22%
Potato	182	17134	1.06%	1.21%
Green Cabbage	180	16768	1.07%	1.19%
Pumpkin	119	1400	8.50%	0.79%
Dill	92	2756	3.34%	0.61%
Multiple vegetables^* * Multiples vegetables are foods that could not be classified separately for parasitic analyses, as wel as “pumpkin leaves”, “asparagus leaves”, “beet leaves”, “green leaves”, ready-to-eat foods and “corn husks”;	3074	39622	7.76%	20.36%
Others^ Others includes the following vegetables: bell pepper, chicory, onion, purslane, parsley, savory, spark, white jute, avocado, pepper, sprouts, pea, Orange, tarragon, vietnamese balm, eggplant, mango, shallot, gongroneme, jute mallow, rhubarb, basil, grape, yam, thyme, garlic, blackberry, cashew, apple, pear, cherry tomato, mustard, banana, bluberry, perilla, milkweed, amaranth, plumosa crest, beans, raspberry, okra, broccoli, chinese yoghurt, marjoram, swiss chard, chrysanthemum, dandelion, endive, ginger, watermelon, plum, blackberry, boldo, canton, cauliflower, turmeric, guava, melon, nectarine, oregano, peach, schizonepeta, green beans and vinegar.	613	16602	3.69%	4.06%

Parameter	n	Pooled frequency	CI (0.95)		Heterogeneity (I²)	p-value
POOLED FREQUENCY	391291	0.08	0.06	0.09	99%	<0.01
COUNTRY
Iran	76419	0.05	0.03	0.09	99%	<0.01
Brazil	19158	0.11	0.08	0.14	95%	<0.01
Iraq	205115	0.06	0.02	0.19	100%	<0.01
Saudi Arabia	6989	0.07	0.03	0.16	99%	<0.01
Nigeria	16432	0.07	0.03	0.16	99%	<0.01
Libya	630	0.29	0.26	0.33	not applied	not calculated
Turkey	1550	0.13	0.03	0.52	98%	<0.01
Syria	1444	0.06	0.04	0.10	80%	0.02
Ethiopia	9796	0.08	0.05	0.13	97%	<0.01
United Arab Emirates	574	0.06	0.04	0.08	not applied	not calculated
Spain	76	0.58	0.48	0.70	not applied	not calculated
Cambodia	144	0.23	0.17	0.31	not applied	not calculated
Nepal	1013	0.01	0.01	0.02	not applied	not calculated
India	1312	0.11	0.03	0.43	99%	<0.01
Morocco	304	0.11	0.08	0.15	not applied	not calculated
Portugal and Spain	700	0	0	0.01	not applied	not calculated
Thailand	2340	0.18	0.05	0.64	100%	<0.01
Venezuela	1062	0.04	0.03	0.05	not applied	not calculated
Egypt	4791	0.11	0.06	0.20	98%	<0.01
Palestine	600	0.09	0.07	0.12	not applied	not calculated
Canada	5145	0.01	0	0.10	98%	<0.01
Philippines	1274	0.22	0.20	0.24	0%	0.52
Greece	144	0.01	0	0.06	not applied	not calculated
Poland	1102	0.09	0.05	0.16	83%	<0.01
European countries	1692	0.02	0.01	0.03	not applied	not calculated
Pakistan	13906	0.04	0.02	0.10	99%	<0.01
Korea	832	0.07	0.02	0.17	70%	0.07
Ghana	1440	0.17	0.15	0.19	not applied	not calculated
China	4297	0.03	0	0.22	99%	<0.01
Costa Rica	500	0.06	0.04	0.08	not applied	not calculated
Sudan	1554	0.02	0.01	0.03	not applied	not calculated
Cuba	200	0.02	0.01	0.05	not applied	not calculated
Norway	1188	0.02	0.02	0.03	not applied	not calculated
Vietnam	1963	0.12	0.09	0.17	64%	0.06
Eritrean	56	0.27	0.17	0.41	not applied	not calculated
Italy	3888	0.01	0	0.01	not applied	not calculated
Czech Republic	1246	0.02	0.02	0.03	not applied	not calculated
Jordan	415	0.39	0.34	0.44
among groups						<0.01
HDI
Low: 1	27838	0.07	0.04	0.13	98%	<0.01
Medium: 2	224678	0.07	0.04	0.13	100%	<0.01
High: 3	112929	0.09	0.07	0.12	99%	<0.01
Very high: 4	25846	0.06	0.03	0.10	98%	<0.01
among groups						0.45
SAMPLE ORIGIN
Vegetable garden	10318	0.14	0.09	0.21	98%	<0.01
Market and garden	41134	0.07	0.04	0.11	97%	<0.01
Market	284640	0.07	0.05	0.10	100%	<0.01
Street fair	2450	0.03	0.02	0.06	94%	<0.01
Multiple locals	31930	0.05	0.02	0.10	99%	<0.01
Not informed	144	0.01	0	0.05	not applied	not calculated
Forest and garden	78	0.19	0.12	0.29	not applied	not calculated
Market and street fair	19802	0.07	0.01	0.28	100%	<0.01
Street fair and garden	480	0.06	0.04	0.09	54%	0.14
Restaurants	315	0.06	0.04	0.09	0%	0.72
among groups						<0.01

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E-mail: cbpv_rbpv.fcav@unesp.br

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[1] *Corresponding author: Rafael Alves Santomauro. E-mail: rafaelsantomauro@gmail.com