Gastrointestinal parasites in pigs in Brazil: prevalence, risk factors, diagnosis, and extension activities

Abstract

Brazil is a major pig-producing country with production systems that include both industrial and family farms. In these facilities, parasitic diseases present an obstacle to production. This study aimed to estimate the prevalence and risk factors of the gastrointestinal parasites that infect pigs as well as to provide information for producers through extension activities. Visits were made to 15 pig farms in cities in the states of Rio de Janeiro and Minas Gerais. Fecal samples were collected, questionnaires administered, and extension activities conducted. A total of 1,148 samples were collected: 299 from family farms and 849 from industrial farms. Stool samples were subjected to direct examination, sedimentation, flotation, and FLOTAC techniques. The most frequently detected parasites were cysts and trophozoites of the Ciliophora group, non-sporulated coccidian oocysts, eggs of Trichuris suis, strongyles, Strongyloides ransomi, and Ascaris suum. Statistical analysis revealed significant differences (p ≤ 0.05) in parasite presence and egg counts, with family farms exhibiting higher parasite burdens (p < 0.0001). Several risk factors were associated with the frequency of parasite infection, including the arrangement of watering systems on the pen floors and the type—or absence—of antiparasitic medication provided. Among the extension activities implemented, the “happy pig and sad pig” activity and “homework correction” stood out. These results highlighted the need for improvements in national pig production. This includes the development of programs offering credit, assistance, and training for pig producers to aid in the control of these parasites, with a focus on production and animal welfare.

Introduction

Brazil currently has one of the largest pig herds in the world and ranks fourth among pork producers and third among worldwide exporters (Embrapa 2024). This remarkable growth in national pig production, mainly observed in industrial farming, may be directly related to the implementation of new technologies in pig farming, improvements in animal health management, genetics, and the growing demand for high-quality meat production (Allievi et al. 2024; Thanasuwan et al. 2024).

Small- and medium-sized pig farms, which make up a significant portion of the agricultural sector, have several characteristics that distinguish them from industrial production facilities (Pinto et al. 2007). This type of family/traditional farming is an integral part of the rural economy in many parts of the world, providing additional sources of animal protein for human consumption, generating employment opportunities, and reducing poverty (Amadi et al. 2018; Abonyi and Njoga 2019; Omoruyi and Agbinone 2020; Thanasuwan et al. 2024).

Pig production has several advantages over other agricultural sectors, including greater and faster returns on investment because of high fertility rates of the pigs, early maturity, short generation intervals, lower rearing space requirements, and the adaptability of pigs to different production and health management systems (Amadi et al. 2018; Omoruyi and Agbinone 2020; Class et al. 2022; Chaudhary et al. 2023; Thanasuwan et al. 2024).

In developing countries, infectious diseases represent a serious threat to animal health and production, among which parasitic diseases are prominent (Ahmed et al. 2019). In national herds, parasitic diseases can cause frequent health problems at all stages of pig production and are therefore among the limiting factors in pig farming (Barbosa et al. 2015; Carreiro et al. 2016). Gastrointestinal parasitic infections in pigs are usually subclinical; therefore, farmers do not detect the first signs of infection and rarely consider parasites to be the causative agent (Abonyi and Njoga 2019; Symeonidou et al. 2020; Allievi et al. 2024; Thanasuwan et al. 2024). Pigs may harbor subclinical intestinal parasites, including the protozoa Balantioides coli, Entamoeba spp., and Cryptosporidium spp., and the nematodes Ascaris suum and Trichuris suis (Băieş et al. 2022).

Parasites are known to cause several problems in pigs, such as poor feed conversion, reduced fertility, a low number of piglets born and weaned, low piglet weight at birth and at weaning, and losses related to the high condemnation rate of viscera in slaughterhouses (Class et al. 2022; Addy et al. 2023; Jankowska-Mąkosa et al. 2023; Allievi et al. 2024; Alegre et al. 2024; Thanasuwan et al. 2024). Parasitized pigs tend to be more susceptible to other infectious and noninfectious diseases, which impair their health and well-being (Symeonidou et al. 2020; Bohach et al. 2023). In addition, pigs infected by parasitic agents have a 5% reduction in daily feed intake, an average daily growth of 31%, and an average feed conversion rate of 17% compared with pigs on a parasite-free diet (Bohach et al. 2023).

Notably, pigs are the main reservoirs of several gastrointestinal parasites with zoonotic potential, especially B. coli, a protozoan that can infect other species, including humans who are in close proximity to these animals, such as farmers (Solaymani-Mohammadi and Petri Jr 2006; Barbosa et al. 2018; Silva et al. 2021; Class et al. 2022). The presence of zoonotic parasites in pigs is an ongoing public health concern, as these agents can cause serious diseases in humans, including diarrheal, dysenteric, and even extraintestinal infections (Lee et al. 2022; Alegre et al. 2024). Moreover, other gastrointestinal parasites that infect pigs have zoonotic potential and public health relevance, including Blastocystis sp., Entamoeba sp., Cryptosporidium sp., and Ascaris sp. (Solaymani-Mohammadi and Petri Jr 2006; Johnson et al. 2008; Kvác et al. 2009; Leles et al. 2012; Fausto et al. 2015).

Unfortunately, in Brazil, there is a substantial gap in epidemiological studies comparing gastrointestinal parasites of pigs raised in family and industrial farming systems, and most of these studies focus only on the diagnosis of the parasitic agent in one type of system (Symeonidou et al. 2020; Class et al. 2022; Allievi et al. 2024). Thus, the aim was to conduct the first epidemiological study in Brazil involving both family and industrial pig farms located in several cities, combining different qualitative and quantitative laboratory techniques to provide a solid estimate of the frequency and inherent risk factors of the gastrointestinal parasites that infect these animals. In addition, extension activities were conducted with the aim of evaluating producers’ animal management practices and providing information about gastrointestinal parasitosis.

Materials and methods

Study locations and sampling

This study was conducted from July 2023 to July 2024 on pig farms with family and industrial production systems located in different municipalities of the states of Rio de Janeiro and Minas Gerais. The state of Rio de Janeiro was selected for this study due to the research group’s prior experience working with this topic in the region, which provided familiarity with the location of pig farms in the area (Barbosa et al. 2015; Class et al. 2020, 2022). Additionally, the Parasitology Laboratory of the Fluminense Federal University (UFF), where the analyses were conducted, is located in this state, and this geographical proximity facilitated the logistics of the study.

The state of Minas Gerais, specifically the municipalities of Rio Pomba and Barbacena, was included because of its proximity to Rio de Janeiro and the limited number of industrial pig farms in the latter. Therefore, the selected farms in Minas Gerais served to complement the sample size of properties with this production profile in the study.

The state of Rio de Janeiro is located in the eastern portion of the Southeast Region of Brazil, covers an area of 43,750.425 km², and is bordered by the states of Minas Gerais, Espírito Santo, and São Paulo. Currently, the state is divided into 92 municipalities, which are grouped into government regions. The climate in the state is predominantly tropical, with average annual temperatures ranging from 22 to 24 °C (Brasil 2022). Although Brazil does not maintain official data on the population of pigs kept on family farms, according to the last census by the Secretary of Agriculture, Livestock, Fisheries, and Supply, the state of Rio de Janeiro had approximately 26,429 pigs raised on industrial farms (SEAPPA/RJ n.d.). Thirteen family pig farms located in the interior municipalities of the metropolitan region of the state of Rio de Janeiro (Itaboraí, Maricá, Tanguá, Rio Bonito, and Silva Jardim), coastal lowlands (Casimiro de Abreu and Saquarema), and mountainous region (Cachoeiras de Macacu) were invited to participate in the study because these places still have active agricultural sectors; that is, they concentrate rural producers. In addition, two industrial farms located in the municipalities of Nova Friburgo, a city in the mountainous region of the state, and Pinheiral, located in the central Paraíba region, also participated in the study. It is worth noting that, in the municipalities of Maricá, Rio Bonito, and Cachoeiras de Macacu, two properties were included.

The state of Minas Gerais is in the northwestern portion of the Southeast Region of Brazil, covering an area of 586,513.983 km², and is considered the fourth largest state in the country, containing 853 municipalities. The predominant climate is tropical highlands, characterized by hot, rainy summers and dry, mild winters. The average temperatures are between 18 and 24 °C (Brasil 2022). Minas Gerais is among the states with the greatest pig production in the country, with a production of approximately 6,573,169 heads in 2023 (ABCS 2024). Among the various regions in the state, the locations with the highest concentrations of pig farming are Zona da Mata, Alto Paranaíba, and Triângulo Mineiro (Fernandes 2010). Owing to the scarcity of industrial farms in the state of Rio de Janeiro, two farms in the cities of Rio Pomba and Barbacena in the Zona da Mata region of Minas Gerais, which borders the municipalities of the mountainous region of Rio de Janeiro, were also included.

The farms selected for this study were identified through recommendations from pig farmers, veterinarians, and researchers in pig production or related fields. The involvement of trusted intermediaries was essential to facilitate initial contact and engagement with the farm owners, thereby enabling the implementation of the study. All farm owners were contacted in advance by telephone and formally invited to participate in the research, all of whom provided voluntary consent.

All the farms included in this study were identified by letters (A–O) to preserve their anonymity. For all farms, newborn piglets and sick animals were excluded from fecal sampling. Owing to the lack of information on the number of family farms in the municipalities of Rio de Janeiro, the sample size calculation to achieve a minimum confidence level of 95% was based on other parasitological surveys conducted in pigs from farms located in other cities of Rio de Janeiro, which reported parasite frequencies ranging from 86.1 to 93.1% (Barbosa et al. 2015; Class et al. 2020, 2022). For the industrial farms, a 95% confidence level was also adopted for sampling in accordance with previous studies on industrial farms also located in Rio de Janeiro and Minas Gerais (Barbosa et al. 2015; Carreiro et al. 2016; Nishi et al. 2000). An exception was the nursery and fattening sectors of industrial farm M, which contained more than 1000 animals in each sector; at this facility, convenience sampling was applied, and at least 100 fecal samples were obtained from nursery and fattening piglets.

The cities in the states of Rio de Janeiro and Minas Gerais in which the pig farms are located are highlighted in color on the map shown in Fig. 1.

Fig. 1.

Locations of pig farming properties in different municipalities in the states of Rio de Janeiro and Minas Gerais, Brazil, highlighted in color

Study design and collection of biological samples

This study was conducted over three technical visits to each pig farm. The visits had different objectives and were always scheduled in advance with each producer and their family members. In general, the intervals between visits varied, with an average of approximately 7 days.

First technical visit

The first visit consisted of presenting the study through simple and clear conversations with all the people directly involved in the production of the animals (handlers and farmers). Those who agreed to participate in the study signed the informed consent form required by the Committee on Ethics in the Use of Animals of Fluminense Federal University (CEUA) and Ethics Committee on Human Research (CEP) and completed a semi-structured questionnaire about pig management and infrastructure conditions of the farm. After completing the questionnaire, the extension activity “walk around the property” was performed to become familiar with the property. Fecal samples from the animals were collected directly from the rectal ampulla using a rectal palpation glove lubricated with glycerin or immediately after spontaneous defecation.

Second technical visit

On the second visit, the parasitological results were delivered and verbally explained to the producers. An interactive lecture was given with the aid of a textbook entitled “Parasites and the Importance of Their Control” according to our group’s previous methodology (Class et al. 2020, 2022). Additionally, during this visit, the extension activity “happy pig and sad pig” was performed, which aimed to stimulate self-recognition by the producers regarding their conduct in the management of pigs. At the same visit, a “health calendar” was established on the farm, in which the producer can note the application dates of drugs, including medicines and vaccines. In addition, a newsletter entitled “10 Important Steps for Producers: Hygiene and Pig Breeding” reviews key measures for routine pig management.

Third technical visit

At the third visit, fenbendazole-based anthelmintics were delivered to the farmers who did not have the financial means to purchase medicine. According to the medicine leaflet, the dosage indicated for pigs was 20 g for every 80 kg of live weight administered in a single dose, excluding pregnant sows. In this visit, a questionnaire called “homework correction” was administered to the farmers to verify whether the information learned during the study period was retained and clear. Finally, all producers participating in this study received a certificate of participation.

Laboratory processing

The fecal material collected from the pigs was brought to the Parasitology Laboratory at UFF and processed the same day for direct examination followed by the qualitative coproparasitological techniques of Lutz sedimentation (1919) and centrifugal Sheather’s flotation (1923) as modified by Huber (2003), as well as the quantitative FLOTAC technique (Cringoli et al. 2010) using an NaCl solution (d = 1.200 g/dl). All the microscope slides and FLOTAC chambers were read under an Olympus® BX 41 binocular optical microscope at × 100 magnification; if necessary, the samples were viewed at × 400 magnification for confirmation. All the results were recorded in technical notebooks, including the counts of parasitic structures visualized in the FLOTAC chambers.

Statistical analysis

The fecal sample was considered positive when at least one form of a parasite (trophozoites, cysts, oocysts, larvae, or eggs) was detected. The frequency was determined by dividing the number of positive samples by the total number of samples collected, and these results are presented as percentages (%). All qualitative information obtained with the questionnaire was tabulated and presented descriptively, using tables to highlight the most common responses. For the industrial farms, the pigs were categorized as follows: breeding sows (including those in farrowing and gestation rooms, pregnant, and resting sows), breeding males (boars), nursery piglets (weaned at 17 weeks), and finishing piglets (18–22 weeks). These data were not available for family farms because pigs are not classified in this way. Data on the sex of pigs from both family and industrial farms, as well as animal categories from industrial farms, were retrieved and tabulated.

All these retrieved data, as well as data obtained from the questionnaire and the sex and age of the animals, were stored in a database created using Microsoft Excel 2007®. Statistical analyses were performed to determine the significance of the parasite frequencies between the family owned and industrial farms and among the categories of pigs raised on the industrial farms using the chi-square test or Fisher’s exact test. For the distribution of parasite frequencies in the pig classifications, the effect size was determined with the Cramér’s V measure. In addition, to verify if there was any significant association of the questionnaire responses and the sex of the animals with positive parasite detection, a univariate exploratory analysis was performed. Significant variables in the univariate analysis were included in the multivariate logistic regression model with a 5% significance level, and the possible risk factors were assessed using the odds ratios (ORs) and their respective 95% confidence intervals. All the statistical analyses were performed using SPSS software version 29.0.

The egg counts obtained with the FLOTAC technique were tabulated according to the parasite taxon, and the parasitic load was classified according to the classification of Nwafor et al. (2019) with adaptations as follows: low to moderate load, eggs per gram (EPG) between 0 and 500, and high load, EPG greater than or equal to 500. Mean values, standard deviations, minimum and maximum count values, and the coefficient of variation between the pig samples were calculated according to the type of farm. The differences in EPG among the farms were analyzed using the Mann–Whitney nonparametric statistical test at the 5% significance level. The relative frequencies (%) were determined by dividing the number of positive samples by the total number of samples collected.

Results

Estimation of the frequency of gastrointestinal parasites in family and industrial pig farms

Among the 15 farms included in this study, the total number of animals ranged from 6 to 440, totaling 1,148 pigs of different age groups and sexes (Table 1). Among the pig samples positive for one or more gastrointestinal parasites, 93.6% were from family farms, and 61.6% were from industrial farms, with a significant difference (p < 0.05) in the total number of parasitized animals between the two production systems. When the parasitological laboratory techniques used were combined, an overall frequency of parasite-positive samples of 69.9% was observed. Protozoa were detected more often than helminths (Table 1).

Table 1.

Gastrointestinal parasites detected in fecal samples of pigs from family owned and industrial farms located in different municipalities in the states of Rio de Janeiro and Minas Gerais

Gastrointestinal parasite	Farms
	Family											Industrial
	A (n = 18)	B (n = 6)	C (n = 17)	D (n = 24)	E (n = 31)	F (n = 9)	G (n = 6)	H (n = 82)	I (n = 13)	J (n = 76)	K (n = 17)	L (n = 57)	M (n = 440)	N (n = 113)	O (n = 239)	Total (n = 1,148)	p value
Ciliophora group	7 (38.8%)	6 (100%)	3 (17.6%)	10 (41.6%)	28 (90.3%)	6 (66.6%)	5 (83.3%)	31 (37.8%)	12 (92.3%)	65 (85.5%)	13 (76.4%)	47 (82.4%)	190 (43.1%)	57 (50.4%)	95 (39.7%)	575 (50%)	0.00
Coccidian oocysts	14 (77.7%)	1 (16.6%)	10 (58.8%)	14 (58.3%)	31 (100%)	1 (11.1%)	1 (16.6%)	48 (58.5%)	13 (100%)	72 (94.7%)	17 (100%)	13 (22.8%)	76 (17.2%)	42 (37.1%)	76 (37.3%)	429 (37.3%)	0.00
Amoebids	0	1 (16.6%)	0	0	2 (6.4%)	0	0	2 (2.4%)	0	0	0	0	0	0	0	5 (0.4%)	0.00
Blastocystis sp.	0	0	3 (17.6%)	0	0	0	0	2 (2.4%)	0	0	0	0	5 (1.1%)	5 (4.4%)	0	15 (1.3%)	0.00
Protozoa	14 (77.7%)	6 (100%)	11 (64.7%)	18 (75%)	31 (100%)	6 (66.6%)	5 (83.3%)	59 (71.9%)	13 (100%)	75 (98.6%)	17 (100%)	50 (87.7%)	229 (52%)	76 (67.2%)	145 (60.6%)	755 (65.7%)	0.00
Ascaris suum	1 (5.5%)	0	0	0	15 (48.3%)	0	4 (66.6%)	53 (64.6%)	0	1 (1.3%)	12 (70.5%)	10 (17.5%)	0	0	1 (0.4%)	97 (8.4%)	0.00
Trichuris suis	3 (16.6%)	4 (66.6%)	0	4 (16.6%)	13 (41.9%)	0	0	44 (53.6%)	9 (69.2%)	35 (46%)	12 (70.5%)	0	0	1 (0.8%)	102 (42.6%)	227 (19.7%)	0.00
Strongyles	14 (77.7%)	4 (66.6%)	1 (5.8%)	15 (62.5%)	31 (100%)	8 (88.8%)	3 (50%)	52 (63.4%)	11 (84.6%)	48 (63.1%)	17 (100%)	3 (5.2%)	0	8 (7%)	4 (1.6%)	219 (19%)	0.00
Strongyloides ransomi	13 (72.2%)	4 (66.6%)	0	7 (29.1%)	30 (96.7%)	6 (66.6%)	0	15 (18.2%)	10 (76.9%)	19 (25%)	4 (23.5%)	1 (1.7%)	0	0	0	109 (9.4%)	0.00
Nematode larvae	0	4 (66.6%)	2 (11.7%)	1 (4.1%)	4 (12.9%)	0	0	0	1 (7.6%)	0	2 (11.7%)	0	0	0	0	14 (1.2%)	0.00
Hymenolepis sp.	4 (22.2%)	0	0	0	0	0	0	0	0	0	0	0	0	0	0	4 (0.3%)	0.00
Helminth	16 (88.8%)	5 (83.3%)	3 (17.6%)	15 (62.5%)	31 (100%)	8 (88.8%)	6 (100%)	73 (89%)	13 (100%)	62 (81.5%)	17 (100%)	13 (22.8%)	0	9 (7.9%)	106 (44.3%)	377 (32.8%)	0.00
Subtotal	17 (94.4%)	6 (100%)	11 (64.7%)	18 (75%)	31 (100%)	8 (88.8%)	6 (100%)	77 (93.9%)	13 (100%)	76 (100%)	17 (100%)	51 (89.47)	229 (52%)	76 (67.2%)	167 (69.8%)	803 (69.9%)	0.00

Family pig farms are represented by letters A–K; industrial farms are represented by letters L–O. A p value ≤ 0.05 was considered statistically significant. Strongyles: eggs of the superfamilies Trichostrongyloidea and Strongyloidea

In general, the parasites most frequently detected in the fecal samples of the animals were cysts and trophozoites of Ciliophora group, oocysts of non-sporulated coccidia, eggs of T. suis, eggs of strongyles, eggs of Strongyloides ransomi, and A. suum. The number of samples positive for these parasites was statistically significant (p ≤ 0.05) (Table 1). In addition, cysts of amoebids, Blastocystis sp., nematode larvae, and Hymenolepis sp. were detected (Table 1).

In the feces of the animals, polyparasitized fecal samples, which contained more than one parasite taxon, were more common than monoparasitized samples. Combinations of two parasite taxa, particularly the combination of Ciliophora group and coccidia and the combination of Ciliophora and T. suis, were the most frequently identified polyparasitized samples, followed by samples with combinations of three taxa, including the combination of Ciliophora, coccidia, and strongyles and the combination of Ciliophora, coccidia, and T. suis (Fig. 2).

Fig. 2.

Monoparasitic and polyparasitic fecal samples of pigs from industrial and family farms in different cities of the states of Rio de Janeiro and Minas Gerais

Frequency of parasites according to pig production categories on industrial farms

Among the samples from the industrial farms, the highest infection rates for most of the detected parasite taxa were found in the fattening pigs (Table 2). There were statistically significant differences (p < 0.05) in all parasite taxa among animal categories. However, the greatest effect sizes as determined by Cramér’s V were observed in the frequency of samples positive for A. suum (V² = 0.387), T. suis (V² = 0.383), and in the Ciliophora group (V² = 0.274), which were more frequently detected in pigs in the older age groups.

Table 2.

Gastrointestinal parasites stratified according to the categories of pigs raised on industrial farms in different cities of the states of Rio de Janeiro and Minas Gerais

Industrial pig farms	Pigs categories	Ciliophora groupa	Coccidiaa	A. suuma	T. suisa	Strongylesa	S. ransomia
L (n = 23)	Nursery (n = 273)	19	0	1	0	1	0
M (n = 122)		17	7	0	0	0	0
N (n = 62)		26	15	0	0	3	0
O (n = 66)		17	16	0	11	1	0
		79 (20.3%)	38 (18.4%)	1 (9.1%)	11 (10.7%)	5 (33.3%)	0
L (n = 1)	Lactating sows (n = 94)	1	0	0	0	0	0
M (n = 54)		25	8	0	0	0	0
N (n = 23)		10	17	0	0	5	0
O (n = 16)		4	5	0	0	1	0
		40 (10.3%)	30 (14.5%)	0	0	6 (40%)	0
L (n = 0)	Breeding sow (n = 116)	0	0	0	0	0	0
M (n = 112)		50	32	0	0	0	0
N (n = 0)		0	0	0	0	0	0
O (n = 4)		1	2	0	1	0	0
		51 (13.1%)	34 (16.4%)	0	1 (1%)	0	0
L (n = 8)	Fatteners (n = 320)	4	5	0	0	1	0
M (n = 141)		93	22	0	0	0	0
N (n = 25)		18	8	0	0	0	0
O (n = 146)		71	52	1	90	1	0
		186 (47.8%)	87 (42%)	1 (9.1%)	90 (87.4%)	2 (13.3%)	0
L (n = 25)	Breeding boars (n = 46)	23	8	9	0	1	1
M (n = 11)		5	7	0	0	0	0
N (n = 3)		3	2	0	0	0	0
O (n = 7)		2	1	0	0	1	0
		33 (8.5%)	18 (8.7%)	9 (81.8%)	0	2 (13.3%)	1 (100%)
	Total	389	207	11	102	15	1

Industrial farms are represented by letters L–O, ^ap ≤ 0.05

Information obtained through questionnaires administered to pig producers was subjected to univariate statistical analyses

According to the questionnaires completed by the producers regarding the physical facilities, animals were housed in a pen with cement and/or wood walls, most of which were fully or partially covered with fiber cement tiles and/or ceramic tiles, and the floors of the facilities were predominantly cement, with plastic flooring in the nursery sectors of some industrial farms (L–N). Most producers reported cooling animals by splashing water over their bodies with a hose; however, the industrial farms in Rio de Janeiro also included a drop in the ground that accumulates a layer of water in the collective fattening pens for this purpose (L, M). The watering systems used were mostly cement vessels, and other containers were placed directly on the floor of the pens (A, B, E–K). However, family farms C and D and industrial farms L–O also used nipple-type watering systems. Most of the water used in pig production was untreated, i.e., water from a river, spring, pond, or artesian well (A–J/M–O). In terms of feed, pigs from industrial farms (L–O) received feed formulated specifically for each production phase. Pigs from family farms received mostly human food leftovers and agricultural by-products supplied predominantly in cement feeders arranged on the floor and/or suspended feeders. Approximately seven participating farms provided a source of heat, such as a creep, in the first days of the piglets’ lives.

The farms had proportionally more female pigs than male pigs. In addition, all farms had the presence of other animal species, such as canines, Galliformes, and Passeriformes; and on almost half of the farms, these animals were observed to share space with the pig-breeding site. The research team observed the presence of tools and infrastructure on several pig farms that were favorable for animal welfare. All producers reported never observing blood in the animals’ feces; however, the majority reported behavioral changes, including cannibalism, coughing, sneezing, itching, vocalization, and excessive salivation but no occurrence of diarrhea episodes. In general, on most family farms, pigs did not always receive antiparasitic drugs; when drugs were provided, the main active constituents were piperazine, fenbendazole, and levamisole. In contrast, on farms C, L, M, N, and O, macrocyclic lactones were the most supplied anthelmintics. With respect to the use of coccidiostats, only the industrial farms M and N used toltrazuril in the first days of the life of the piglets (data not shown in the table). In almost 100% of the farms, basic care, including teeth rasping and cutting, navel healing, breastfeeding control, vaccination, and iron supplementation and to ensure that all piglets had access to teats, was provided to piglets during their first days of life.

Excreta accumulation was observed in several pens on the family farms and on industrial farms M and O. However, all farms had utensils intended only for cleaning pig pens, including brooms, shovels, water hoses, and buckets. Manual cleaning directly with water was the most reported cleaning method, but some properties (B–D, L–N) preferred dry environmental cleaning using only a broom and/or scraping with a shovel. The treatment of excreta removed from pens was reported by most farms, especially the industrial farms (L–O) and family farms C–E and H, with the use of manure and settling ponds being the most reported. The raw disposal was widely reported on family farms. Positive practices for sanitary management were observed on the industrial farms, especially farm L, which was in Rio de Janeiro; this farm applied lime to the walls, enforced sanitary break and quarantine, and used a flamethrower during deep cleaning during the sanitary evacuation period. On the family farms, similar sanitary management measures were rarely reported, with most measures reported by farm C, which also applied lime to the walls and enforced quarantine and sanitary breaks of the premises. During the technical visits, the team observed that approximately half of the pigs included in the study were exposed to a high number of muscids, which was observed on six farms.

Univariate analysis revealed that most of the variables collected were statistically significant factors (p ≤ 0.05) for the overall frequency of parasite infection, as well as for the main taxa detected (Table 3). These variables were included in the final logistic regression model (Table 4).

Table 3.

Univariate analysis of gastrointestinal parasites detected in fecal samples from pigs raised on family owned and industrial farms

Information	Gastrointestinal parasite		Ciliophora group		Coccidia		A. suum		T. suis		Strongyles		S. ransomi
	%	p value	%	p value	%	p value	%	p value	%	p value	%	p value	%	p value
Type of farm				0.00*
Family (n = 299)	93.65	0.00*	62.21		74.25	0.00*	28.76	0.00*	41.47	0.00*	68.23	0.00*	36.12	0.00*
Industrial (n = 849)	61.60		45.82		24.38		1.3		12.13		1.77		0.12
Facilities type
Pens with wood wall (n = 17) (K)	100	0.00*	76.47	0.04*	100	0.00*	70.59	0.00*	70.59	0.00*	100	0.00*	23.53	0.06
Pens with cement and/or wood wall (n = 1131) (A–J, L–O)	69.50		49.69		36.43		7.52		19.01		17.86		9.28
Roof pen
Roofless (n = 13) (I)	100	0.01*	92.31	0.00*	100	0.00*	0	0.61	69.23	0.00*	84.62	0.00*	76.92	0.00*
Totally or partially covered (n = 1135) (A–H, J–O)	69.60		49.60		36.65		8.55		19.21		18.33		8.72
Floor of the buildings
Cemented (n = 538) (A–K, O)	83.09	0.00*	52.23	0.174	55.39	0.00*	16.17	0.00*	42.01	0.00*	38.66	0.00*	20.07	0.00*
Cemented associated with plastic flooring and/or bare ground (n = 610) (L–M)	58.36		48.20		21.48		1.64		0.16		1.8		0.16
Water to cool the pig
Splashing water on the animals’ bodies (n = 651) (A–K, N, O)	80.34	0.00*	51.92	0.17	52.23	0.00*	13.36	0.00*	34.87	0.00*	33.18	0.00*	16.59	0.00*
Accumulates a layer of water (n = 497) (L, M)	56.34		47.69		17.91		2.01		0		0.6		0.2
Supply of drink water
Provided 2 or 3 times a day (n = 251) (A, B, D, F–K)	94.82	0.00*	61.75	0.00*	72.11	0.00*	28.29	0.00*	44.22	0.00*	68.53	0.00*	31.08	0.00*
Ad libitum (n = 897) (C, E, L–O)	62.99		46.82		27.65		2.9		12.93		5.24		3.46
Waterers
Containers placed on the floor (n = 258) (A, B, E, F–K)	97.29	0.00*	67.05	0.00*	76.74	0.00*	33.33	0.00*	46.51	0.00*	72.87	0.00*	39.15	0.00*
Nipple or suspended waterers (n = 890) (C, D, L–O)	62.02		45.17		25.96		1.24		12.02		3.48		6.9
Origin of the water used by the property
Municipal piped water (n = 74) (K, L)	91.89	0.00*	81.08	0.00*	40.54	0.61	29.73	0.00*	16.22	0.54	27.03	0.09	6.76	0.53
Untreated watera (n = 1074) (A–J, M–O)	68.44		47.95		37.15		6.98		20.02		18.53		9.68
Food provided to pig
Remains of human and agricultural by-products (n = 299) (A–K)	93.65	0.00*	62.21	0.00*	74.25	0.00*	28.76	0.00*	41.47	0.00*	68.23	0.00*	36.12	0.00*
Feed by breeding phase (n = 849) (L–O)	61.60		45.82		24.38		1.30		12.03		1.77		0.12
Feeder
Containers and/or cement feeder on the floor (n = 119) (A, B, H, I)	94.96	0.00*	47.06	0.49	63.87	0.00*	45.38	0.00*	50.42	0.00*	68.07	0.00*	35.29	0.00*
Feeders on the floor and/or suspended (n = 1029) (C–G, J–O)	67.06		50.44		34.31		4.18		16.23		13.41		6.51
Creep/Heat source
No (n = 124) (A–G, I)	88.71	0.00*	62.10	0.00*	68.55	0.00*	16.13	0.00*	26.61	0.05*	70.16	0.00*	56.45	0.00*
Yes (n = 1024) (H, J–O)	67.68		48.63		33.59		7.52		18.95		12.89		3.81
Sex
Male (n = 464) (A–E, G–O)	69.18	0.64	50.00	1.00	38.79	0.42	7.54	0.38	23.92	0.00*	20.04	0.49	11.64	0.05*
Female (n = 684) (A, C–O)	70.47		50.15		36.4		9.06		16.96		18.42		8.04
Other animals on the property
Yes (n = 1148)	69.95	NA	50.09	NA	37.37	NA	8.45	NA	19.77	NA	19.08	NA	9.49	NA
Other animals share the same location as pigs
No (n = 389) (B–G, L, O)	76.61	0.00*	51.41	0.53	37.79	0.84	7.71	0.57	31.62	0.00*	17.74	0.42	12.34	0.02*
Yes (n = 759) (A, H–K, M, N)	66.53		49.41		37.15		8.83		13.7		19.76		8.04
Enrichment elements associated with animal welfare
No (n = 181) (A–G, I, L)	88.95	0.00*	68.51	0.00*	54.14	0.00*	16.57	0.00*	18.23	0.61	49.72	0.00*	39.23	0.00*
Yes (n = 967) (H, J, K, M–O)	66.39		46.64		34.23		6.93		20.06		13.34		3.93
Observation of blood in the stool
No (n = 1148)	69.95	NA	50.09		37.37	NA	8.45	NA	19.77	NA	19.08	NA	9.49	NA
Behavior change
No (n = 220) (A, B, E, G, J–L)	96.36	0.00*	80.45	0.00*	68.18	0.00*	19.55	0.00*	30.45	0.00*	58.18	0.00*	35	0.00*
Yes (n = 928) (C, D, F, H, I, M–O)	63.69		42.89		30.06		5.82		17.24		9.81		3.45
Observation of diarrhea
No (n = 432) (A–C, E–G, I–K, O)	81.48	0.00*	55.56	0.00*	54.63	0.00*	7.87	0.66	41.2	0.00*	32.64	0.00*	19.91	0.00*
Yes (n = 716) (D, H, L, M, N)	62.99		46.79		26.96		8.80		6.84		10.89		3.21
Antiparasitic medicine provided to pigs
Macrocyclic lactones or combined with another medications (n = 866) (C, L–O)	61.66	0.00*	45.27	0.00*	25.06	0.00*	1.27	0.00*	11.89	0.00*	1.85	0.00*	0.12	0.00*
Does not provide or provides other active constituentsb (n = 282) (A–B, D–K)	95.39		64.89		75.18		30.5		43.97		71.99		38.3
Care for piglets
Performs initial care (n = 1142) (A, C–O)	69.79	0.18	49.82	0.03*	37.48	0.42	8.49	1.00	19.53	0.01*	18.83	0.01*	9.19	0.00*
Does not perform (n = 6) (B)	100.00		100.00		16.67		0		66.67*		66.67		66.67
Accumulation of excreta in the pig pen
No (n = 433) (A, C–H, J, L, N)	85.68	0.00*	59.82	0.00*	56.81	0.00*	19.4	0.00*	23.09	0.03*	42.26	0.00*	21.02	0.00*
Yes (n = 715) (B, D–G, I, K, M, O)	60.42		44.20		25.59		1.82		17.76		5.03		2.52
Cleaning type
Manual cleaning with water (n = 491) (A, E–K, O)	83.91	0.00*	53.36	0.05*	55.6	0.00*	17.72	0.00*	44.4	0.00*	38.29	0.00*	19.76	0.00*
Manual dry cleaning (n = 657) (B–D, L–N)	59.51		47.64		23.74		1.52		1.37		4.72		1.83
Cleaning utensils intended only for cleaning the pig facility
Yes (n = 1148)	69.95	NA	50.09	NA	37.37	NA	8.45	NA	19.77	NA	19.08	NA	9.49	NA
Disposal of feces
Disposal in sewer in natura (n = 145) (A, B, F, G, I–K)	98.62	0.00*	78.62	0.00*	82.07	0.00*	12.41	0.07	43.45	0.00*	72.41	0.00*	38.62	0.00*
Undergoes treatment (n = 1003) (C–E, H, L–O)	65.80		45.96		30.91		7.88		16.35		11.37		5.28
Apply lime paint to the facilities
No (n = 175) (A, B, D, F–I,K)	92.57	0.001*	51.43	0.74	62.29	0.00*	40	0.00*	43.43	0.00*	70.86	0.00*	33.71	0.00*
Yes (n = 973) (C, E, J, L–O)	65.88		49.85		32.89		2.77		15.52		9.76		5.14
Sanitary break
No (n = 521) (A, B, D–K, O)	83.69	0.00*	53.36	0.04*	55.28	0.00*	16.7	0.00*	43.38	0.00*	39.73	0.00*	20.73	0.00*
Yes (n = 627) (C, L–N)	58.53		47.37		22.49		1.59		0.16		1.91		0.16
Quarantine
No (n = 282) (A, B, D–K)	95.39	0.00*	64.89	0.00*	75.18	0.00*	30.5	0.00*	43.97	0.00*	71.99	0.00*	38.3	0.00*
Yes (n = 866) (C, L–O)	61.66		45.27		25.06		1.27		11.89		1.85		0.12
Flamethrower
No (n = 1091) (A–K, M–O)	68.93	0.00*	48.40	0.00*	38.13	0.02*	7.97	0.02*	20.81	0.00*	19.8	0.00*	9.9	0.03*
Yes (n = 57) (L)	89.47		82.46		22.81		17.54		0		5.26		1.75
Presence of flies
No (n = 558) (C, D, F, G, J–L, N, O)	77.06	0.00*	53.94	0.01*	44.09	0.00*	5.02	0.00*	27.6	0.00*	19.18	0.94	6.63	0.00*
Yes (n = 590) (A, B, E, H, I, M)	63.22		46.44		31.02		11.69		12.37		18.98		12.2

*p ≤ 0.05, ^aWater from a river, spring, pond or artesian well, ^bPiperazine and fenbendazole or piperazine and levamisole, NA not applicable, as there are no two categories of answers

Table 4.

Multiple logistic regression model of the variables statistically associated with the gastrointestinal parasites detected in samples from pigs raised on family and industrial farms

Information	Multivariate logistic regression
	p value (p ≤ 0.05)	OR adjusted (95% CI)
Gastrointestinal parasite
Water to cool the pig	0.004	1.9 (1.2–2.9)
Waterers	0.001	43.6 (4.5–421.9)
Antiparasitic medicine provided to pigs	< 0.001	16.4 (6.4–41.9)
Ciliophora group
Waterers	< 0.001	6.3 (2.7–14.8)
Quarantine	0.014	7.7 (1.5–39.4)
Coccidia
Type of farm	< 0.001	20.4 (5.4–75.9)
Water to cool the pig	< 0.001	2.7 (1.7–4.2)
Waterers	0.028	2.8 (1.1–7.2)
Food provided to pig	< 0.001	20.4 (5.4–75.9)
Observation of diarrhea	< 0.001	2.9 (1.8–4.8)
Antiparasitic medicine provided to pigs	< 0.001	10.6 (6.4–17.7)
Cleaning type	0.013	3.6 (1.3–10.1)
Quarantine	< 0.001	117.4 (20.5–673.8)
Ascaris suum
Supply of drink water	< 0.001	133.3 (28.9–615.0)
Creep/heat source	< 0.001	9.8 (3.5–27.5)
Antiparasitic medicine provided to pigs	< 0.001	44.9 (22.2–90.8)
Apply lime paint to the facilities	0.001	3.3 (1.6–6.8)
Quarantine	0.003	28.9 (3.2–262.0)
Trichuris suis
Roof pen	0.01	6.2 (1.5–25.1)
Waterers	0.046	3.3 (1.0–10.7)
Behavior change	< 0.001	129.7 (40.4–416.4)
Observation of diarrhea	< 0.001	128.9 (44.0–377.5)
Antiparasitic medicine provided to pigs	< 0.001	90.8 (34.7–238.1)
Accumulation of excreta in the pig pen	< 0.001	6.7 (2.5–17.7)
Cleaning type	0.029	3.2 (1.1–9.0)
Sanitary break	< 0.001	97.7 (7.8–1222.9)
Quarantine	0.001	13.7 (2.8–67.7)
Strongyloides ransomi
Waterers	< 0.001	17.7 (6.3–49.7)
Creep/heat source	< 0.001	8.4 (4.0–17.6)
Enrichment elements associated with animal welfare	< 0.001	33.5 (7.1–157.0)
Antiparasitic medicine provided to pigs	< 0.001	673.2 (46.3–9786.2)
Disposal of feces	0.018	2.9 (1.2–7.1)
Presence of flies	< 0.001	13.8 (5.2–36.6)
Strongyles
Type of farm	0.019	7.8 (1.4–43.6)
Floor of the buildings	0.016	4.5 (1.3–15.2)
Water to cool the pig	< 0.001	12.5 (3.3–48.1)
Waterers	< 0.001	10.5 (4.0–27.1)
Food provided to pig	0.019	7.8 (1.4–43.6)
Creep/heat source	0.002	3.9 (1.6–9.2)
Enrichment elements associated with animal welfare	0.001	3.5 (1.6–7.6)
Antiparasitic medicine provided to pigs	< 0.001	115.9 (62.2–215.8)
Quarantine	< 0.001	150.7 (32.9–690.0)

^*p ≤ 0.05

Risk factor estimation for pig parasitic infections based on logistic regression modeling

According to the logistic regression model, the variables that appeared to be recurrent in parasitic infections were the type of watering systems and the supply of antiparasitic drugs. The supply of water in bowls, cement containers, and others on the floor was significantly associated (p ≤ 0.05) with positivity for gastrointestinal parasites overall, as well as for Ciliophora group, coccidia, T. suis, S. ransomi, and strongyles specifically; that is, pigs that consumed water from this type of waterer were between 2.8 and 43.6 times more likely to have a parasitic infection than those that drank water from nipple-type or suspended devices. In addition, not providing any antiparasitic drugs and using medicine such as piperazine, fenbendazole, or levamisole were significantly associated with a greater frequency of gastrointestinal parasites, and several specific taxa were detected (p ≤ 0.05). Specifically, the pigs that received this type of treatment were at least 10.6 times more likely to be infected than those receiving antiparasitic drugs based on macrocyclic lactones (Table 4).

Other variables were also identified as risk factors for the presence of specific parasites, including the lack of a quarantine protocol for Ciliophora group, coccidia, A. suum, T. suis, and strongyles; the absence of a heat source such as creep for A. suum, S. ransomi, and strongyles; and the lack of tools that promote animal welfare for S. ransomi and strongyles. Raising pigs on family farms, splashing water on the animals, and providing food scraps and agricultural by-products were risk factors for the presence of coccidia and strongyles in pig herds. The occurrence of diarrhea and cleaning the facilities directly with water were also associated with coccidia and T. suis infections (Table 4). Other factors were associated with infections of specific individual parasitic taxa, as shown in Table 4.

Quantitative estimation of parasitic load using a parasitological technique

Of the 1,148 fecal samples from pigs included in this study, 957 (83.36%) had a weight equal to or greater than 5 g of feces and were subjected to the quantitative FLOTAC technique to estimate the parasite load. The greatest mean EPG values for all nematode taxa, represented by the egg counts determined with the quantitative FLOTAC technique, were observed in samples obtained from pigs kept on family farms. High coefficients of variation in egg counts were observed in the fecal samples of pigs from both family farms and industrial farms; however, the greatest coefficients were observed in the samples from the industrial farms. In general, statistically significant differences (p < 0.0001) in EPG values between the types of properties (family versus industrial) were detected. Most of the samples with EPG values above 500, which is considered a high parasite load, were from pigs raised mainly on family farms (Table 5).

Table 5.

Comparison of EPG values between family and industrial pig farms

Parasites	Type of farm	Min–Max	Mean	SD	CV (%)	Mann–Whitney	Frequency
						p value	0–500	≥ 500
Ascaris suum	Family	1–8336	137.4	767.6	558.66	< 0.0001	231 (77.2%)	10 (3.3%)
	Industrial	1–4	0.02	0.22	992.78		707 (83.2%)	0
Trichuris suis	Family	1–3438	64.38	342.49	532.01	< 0.0001	235 (78.5%)	6 (2%)
	Industrial	1–3290	16.89	150.79	892.57		702 (82.6%)	5 (0.5%)
Strongyloides ransomi	Family	1–8765	93.14	594.85	638.69	< 0.0001	235 (78.5%)	12 (4%)
	Industrial	1	0.001	0.038	2660.83		1 (0.1%)	0
Strongyles	Family	1–1344	79.14	180.84	228.51	< 0.0001	237 (79.2%)	12 (4%)
	Industrial	1–9	0.05	0.48	1003.33		707 (83.2%)	0

Statistically significant p value: p ≤ 0.05. Low-to-moderate EPG parasite load: 0–500; high EPG parasite load: ≥ 500. Adapted from Nwafor et al. (2019)

SD standard deviation, CV coefficient of variation

Extension activities conducted with rural producers

In general, the producers actively participated in the extension activities, particularly the interactive lecture using the book “Parasites and the Importance of Their Control” by asking questions and talking about the subject. During that activity, family farmers reported raising pigs for consumption and small financial transactions, and producers on both family farms and industrial farms were unaware of the damage caused by the parasites to the animals or of the existence of zoonotic protozoa that can be excreted in the feces of pigs.

Additionally, through the “happy pig and sad pig” extension activity, which is a self-recognition activity, the producers recognized inadequacies in their animal production. The main inadequacies observed in this activity were the habit of not removing feces and food scraps from the facilities before washing (question 3 Table 6) and not performing a periodic deeper wash with the use of detergents, water, and a broom (question 4 Table 6). In the “homework correction” activity, producers from both types of pig farms remembered almost all the information provided during the visits by the team. On family farm K, the person responsible for the animals reported that he provided the pigs with feed of unknown human origin because he did not have the financial resources to afford higher quality feed, and on family farm A, the person responsible for the animals either did not understand the question or did not remember the provided information regarding antiparasitic drugs, giving a shorter answer than expected for question 8 in this block (Table 6).

Table 6.

Results of extension activities completed by pig producers

“Happy pig and sad pig” activity	Yes	No
1) Use protective equipment for handling animals	13 (86.6%)	2 (13.3%)
2) Use cleaning utensils for facility hygiene	15 (100%)	0
3) Remove feces and dry food debris from pens	7 (46.6%)	8 (53.3%)
4) Washing the pens with detergent, water and a broom	4 (26.6%)	11 (73.3%)
5) Washing containers intended for supplying water and food daily	11 (73.3%)	4 (26.6%)
6) Provide water and food daily for animals	14 (93.3%)	1 (6.6%)
7) Provide pregnant females with a clean environment, dry and with straw bed	15 (100%)	0
8) Don’t provide spoiled or sour food to animals	13 (86.6%)	2 (13.3%)
9) Seek professional help for diagnosis and treatment of animals	15 (100%)	0
10) Don’t leave animals in dirty enclosures, wet or muddy	14 (93.3%)	1 (6.6%)
“Homework correction” activity	Yes	No
1) We can use the same everyday clothes to handle pigs	0	15 (100%)
2) Cleaning utensils used to clean your home can also be used to clean animal enclosures	0	15 (100%)
3) Feces and food debris must be removed from animal enclosures daily	15 (100%)	0
4) Water can only be supplied to pigs once a week	0	15 (100%)
5) Water and food are provided in places that don’t need to be clean	0	15 (100%)
6) I always provide my animals with leftover food of unknown origin	1 (6.6%)	14 (93.3%)
7) Pregnant females must be kept in clean enclosures, dry and with straw bed	15 (100%)	0
8) Antiparasitic must be provided to animals at regular intervals	14 (93.3%)	1 (6.6%)
9) With the activities carried out in this project it became clear that some intestinal parasites can be transmitted from pigs to humans	15 (100%)	0
10) Intestinal parasites cause harm to the health of humans and pigs, as well as economic losses for the producer	15 (100%)	0

Discussion

When integrating the parasitological results obtained from family and industrial farms located in different municipalities of Rio de Janeiro and Minas Gerais, the overall percentage of samples positive for parasites was 69.9%. These pathogens were detected with the greatest frequency in pigs raised on family farms, with an overall detection frequency greater than 90%. Gastrointestinal parasites have been detected in pig feces at frequencies equal to or greater than 90% on family farms in Africa, Brazil specifically in the state of Sergipe, and other cities in Rio de Janeiro, Colombia, and Argentina (Kagira et al. 2008; Brito et al. 2012; Barbosa et al. 2015; Pinilla et al. 2020; Addy et al. 2023; Alegre et al. 2024). The frequencies of positive parasitic samples reported in epidemiological studies conducted in Venezuela, Ethiopia, India, Uganda, other states and cities in Brazil, Nigeria, Korea, and Thailand, all of which included family type pig farms, ranged from 13.2 to 79.5%, which was lower than the frequency in the present parasitological survey (Perfetti et al. 2012; Kumsa and Kifle 2014; Dadas et al. 2016; Roesel et al. 2017; Araújo et al. 2019; Class et al. 2020, 2022; Mattos et al. 2020; Omoruyi and Agbinone 2020; Charitha et al. 2022; Lee et al. 2022; Thanasuwan et al. 2024).

Notably, most of the farms included in this study were family type; that is, they were traditional farms with simpler facilities that used the property’s own structural resources. The main objectives of these farms are the subsistence of the producers or providing a source of income for the nuclear family, who usually manage the animals directly. This production model is an important source of income for Brazil and other developing nations (Silva Filha et al. 2008; Araújo et al. 2019; Class et al. 2020). The high positivity of gastrointestinal parasites in this study demonstrates the urgent need for the government to invest in these small producers through the creation of cooperatives that aim to organize and officialize these production systems so that they can be officially recognized, invest in animal health and consequently in the control of these parasitic agents. Because family pig farms have less financial investment, the greater prevalence rates of parasites than those of industrial farms were expected. Moreover, it is important to note that most of these farms had a small number of pigs, resulting in low financial returns for the producers, which limited their ability to invest in improvements to the farm, including sanitary management practices for parasite control.

Although the overall positivity observed in the samples from the industrial farms (61.6%) was below the index observed in the family farms, the estimated prevalence was still greater than those reported in other studies that analyzed the feces of pigs reared under this system. These studies were conducted in Brazil, China, Nigeria, and Italy (Nishi et al. 2000, D’Alencar et al. 2011; Lin et al. 2013; Barbosa et al. 2015; Allievi et al. 2024). Among the four industrial farms included in the present study, three (L, N, and O) belonged to public teaching institutions; both protozoa and helminths were identified in these farms. In these institutions, the professionals reported that laws and bidding processes had to be followed for the acquisition of any products, materials, equipment, and supplies, including medicine, feed, and materials for cleaning the facilities. Therefore, even though the professionals are committed to raising animals, the numerous legal requirements of the national public system and the complexity of the bidding process make it difficult to acquire materials that are essential for sophisticated sanitary management and adequate parasite control. This problem may have been reflected in the parasitic frequency detected in this study.

The different frequencies detected in previous parasitological surveys compared with those in this study may be related to the different sample sizes or the use of only one laboratory test to recover parasitic structures of different shapes and densities. In addition, the geographical location of the farms and, more than anything, the management employed may also have influenced parasitic positivity. These factors complicated comparisons of the epidemiological indices among the different studies.

In general, protozoa were detected more frequently than helminths were, and the most common parasites that naturally infect pigs were cysts and trophozoites of Ciliophora group, which are morphologically compatible with B. coli. Consistent with the present study, this parasite taxon was the most commonly reported in other parasitological surveys of pigs conducted in different countries, such as Brazil, China, Spain, Venezuela, the Philippines, Colombia, Romania, and Korea (Nishi et al. 2000; Weng et al. 2005; Bornay-Linares et al. 2006; Antunes et al. 2011; Lai et al. 2011; Brito et al. 2012; Perfetti et al. 2012; Barbosa et al. 2015; Ybañez et al. 2018; Pinilla et al. 2020; Class et al. 2022; Băieş et al. 2022; Lee et al. 2022).

Although pigs are considered the main hosts of B. coli, in this study, the taxonomic name of the Ciliophora group was used because confirmation of B. coli can be performed only by more sophisticated laboratory techniques, such as molecular techniques. Notably, B. coli is a parasite with the potential for zoonotic transmission that can lead to severe clinical manifestations in humans (Silva et al. 2021). However, for pigs, no zootechnical or clinical studies have evaluated the true impact of this infection on the health and welfare of the animals or the economic impact on pig farming.

Parasitic structures from the Ciliophora group were detected in pigs raised on both family-run and industrial farms, including animals of both sexes and all age groups. However, in the animals from the industrial farms, the forms of this parasite were mainly detected in animals in the fattening phase. Similar results have been reported on farms in Venezuela, Brazil, and Greece (Perfetti et al. 2012; Symeonidou et al. 2020; Barbosa et al. 2015; Class et al. 2020, 2022). The higher infection rate in pigs in the fattening phase may be related to the following reasons: (i) The exposure to the environment contaminated with cysts is longer in the fattening phase than in the nursery phase. (ii) Pigs in the nursery phase are kept in collective pens that favor their coprophagous habit until the fattening phase. (iii) Pigs in the fattening phase have a voracious appetite; therefore, they receive a diet with a high carbohydrate content, which is one of the main energy sources for ciliate parasites, stimulating the development of this protozoan in this host.

Among the risk factors associated with parasitic infection, the placement of watering systems directly on the floor of the pens, which mainly occurs on family farms, may favor the contamination of drinking water with feces contaminated with the cystic forms of the Ciliophora group, predisposing the animal to reinfection. In addition, the failure to enforce quarantine, a period of confinement in isolation to verify a possible infection or disease, especially in newly acquired animals in the herd, was one of the reported risk factors to favor parasitic infection and maintenance in the herds included in this parasitological survey.

Oocysts of non-sporulated coccidia, like those of Eimeria sp. and Cystoisospora suis, were also detected in fecal samples from all pig farms and were predominant in the samples from family farms. Similar results were observed in other studies that included pigs from both family and industrial farms located in China, Brazil, and Nepal (Lai et al. 2011; Barbosa et al. 2015; Chaudhary et al. 2023). The high frequency of these parasites on family farms was related to cleaning the enclosures with water alone. In addition, the positive results appear to be directly related to the lack of financial resources and knowledge on the part of the producers of the importance of supplying a coccidiostat such as toltrazuril in the first days of life of pigs, since these behaviors were observed only in industrial farms M and N.

Despite the high positive rate of infection, most of the animals included in the study had no diarrhea episodes. The suckling piglet is the age group most susceptible to diarrhea and reduced weight gain that are typical of coccidiosis (Shrestha et al. 2015). However, to preserve animal welfare, feces from suckling piglets were not included in this study because of the high sensitivity of this age group. Nevertheless, the identification of coccidia in the feces of the other age groups in this study suggests that these animals may act as a source of infection for the next generation of piglets, especially the sows and the previous litter that has already contaminated the pens.

Other factors were directly associated with infection by this group of parasites, such as the habit of splashing water on the animals to cool them. Because Rio de Janeiro is a tropical, hot, and humid state, the practice of splashing water on an animal’s body has also been reported in other studies conducted in the same state (Class et al. 2020, 2022). This behavior may have favored the dispersion and viability of oocysts in the environment owing to the increase in humidity in the pens. In addition, placing the watering systems directly on the floor, leading to contamination of the drinking water, and the supply of food remnants to the animals were also linked to infection. Pigs are considered feed recyclers; that is, they can convert feed of low nutritional quality into animal protein (Silva Filha et al. 2008). Nevertheless, the use of leftovers as animal diets can generate inflammation in the intestinal mucosa, increasing the susceptibility of animals to infections by intracellular parasites, such as Eimeria sp. and C. suis.

The helminths most frequently detected in the fecal samples of the animals were T. suis and strongyles, followed by S. ransomi and A. suum. The predominance of T. suis and strongyles in pig feces has also been observed in family farms in intensive farming in Nigeria and Brazil and in the industrial farms in France (Rocha and Silva et al. 2015; Delsart et al. 2022).

In general, strongyle eggs are the parasitic forms most commonly detected in pig feces, regardless of the production system, in other countries, such as Uganda, Poland, Colombia, Sweden, India, Thailand, and Argentina (Pinto et al. 2007; Antunes et al. 2011; Brito et al. 2012; Barbosa et al. 2015; Loddi et al. 2015; Carreiro et al. 2016; Roesel et al. 2017; Kochanowski et al. 2017; Class et al. 2020; Melo et al. 2020; Pradella et al. 2020; Pinilla et al. 2020; Class et al. 2022; Charitha et al. 2022; Machado et al. 2022; Jankowska-Makosa et al. 2023; Thanasuwan et al. 2024; Alegre et al. 2024).

The persistence of strongyles in pig farms should always be given close attention, as the larvae of this nematode may remain in hypobiosis in the stomach and intestinal mucosa of the animals. In the case of sows close to the farrowing period, hormonal changes and climatic conditions can stimulate the larvae to leave hypobiosis and become adult parasites during the lactation period, i.e., when these animals require high energy expenditure. Notably, strongyles, especially Hyostrongylus rubidus and Oesophagostomum spp., can cause significant economic losses in pig production, since sows infected by these nematodes can develop “lean sow syndrome,” a condition diagnosed in sows during the suckling period of piglets (Roepstorff and Nansen 1996).

Although the diagnosis of A. suum was lower compared to other intestinal nematodes, it was still detected—mainly in family farms in Rio de Janeiro and in industrial farms in both Rio de Janeiro and Minas Gerais. Overall, this parasite has been consistently reported in pig farms in these states (Barbosa et al. 2015; Class et al. 2020, 2022; Fausto et al. 2015). This nematode is known to be extremely important in pig farming owing to its impact on productivity, particularly by reducing weight gain (Roepstorff and Nansen 1996). Moreover, pig livers may be discarded in slaughterhouses due to the presence of “milk spots,” a pathology caused by larval migration through liver tissue (Fausto et al. 2015). However, liver condemnation is rare on family farms, where most animals are slaughtered without official meat inspection (Class et al. 2020).

Although nematodes were more frequently detected in the feces of pigs kept on family farms, they were also detected in pigs from industrial farms with a wide range of EPG values. This variation highlights that even within the same production system, the sanitary management methods used to control nematodes are diverse. In general, massive parasitic infections (EPG greater than 500) were concentrated mainly in family farms.

The greatest number of nematodes was detected in pigs kept on farms that did not have a program for the supply of antiparasitic or administered medicine that did not contain macrocyclic lactones with active constituents, highlighting most of the family farms in this group. These nematodes, especially T. suis identified on industrial farm O with EPG values greater than 500, may also be linked to problems supplying antiparasitic drugs, as reported by the producer, or even to possible resistance of the parasites to routinely used antiparasitic drugs.

Additionally, the climate of the Brazilian states where the farms are located should be considered when analyzing parasite frequency. According to the Köppen-Geiger classification, the climate in the state of Rio de Janeiro is classified as Aw and Af (tropical humid and superhumid), and that of the cities of Minas Gerais varies between Aw and Cwb (tropical and subtropical altitudes), with high annual rainfall above 1500 mm (Embrapa 2025). The combination of this set of climatic factors favors the faster development and maintenance of the infective forms of these parasites in the environment, emphasizing the need for even more frequent cleaning of facilities in properties located in tropical countries.

In addition to climatic conditions, the socioeconomic context in which pig farmers in Brazil are situated must also be considered when evaluating the frequency of gastrointestinal parasites in animals. The highest poverty rates in Brazil are found among individuals with low levels of education and without formal, legal employment—a profile commonly seen among family farmers (IBGE 2024). Although these producers wish to improve their herds, they often lack both the technical knowledge and the financial support needed to succeed in controlling these parasitic agents.

On the industrial farms, the breeding boars were mainly diagnosed with A. suum and the fattening pigs with T. suis. These results are consistent with findings from industrial pig farms in China, Brazil, and Nigeria and organic pig farms in the USA (Weng et al. 2005; Barbosa et al. 2015; Mattos et al. 2020; Amadi et al. 2018; Li et al. 2022). The detection of these parasite taxa in these pigs’ categories was expected because the prepatent period of these nematodes varies between 6 and 8 weeks, during which the animal has already been transferred to the fattening sector or classified as sire, sow, or boar. Infections by these parasites are usually subclinical and go unnoticed on farms because they do not affect behavior; however, they can impact feed conversion in the fattening sector because the parasite competes for nutrients (Roepstorff and Nansen 1996). This situation should be considered carefully because, in the present study, pigs infected with T. suis did not show any clinical changes during the sample collection period. This problem is even more acute for those who raise pigs as a primary source of income, as is the case for some family farmers who participated in this study.

In addition to these factors, the restricted supply of water for the pigs to drink and the application of lime to the walls of the pens had a significant effect on the presence of A. suum, and the lack of a creep/heat source had a significant effect on A. suum, strongyles, and S. ransomi. An ad libitum water supply is essential because it enables the maintenance of the hydroelectrolytic balance and body temperature of the animal (Mroz et al. 1995), which may minimize the colonization of parasites in the gastrointestinal tract. Few producers have reported the use of lime on the walls and other structures of the facilities, and this deficiency is related mainly to the lack of knowledge of the microbicidal action of this substance, which could act as another factor in the control of these pathogens. Because pigs have difficulty warming up and maintaining thermal comfort, the limited use of heat sources such as creepers, incandescent lamps, and straw bedding in pens can also trigger homeostatic imbalances favoring infections caused by the parasitic agents highlighted above.

In this study, the frequency of T. suis infection was also directly linked to a lack of roofs on the pens, cleaning the enclosure with water only, and a lack of a sanitary break (downtime). The precarious infrastructure observed in some family farms, including the lack of roofs on the premises, leaves the animals vulnerable to environmental factors, which may increase their susceptibility to infection by nematodes. In addition, cleaning the animals’ enclosures with water alone may not be sufficient to remove T. suis eggs from the enclosures, even though no accumulation of excreta was observed on the floors. T. suis is a geohelminth that produces eggs that are extremely resistant to the environment (Szuba et al. 2024). Thus, deep cleaning, which includes disinfection and the sanitary break (downtime), should be encouraged to remove these resistant structures as much as possible. The problem of cleaning and the inefficient sanitary break (downtime) does not occur only in family farms in developing countries such as Brazil; once, this situation has previously been reported in industrial production in Sweden (Pettersson et al. 2021).

During the extension activities, especially during the “happy pig and sad pig” activity, the team advised that the feces should be routinely removed from the environment by dry cleaning before proceeding with the washing process, at least once a day. In addition, the team also recommended that it would be ideal to periodically wash the environment with at least neutral detergent to facilitate the removal of the remaining organic matter from the pens and the mechanical removal of parasitic structures such as eggs, larvae, cysts, and oocysts.

Another extremely relevant risk factor for infection by T. suis, strongyles, and S. ransomi was the placement of watering systems directly on the floor of the pens. This risk factor was also noted for Ciliophora group and coccidia, emphasizing that placing any water or food storage vessels on the floor should be completely avoided because of the high fecal volume excreted in the environment of pigs, which are usually housed in groups. Thus, suspended or nipple-type watering systems should be implemented because this style facilitates cleaning and access for animals, preventing water waste and contamination (D’Alencar et al. 2011).

Specifically, for S. ransomi, the disposal of untreated feces into the environment was a relevant and concerning factor. Although this subject has rarely been explored in the literature, the environmental resources in the locations where these excreta are disposed of cannot be ignored because they are fundamental for supplying the property with drinking water, which may already be contaminated when provided to the pigs and harbor other infectious agents with zoonotic potential for humans. During the fieldwork, the team noted the presence of flies in the pens inside the farms; as expected, the insect, acting as a mechanical vector, was also associated with the frequency of infection with this nematode. The potential of Musca domestica to carry the eggs and larvae of helminths that infect pigs was previously demonstrated in a study conducted in Germany (Förster et al. 2009). Owing to these observations, during the extension activities, the team explained the indirect and direct aggressions caused by these insects on pig farms to the producers.

A major problem observed on the pig farms was the physical structure, which, despite being masonry, did not receive periodic maintenance in many facilities. As a result, cemented floors were worn, with crevices and cracks. This condition may hinder the cleaning of the floor of the pens and, in this study, may have affected the presence of strongyles. A cement floor has been identified as a risk factor for infection with gastrointestinal parasites in pigs in studies conducted in Kenya, the Philippines, Brazil, and Italy (Kagira et al. 2008; Ybañez et al. 2018; Class et al. 2022; Class et al. 2022; Allievi et al. 2024). In addition, the habit of splashing water on the animals’ body to cool them off, the provision of food remnants of unknown quality to the animals, and the failure to enforce the practice of quarantine as indicated for coccidia were clear risk factors for infection with the group of strongyles.

In this study, several variables were thoroughly evaluated as risk factors for infection by gastrointestinal parasites, including variables inherent to the physical structure of the property, those of the animals themselves, and those that are directly related to management. During the technical visits, the presence of enrichment elements such as chains, plastic containers, tires, and ropes, which were suspended at a comfortable height for the animals to browse and play, was also observed in the pens. It is worth noting that these utensils distract the animals and the lack of them can reinforce the pigs’ coprophagic habits. Unfortunately, comparisons of these results with the literature were limited because no studies that had previously evaluated this variable were retrieved.

Other parasites with zoonotic potential, such as Blastocystis sp., Entamoeba sp., and Hymenolepis sp., were also detected in pig feces. Notably, the identification of eggs of Hymenolepis sp. was an intriguing finding because it highlights the pseudoparasitism of pigs through the ingestion of feces from other animals, such as rodents, and predation on rodents and even infected arthropods that act as intermediate hosts. Similar results have been reported for family farms in Venezuela and industrial farms in Italy (Perfetti et al. 2012; Alievi et al. 2024).

During the extension activities, including the lecture “Parasites and the importance of their control” conducted using a comprehensive book, the producers and other family members interacted with the team members, answering questions and posting reports of their daily lives. In addition, the use of real images in this comprehensive book was found to be a good communication strategy because the producers recognized situations similar to those experienced in the routine of pig farming. During the subsequent dynamics of the “happy pig and sad pig,” the producers were given the opportunity to recognize and qualify their behaviors regarding the management of the animals. All producers participated in a unique way in the activities, which resulted in self-reflection on possible improvements. Although this study encompassed a substantial sample size of pigs, certain limitations should be acknowledged. Fecal samples from suckling piglets were not collected owing to the fragility of this age group and the limited quantity of fecal material available. Moreover, the lack of molecular techniques, mainly due to financial constraints, ultimately prevented a more specific taxonomic identification of certain parasitic taxa.

This study underscores the high prevalence of gastrointestinal parasites in pig farms, particularly in family-run systems, which exhibited the highest EPG values for helminths. Protozoa from the Ciliophora group, consistent with B. coli, emerged as the most frequently detected taxa. In industrial farms, the Ciliophora group was primarily identified in pigs at the fattening stage. In general, several risk factors were repeatedly identified for multiple parasite taxa. This situation may have favored the cases of polyparasitism observed in the present study. Thus, the results generated by this study highlight the need for improvements in national pig production, including the creation and implementation of programs targeting rural areas that facilitate the acquisition of credit by rural producers so that they can invest in improvements in infrastructure and the purchase of materials. In addition, it is essential that public technical assistance and rural extension companies carry out more training, refresher, and updating activities for pig producers through workshops, lectures, and field days that include the provision of information on infectious agents in pigs and their control methods.

Author contribution

C.S.C.C,R.S.F,A.L.S.A,I.S.R,B.T.S,F.B.K.,L.L.C,J.A.A,M.J.M.A.,D.C.T and A.S.B. performed the experiments, conceived the experiments and analyzed the data. C.S.C.C., R.J.P.D. and A.S.B. wrote the manuscript. C.S.C.C., R.J.P.D. and A.S.B. supervised the project, conceived the experiments, analyzed the data, acquired the funding, reviewed and edited the manuscript. All authors contributed to the article and approved the submitted version.

Funding

This study was supported by the Rio de Janeiro State Research Support Foundation (FAPERJ) through the Support Program for Young Female Scientists with Links to ICTs in the State of Rio de Janeiro (E-26/210.041/2024) and the Young Scientist of Our State Grant (FAPERJ E-26/204.492/2024); the Productivity Grant from the National Council for Scientific and Technological Development (CNPq 312037/2022–8); and Research Support Foundation of the State of Minas Gerais/FAPEMIG (APQ-02984–24).

Data availability

No datasets were generated or analysed during the current study.

Declarations

Ethics approval

This study was approved by the Committee on Ethics in the Use of Animals of Fluminense Federal University (CEUA/UFF; Protocol No. 8394191222). It was also approved by the Committees on Ethics in the Use of Animals of each Federal Institute of Education, Science and Technology that participated in this study (Registration Nos. 03/2022 and 02/2023). Furthermore, this study was approved by the Ethics Committee on Human Research (CEP/UFF; No. 5,966,227; CAAE: 63709022.0.0000.5243; CEP/IFRJ; No. 6,045.672; CAAE: 63709022.0.3003.5268; CEP/IFMG; No. 6,072.109; CAAE: 63709022.0.3002.5588).

Consent to participate

Not applicable.

Consent for publication

All authors approved the publication of the manuscript.

Competing interests

The authors declare no competing interests.