ORIGINAL

Presence of gastrointestinal parasites in swine and human of four swine production farms in Cundinamarca- Colombia

Presencia de parásitos gastrointestinales en cerdos y humanos de cuatro granjas porcícolas de Cundinamarca- Colombia

María F Mendoza-Gómez,¹ Bact, Adriana Pulido-Villamarín,¹* M.Sc, Angélica Barbosa-Buitrago,² MV, Moisés Aranda-Silva,³ M.Sc.

¹ Pontificia Universidad Javeriana, Facultad de Ciencias, Departamento de Microbiología, Unidad de Investigaciones Agropecuarias (UNIDIA). Bogotá, Colombia. Carrera 7° N° 43-82 Edificio 52 Oficina 608, Telf 57-1-3208320 ext 4020.
² Universidad El Bosque Maestría en Ciencias Biomédicas, Práctica privada. Bogotá, Colombia.
³ Pontificia Universidad Javeriana, Facultad de Ciencias, Departamento de Matemáticas. Bogotá, Colombia.

*Correspondence: adriana.pulido@javeriana.edu.co

Received: February 2015; Acepted: May 2015.

ABSTRACT

Objective. Determine the presence and the type of endoparasites with zoonotic potential in swine and human of two technified and two semi-technified farms in the department of Cundinamarca, Colombia. Materials and methods. Three serial samplings of feces were taken in a pen row within intervals of 15 days, in two technified and two semi-technified farms in different age groups distributed as follows: pregnant-sows, nursing-females, boars, weaners, suckling-piglets, and growing-pig. By means of informed consent thirty-three people agreed to enter the study. Thirty-three samples from men and women of different ages were received. The pool and individual samples of fecal were evaluated by direct analysis, qualitative flotation and sedimentation techniques and modified Ziehl-Neelsen stain. Results. For the porcine population, on the average, the results obtained from both technified farms showed that Balantidium coli (42%), Endolimax nana (21.9%) and Iodamoeba bütschlii (7.8%) were the most common parasites. In semi-technified farms they were: Entamoeba coli (40%), Endolimax nana (35%), Iodamoeba bütschlii (25%) and Balantidium coli (5%). By means of the test chi² it is possible to conclude that there is a significant difference between the parasites species and the type of farm. The results obtained in human showed the presence of parasites as: E. coli (42.2%), Entamoeba hystolitica/dispar (12.1%), E. nana (9.1%), B. coli (9.1%), I. bütschlii (3.0%) and Blastocystis hominis (3.0%). Conclusions. The presence of parasites such as Balantidium coli, Endolimax nana, Iodamoeba bütschlii and Entamoeba coli in swine and human suggests a possible rotation of parasitic species between hosts.

Key words: Parasites, swine, zoonoses (Source: DeSC).

RESUMEN

Objetivo. Determinar la presencia y el tipo de endoparásitos con potencial zoonótico en porcinos y humanos de dos granjas tecnificadas y dos semi-tecnificadas del departamento de Cundinamarca-Colombia. Materiales y métodos. Se realizaron tres muestreos seriados de materia fecal con intervalos de 15 días, en dos granjas tecnificadas (92 muestras) y dos semi-tecnificadas (60 muestras) en diferentes grupos etarios distribuidos así: Hembras de cría, hembras de reemplazo, reproductores, lechones, pre-cebo y ceba. Se recibieron 33 muestras de hombres y mujeres de diferentes edades, que mediante consentimiento informado asintieron participar en el estudio. Las muestras de materia fecal colectivas e individuales (de humanos y de cerdos) fueron evaluadas mediante: Análisis directo, técnica de flotación cualitativa, técnica de sedimentación cualitativa y tinción de Ziehl-Neelsen modificado. Resultados. En promedio para la población porcina, los resultados obtenidos de las dos granjas tecnificadas mostraron que los parásitos en común son Balantidium coli (42%), Endolimax nana (21.9%) y Iodamoeba bütschlii (7.8%). En las dos granjas semi-tecnificadas: Entamoeba coli (40%), Endolimax nana (35%), Iodamoeba bütschlii (25%) y Balantidium coli (5%). Por medio de la prueba chi² se puede concluir que hay una diferencia significativa entre la especie de parásitos y el tipo de granja. Los resultados obtenidos en humanos mostraron la presencia de parásitos como: E. coli (42.2%), Entamoeba hystolitica/dispar (12.1%), E. nana (9.1%), B. coli (9.1%), I. bütschlii (3.0%) y Blastocystis hominis (3.0%). Conclusiones. La presencia de parásitos como Balantidium coli, Endolimax nana, Iodamoeba bütschlii y Entamoeba coli en cerdos y humanos sugiere una posible rotación de especies parásitas entre los hospedadores.

Palabras clave: Parásitos, porcinos, zoonosis (Fuente: DeSC).

INTRODUCTION

In Colombia, during the year 2013 the porcine production was 670.612 animals, to which Cundinamarca contributed 4.98% (1); 1.458.179 pigs were slaughtered for human consumption between January and June of 2013, Cundinamarca contributed 20.1% (650.035 pigs)(1).

This type of animal production is affected by the presence of parasites that limit the productive potential of the animals, thus affecting the average daily weight gain, causing heterogeneous lots as well as facilitating weight decrease during weaning, which seems reflected in the alteration of the food conversion indexes and further represents an increase in the time required before slaughter (2). It is important to note the rate of prevalence and the economic importance of the parasites changes depending on the management system, the housing characteristics, the hygienic-sanitary measures, the geographic location and the age of the pig. Thus, all these variables influence the basic requirements of every stage of the parasitic cycle, in both the mechanisms of transmission and the immune response of the host (3).

The parasites that have a major impact on health and porcine production are protozoan parasites such as Eimeria spp., Isospora spp. and Balantidium spp. ; worm infections reported were primarily nematodes (such as Trichinella spp., Strongylus spp., Ascaris spp., Trichuris spp., Oesophagostomum spp. and MetaStrongylus spp. ) secondarily trematodes (such as Fasciola spp. and Dicrocoelium spp. ) and finally cestodes (such as Echinococcus spp. and Taenia solium) (4,5). Many of these pathogens affect porcine production and can be transmitted to humans, and are recognized as zoonotic agents (6) among these we can find Balantidium coli, Toxoplasma gondii, Cryptosporidium spp. and Taenia solium (7).

In Colombia, few epidemiological studies have been made in the matter, which is why not much information is known about the prevalence of porcine parasites. Therefore, it is of vital importance to conduct studies on the topic in order to know which are really parasites of zoonotic importance in this country. Thus the goal of this study was to determine the presence of gastrointestinal parasites (GIP) in swine and human who could be involved with zoonoses at four swine farms in the department of Cundinamarca - Colombia.

MATERIALS AND METHODS

Farm’s Location. Two technified swine farms (T) (≥ 200 females) and two semi-technified farms (ST) (≤ 200 females) with a complete cycle of production with an all in/all out system (AI-AO), were chosen in the following locations

Farm 1 (T1): Located at a height of 1.728 (m.a.s.l. ), with an average temperature of 20°C (8) and a population of 3654 pigs.

Farm 2 (T2): Located at a height of 2.586 (m.a.s.l. ), with an average temperature of 14°C (8) and a population of 2156 pigs.

Farm 3 (ST1): Located at a height of 1.867 (m.a.s.l. ), with an average temperature of 20°C (9) and a population of 244 pigs.

Farm 4 (ST2): Located at a height of 1.384 (m.a.s.l. ), with an average temperature of 20°C (9) and a population of 125 pigs.

Sample size. Bearing in mind that the total population was less than a 100.000 (finite population), the following formula was used to calculate the sampling size (Table 1).

Where:

Z: Level of certainty
p: Estimator of the proportion according to the hypothesis to be analyzed (55% average prevalence reported) (10-12)
q: 1-p
N: Total number of individuals or units in the study
E: Error component for this calculation (10%).

Sample collection. Collective and individual samples (Figure 1) were obtained according to the phases of the productive cycle as follows:

Group 1 Individual Samples: Pregnant sows, Nursing Females, boars.

Group 2 Collective Samples: Weaners, Suckling Piglets, Growing-pig.

Three samples were taken within an interval of 15 days each.

The farm workers and some of their relatives gave us a stool sample; 18 samples were received (12 men, 4 women and 2 children) from the technified farms, and 15 samples (7 men, 5 women and 3 children) from the semi-technified farms.

Ethical aspects. The animal management of the and the samples were taken according with Colombian laws (Decree 2257 of 1986, Article 49 and Resolution 8430 of 1993 TITLE IV: Regarding Research bio-safety, CHAPTER I Regarding research with pathogenic microorganisms or biological material that may contain them concerning research activities related to investigation, prevention and control of zoonosis).

Everyone that entered the study signed an informed consent form as established in Decree 3380 of 1981 Article 10 of Law 23 of 1981 wherein medical ethic laws are established.

Sample processing

Macroscopic and microscopic approach. Macroscopic aspects such as color, consistency, presence of mucus, blood and/or parasites/fragments were evaluated.

A direct examination was conducted in saline and lugol solution, under 10x and 40x magnification; the report of the results obtained was made using a semi quantitative scale with crosses, as follows:

One cross (+) if 1 to 3 parasites per field are present.
Two crosses (++) if 4 to 7 parasites per field are present.
Three crosses (+++) if 8 to 10 parasites per field are present.
Four crosses (++++) if more than 10 parasites per field are present. (13,14)

Semi quantitative concentration method based on flotation. 2 g of fecal matter were deposited in a wide flask with a saturated solution of sodium chloride and glucose, the procedure was made according to what is established in the guide RVC/FAO (15). A direct examination was conducted in the microscope, under 10x and 40x magnification; the report of the results obtained was made using a semi quantitative scale with crosses as previous described (13, 14).

Semi quantitative concentration method based on sedimentation. 2 g of fecal matter were homogenized in water; the procedure was made according to what is established in the guide RVC/FAO (15), finally with the aid of a pipette Pasteur the sediment was taken and a drop of it was placed in a microscope slide, using magnification 10x and 40x; the report of the results obtained was made using a semi quantitative scale (13,14).

Ziehl-Neelsen modified method. From the sediment taken, a smear study was made on a slide as follows: first by adding carbol fuchsin for 5 min and then washed with abundant water, later acid alcohol was added up to the complete discoloration for not more than 3 minutes, then methylene blue was applied by 2 min, finally the sample was washed with abundant water. The samples were analyzed under light microscopy using magnifications 40x and 100x (16).

Statistical analysis. To determine the relationship between the parasites species Vs. the production system and the age groups, the statistical test chi² was applied, additionally the portion of parasites was determined by the test of proportion hypothesis. The data analysis obtained in the human samples was done by the presence or absence of parasites.

RESULTS

Porcine population. In the farm T1 a high presence of Balantidium coli 36.6% was found, followed by Ascaris suum 29.2%, Endolimax nana 15.2%, Giardia spp. 12.1% and by a low prevalence of Iodamoeba bütschlii 7.5% and Trichuris suis 4.8%.On the other hand in farm T2 a high presence of B. coli 48.5% and E. nana 26.4% was found, followed by a low presence of I. bütschlii 8.2% and Strongyloides spp. 5.8%. (Table 2)

Fort the semi-technified farms, in ST1 a high presence of I. bütschlii 57.1%, B. coli 33.3%, E. nana 14.2% was found, followed by a low presence of Cryptosporidium spp. 5% and E. coli 4.7%. Finally in farm ST2 the parasites with a high presence were: E. coli 40%, E. nana 35%, I. bütschlii 25%, Isospora spp. 25%, Eimeria spp. 20% and a low presence of B. coli 5%. (Table 3)

Human samples. The parasites observed in the workers of both technified farms were: In farm T1 E. coli 25%, B. coli 25% and E. nana 25% was found. In farm T2 a presence of parasites such as E. coli 35.7% and E. nana by a 7.1% were evident.

In the samples gathered from humans in both semi-technified farms the following parasites were found: E. coli, B. coli, I. bütschlii, Blastocystis hominis y Entamoeba hystolitica/dispar. In the farm ST1 a presence of E. coli 60%, E. hystolitica/ dispar 40%, B. coli 10% and B. hominis 10% was observed. In the farm ST2 E. coli 40% and I. bütschlii 20%.

DISCUSSION

Comparatively, studies made in Asia (China and Turkey) report and average prevalence of B. coli 24.4%, coccidian 24%, Cryptosporidium spp. 8.82%, Ascaris spp. 3.14%, T. suis 5.2% y Giardia spp. 3.78% (12, 17) while in Europe (Germany) a presence of Oesophagostomum spp., A. suum, T. suis and Eimeria spp. in 79%, 7%, 8% y 29% each (11). In Latin America, in countries such as Cuba (18) and Perú (19) an average percentage of Coccidiosis 41.7%, Oesophagostomum spp., 14.9%, T. suis 14.7%, A. suum 6.7% and Strongyloides spp., 5.5% were reported.

In Colombia only a few epidemiological studies about this topic have been made, thus for this reason the data about the prevalence of swine parasites is yet unknown. The results obtained in this study vs other studies related with to the presence of parasites such as B. coli, A. suum, T. suis, Giardia spp., Strongyloides spp., Eimeria spp. and Cryptosporidium spp., match it; whereas differs in the findings of Oesophagostomum spp., because the last one was not found in the present study.

Only few studies refer to these type of gastrointestinal parasites found by age group in swine production; nevertheless, a study made in Cuba reported B. coli in weaners 21%, suckling piglets 20%, growing-pig 30%, females 16% and boars 3%; A. suum in Weaners 12%, suckling piglets 6%, growing-pig, females and boars 0%; T. suis suckling piglets 4%, weaners, growing-pig, females and boars 0%; Strongyloides spp. in weaners 31%, suckling piglets 0%, growing-pig 4%, females 5% and boars 1%; this study determined that the young pigs are more susceptible to parasite infections than adult pigs (20), as it was shown in the current study where young pigs showed a higher presence of some parasites. (Table 2, Table 3).

According to the data obtained and analyzed by means of the statistical chi² test, this study proves the existent relationship between the presence of parasites and the type of farm analyzed (semi-technified and technified farms) with a value of p<0.001 indicating a higher presence of parasites in the semi-technified farms; simultaneously it shows an existent relationship between the presence of parasites and the age group involved with a value of p<0.001. Additionally, when the test of proportion hypothesis was done it was able to determine that B. coli, was found in a higher proportion in technified farms than in semi-technfied farms with a value of p<0.001. E. nana and I. bütschlii were found in a higher proportion in the semi techn farms than techn ones with a value of p<0.01 and p<0.001 respectively.

It is important to acknowledge that the higher prevalence of parasites is found in the nursing females, pregnant sows, weaners and suckling piglets in technified as in semi-technified farms as well, this higher presence in these age groups is possibly given due to the physiological conditions in which the animals are living; in the females, the stress conditions and well as the immune suppression physiological process they deal during their pregnancy period, making them more susceptible to infections by diverse parasites, thus constituting the main source of infection for the weaners (4) additionally, studies have proved that the age of the weaners is a critical factor in parasite infections, due to the high sensibility of piglets to infections by their immune immaturity in their first three days of life, whereas they achieve a high immunity against infections by their 2 week, (4). As a opposing argument to the report of the current study in, the suckling piglets with an average of 5 weeks of life, were found with a higher prevalence of parasites in both types of farms, a 50% in technified farms and a 81.3% in semi-technified farms.

It has been proven that the prevalence of parasites varies depending on the management, location, weather and deworming processes implemented in each one of the farms. (21) One of the reasons why it is believed that the presence of parasites varies from one farm to another is the weather conditions; this data is relevant for the association of certain parasite species, as the samples in both technified farms were done during the months of August and September in 2012, and according to the report by the hydrology, meteorology and environmental studies institute (IDEAM) (9), the Cundinamarca zone showed pluviosity excess (8). This could be related to the absence of some parasites that are reported in literature and were not found in the current study, such as, Oesophagostomum spp., that reports an optimum temperature for its development of 25°C, (10) whereas for Eimeria spp. and Cryptosporidium spp. a temperature between 21 y 22°C is reported and optimal dry conditions for its development and latter infection (21). Thus, the above might be one of the reasons by which these parasites were not found in farms T1 and T2, due to the temperatures and pluviosity in both locations during the months of the study, and so not helping the infection of these parasites.

On the contrary, in the semi-technified farms the presence of Eimeria spp., Isospora spp. and Cryptosporidium spp. were evident and the presence Oesophagostomum spp. was not found, thus this might be related to the weather conditions during the months of April and May of 2013, during which the samples were taken and had a dry weather as reported by IDEAM. (9)

Another important condition related to the prevalence of parasites are the hygienic and sanitary conditions managed by each farm, as it can be clearly seen in the semi-technified farm ST2, were the water used for animal consumption came from a natural source without any type of treatment due to the owner of the farm who considers that the water is completely pure and so it does not need any treatment whatsoever, and thus this might be related to the high prevalence and variety of parasites found there.

In the present study I. bütschlii was found, and it is reported in literature as an intestinal non pathogen amoeba in humans, apes and swine; even though it was described as the most common intestinal amoeba in swine (22) its presence has not been reported in this host; only one study made in twelve boar intestines in Iran during 2004 showed a prevalence of 17% of I. bütschlii (7).

It is of relevance to acknowledge, the presence of Cryptosporidium spp. in a semi-technified farm in a very low proportion (1+) in three different age groups; the infections by this agent have a higher frequency rate in early stages as weaners and suckling piglets, whereas in adults is slightly probable; the absence of this specie in the other farms might be due to the preventive measures taken such as a pretreatment with coccidiostatics in early stages. On the contrary to the report of the literature in the current study there was evidence of the presence of Cryptosporidium spp., in suckling piglets and females stages (23).

The consistency of the fecal matter samples analyzed from humans in its majority was very soft but not watery. According to the results found in the sampling procedure done to some of the workers of both technified and semi-technified farms, a possible zoonotic process might be correlated with B. coli were the pigs the reservoir of the parasite and the main source of infection for the human (24). The presence of this parasite in humans is conditioned to bad health conditions, lack of basic utilities (water, sinks) and the breeding of the swine in open fields (10), this last aspect was not prevalent in the current study, due to the breeding swine in barns; nevertheless, the conditions and sanitary-hygienic habits of the humans are possibly the highest risk factors in the zoonotic processes.

In Latin America, the prevalence of the infection by B. coli ranges between 0.5 and 2.1% (21), showing low among other protozoan intestinal infections. The quality of the water and thus the presence of parasites, to establish with certainty what is the true source of infection and the existence of transmission between species. A wide study done in Bolivia in 2.000 samples of feces coming from Aymara native children from the Bolivian steep lands region, showed a disseminated infection by B. coli with a general prevalence of 1.2%; besides this, swine fecal samples were analyzed, and the results showed that more than half of the swine (n=50) living in this native community were infected by B. coli, wich clearly indicates a zoonotic transmission (5). The illness in swine is asymptomatic, whereas, in humans it might show clinical outcomes ranging from asymptomatic to severe ones, where the asymptomatic ones serve as reservoirs and disseminators of the illness; diarrhea, blood feces, cramps and abdomen pain is shown in the severe ones (5).

A study made in Egypt, showed the presence of de E. coli and E. histolytica/dispar in samples of swine and dogs in a 7.56% y 3.84% respectively, additionally samples of children with diarrhea were analyzed and showed a high prevalence of both species, thus suggesting a possible anthropozoonotic infection with dogs and swine in the area (25). Additionally, during the current study the presence of E. nana was evidenced, and from which its zoonotic potential has not been established yet, but it is said that it might be involved in zoonosis were swine and humans are in high contact with the infective form (Cysts) by water consumption, food or contaminated hands and thus helping the zoonotic pathogens transmission between species, causing disease (7,26).

A study made in the Republic of Korea, related to zoonotic parasites reported that the main parasites with zoonotic potential are E. nana and I. bütschlii, which are protozoans with sapro-zoonotic potential, meaning humans become infected by contaminated food or water with feces of swine, dogs and cattle (7).

Another parasite found was Blastocystis hominis, which pathogen potential in humans and swine is still controversial due to the absence of symptoms, the presence of this microorganism in feces of a variety of animal species such as birds, apes, rodents, amphibians and humans suggests the rotation among them, thus considered a protozoan with zoonotic potential (7,26), also it is associated with the consumption of water, fruits and vegetables contaminated with feces. This parasite is found in a high prevalence in human population, for example, in Argentina in a 43% of children in school age was found, it has been registered in Venezuela with a prevalence of 27%, from which 24% of children in school age, mainly between the age of 9 and 11 years old and 23.9% of the elderly population were infected by this protozoan. (23)

Although in the analyzed humans, were not observed compatible structures with A. suum, T. suis and Cryptosporidium spp., it is of importance to stand out the zoonotic potential of these parasites. Ascaris lumbricoides and Trichuris trichiura, infect more than a thousand million people worldwide (27), the species A. suum and T. suis in swine have a global distribution, due to the presence of infected swine mainly in the production system (27). Swine and humans alike are infected by the ingestion of the eggs that acquire an infectious stage in the environment (26). This type of parasitosis produces high economic impact, due to the frequent delay in growth and diarrhea in swine. The differentiation between human and swine parasites species has been hard and due to this reason the frequency of infection of A. suum and T. suis in humans cannot be determined (26), but a zoonotic implication is not discarded due to it similarity and the possibility to infect humans especially in areas where swine and humans live close to each other or swine feces is used as agricultural fertilizer in vegetables for human consumption or by water pollution and bad hygiene of workers in the swine farms, thus existing a potential risk of crossed infections (27).

The cryptosporidiosis is a disease of high zoonotic importance, known worldwide as a public health problem that affects mainly people that interact with farm animals on a daily basis (5). Generally, the infections by Cryptosporidium in domestic swine are higly frequent in animals between 1 and 6 months old, reaching a prevalence between 24 and 60%; the 16.5% of the adults had an infection by Cryptosporidium spp. (21), this data supports the fact that adult swine are parasited in a lower degree (21). Recent studies have showed the existence of Cryptosporidium suis, finding done by means of molecular biology which evidenced that this is genetically different from the other species of Cryptosporidium known (21).

It is relevant to evidence the presence of pathogens with zoonotic potential, thus they might prove to become relevant public health issues, besides, pitching in knowledge concerning these type of parasites, will make decision making in preventive measures that deny the rotation of parasites between animal and humans.

Infection due to contaminated water, bad human hygienic practices contributes to the transmission of parasites to swine, and thus these act as a reservoir disseminating the parasites by fecal means. When used as agricultural fertilizer it contaminates crops and water supplies acting as a source of infection for humans and animals alike in an endless cycle.

Acknowledgements

Pontificia Javeriana University. Academic research vice direction. Research proposals financed by own resources of the academic units ID PPTA 00004645, ID PRY 004437. Swine producer’s Colombian association, specially the field technicians.

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