Prevalence of Balantidium coli (Malmsten, 1857) infection in swine reared in South Italy: A widespread neglected zoonosis

Abstract

Background and Aim: Balantidiasis, caused by Balantidium coli (syn. Neobalantidium coli or B. coli), represents a neglected parasitic infection of zoonotic significance affecting a variety of hosts, including domestic pigs that are the main reservoir. B. coli has a direct life cycle with a fecal-oral route transmission that occurs mainly by the ingestion of food and water contaminated with cysts. The ingestion of meat contaminated during inappropriate slaughtering processes may represent a new potential route of transmission. Only a few studies have investigated the prevalence of B. coli in domestic pigs in Italy, despite its high prevalence and zoonotic significance. This study aimed to improve the knowledge on B. coli prevalence in domestic swine reared both in intensive and "en plein air" breeding systems in the south of Italy. Materials and Methods: The infection rate of B. coli in pigs bred in 15 different pig farms and regularly slaughtered in South Italy, in the Calabria region, was investigated. From 2017 to 2019, 177 terminal parts of the rectums of pigs, of which 91 commercial hybrids and 86 autochthonous (Nero Calabrese), reared, respectively, in intensive and "en plein air" breeding system, were tested for parasite detection. After the slaughtering, the terminal part of the rectum was sampled and transported to the laboratories and immediately processed. For the detection of trophozoites, fresh smears of feces were examined at light microscopy. Moreover, flotation was performed using a sodium chloride solution, then smears of feces were dispersed on microscope slides and examined at light microscopy. The observed parasites were identified at the species level using morphological characteristics. Results: B. coli was detected in a total of 83 (i.e., 46.89%) pigs, with a significantly higher prevalence (p<0.0001) found in commercial hybrid (i.e., 59/91-64.84%) pigs rather than in autochthonous ones (i.e., 24/86-27.91%). It follows that the infection was more common in pigs reared in the intensive breeding system than in "en plein air" ones (p<0.0001). The infection prevalence was higher in males than in females and lower in elder animals than in younger ones (p=0.012 and p<0.0001, respectively). Conclusion: The breeding system is likely the main discriminant for the parasite spread as well as the hygienic condition of the farms. Good manufacturing and hygiene practices along the food production chain are crucial in preventing human balantidiasis transmission by meat consumption. The high B. coli prevalence, the wide spectrum of host species, and its zoonotic significance push toward a greater public interest.

Balantidiasis: A Neglected Tropical Disease Used as a Study Model for a Holistic Approach to Sustainable Development in the Framework of Agenda 2030 Goals

“…Furthermore, the linkages and effects that make them relevant to all the SDGs and how the efforts to mitigate their impact will have a direct influence on overall SDGs progress have been investigated [15]. By contrast, other NTZs, such as balantidiasis, despite their wide distribution, have been poorly investigated [23][24][25]. Economic deprivation makes some basic services less accessible and limits opportunities for access to medical cures and basic hygienic conditions.…”

“…This parasite has a worldwide distribution; however, it is more common in the subtropical and tropical regions of the world [28]. The reservoir hosts are the domestic and wild pigs, in which the parasite inhabits mainly the villi or lumen of the large intestine [23]. In its reservoir host, the prevalence of the infection ranges from 0.7% to 100% depending on the animals' reader system, geographic origin of animals, and, mainly, the breeding hygienic conditions [23][24][25]29,30].…”

“…The reservoir hosts are the domestic and wild pigs, in which the parasite inhabits mainly the villi or lumen of the large intestine [23]. In its reservoir host, the prevalence of the infection ranges from 0.7% to 100% depending on the animals' reader system, geographic origin of animals, and, mainly, the breeding hygienic conditions [23][24][25]29,30]. In a reservoir host, B. coli is commonly considered nonpathogenic; however, in symptomatic animals, the clinical presentation is characterized by fetid watery diarrhea, appetite loss, dehydration, loss of body condition, and retarded growth, inevitably leading to economic losses [31].…”

“…In the developing countries, due to poor hygienic conditions, close contact between humans and farmed animals, malnutrition, concomitant infections, and debilitating diseases, B. coli could also represent a serious threat to human health [26,27]. In fact, as is well-known, balantidiasis could be considered a relevant NTZ and particularly in the poorest countries, B. coli is regarded as one of the most underestimated food-and waterborne parasitosis [23], while in the developed countries, B. coli spread could be occasional and related to contamination or a process failure within water utilities or recreational waters (i.e., in swimming pools, water parks) [32,33]. Moreover, this pathogen could be transmitted by the consumption of raw or undercooked meat following carcass contamination during slaughtering [23,34,35].…”

“…In fact, as is well-known, balantidiasis could be considered a relevant NTZ and particularly in the poorest countries, B. coli is regarded as one of the most underestimated food-and waterborne parasitosis [23], while in the developed countries, B. coli spread could be occasional and related to contamination or a process failure within water utilities or recreational waters (i.e., in swimming pools, water parks) [32,33]. Moreover, this pathogen could be transmitted by the consumption of raw or undercooked meat following carcass contamination during slaughtering [23,34,35]. In humans, B. coli infection could outcome in an asymptomatic way or generate a severe syndrome characterized by mucosal ulceration accompanied by diarrhea and dysentery with possible fatal outcomes [36].…”