Balantidiasis, caused by Balantidium coli, is a zoonotic parasitic disease characterized by high infection and incidence rates; however, it is only scantly investigated and therefore considered a neglected tropical zoonosis (NTZ).
Even though the term “One Health” could sound like a modern concept, it dates back to the 19th century, when the father of the One Health theory Rudolf Virchow, investigating swine roundworm, Trichinella spiralis, highlighted the linkages between human and veterinary medicine and coined the term “zoonosis” to indicate an infectious disease passing between humans and animals. In these circumstances, Virchow stated that “Between animal and human medicine there are no dividing lines—or should there be. The object is different, but the experience obtained constitutes the basis of all medicine.” This last sentence, which could be called Virchow’s paradigm, in 2021 is still valid; in fact, it has been estimated that, globally, about one billion cases of illness and millions of deaths occur every year for zoonoses [1]. In the last three decades, over 30 new human pathogens have been detected, and 73% of the currently emerging and re-emerging pathogenic agents may cause zoonoses [2][3][2,3]. The transmission of zoonotic disease occurs at the human-animal interface through direct or indirect exposure of humans to animals, their products (i.e., meat, milk, eggs), the same vectors, and/or sharing the same environment [4][5][4,5]. Environment plays a crucial role in zoonosis transmission and spread. In fact, on the one hand, a healthy environment (in which humans, animals, and the environment are in a perfect balance) could mitigate the spread of infectious diseases [6]; on the other hand, environmental changes, including changes in climate, landscape, and communities of hosts and vectors, have all been implicated in the spread of zoonotic diseases directly (i.e., by modulating immunocompetence) or indirectly (i.e., by modifying the vectors composition and density) [4][7][4,7]. Land use modifications, for instance, intensive livestock farming, urbanization, encroachment into wildlife habitats, and agricultural changes, account for around 50% of all zoonotic emerging infectious diseases [8]. Pathogens traditionally spilled over from animals to humans; however, as testified by the SARS-CoV-2 pandemic, human encroachment into wildlife habitats, exponential human population growth, and exploitation of the environment make spillover more likely, with potentially devastating consequences [9].
The neglected tropical diseases (NTDs) could be defined as a diverse group of diseases whose health and the economic burden falls most heavily on the poorest people and communities [10][17]. Some of these are neglected tropical zoonoses (NTZs) which severely impact the environment, animal, and human health and create severe economic losses. NTZs have been at the cornerstone of the One Health/Ecohealth approach, with an estimated amount of $20 billion in direct costs and over $200 in indirect losses [11][18]. Nowadays, as stated above, the threat of the NTDs emergence due to climate changes, employment of natural resources, the constant increase of the world population, and their new lifestyle are increased worldwide. Some NTZs, for instance, soil-transmitted helminths, dirofilariasis, onchocerciasis, dengue, chikungunya, and schistosomiasis, as well as rabies and leishmaniosis, have been extensively studied due to their high pathogenic relevance [12][13][14][15][19,20,21,22]. 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 [16][15]. By contrast, other NTZs, such as balantidiasis, despite their wide distribution, have been poorly investigated [17][18][19][23,24,25].
Balantidiasis is a parasitic disease caused by the ciliated protozoa Balantidium coli (also known as Neobalantidium coli or Balantioides coli), which affects a variety of hosts including domestic pigs, ruminants, guinea pigs, and rats [18][24]. Balantidium coli features a direct lifecycle with fecal-oral route transmission that occurs mainly by ingestion of food and water contaminated with cysts [20][21][26,27]. This parasite has a worldwide distribution; however, it is more common in the subtropical and tropical regions of the world [22][28]. The reservoir hosts are the domestic and wild pigs, in which the parasite inhabits mainly the villi or lumen of the large intestine [17][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 [17][18][19][23][24][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 [25][31].
In 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 [20][21][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 [17][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) [26][27][32,33]. Moreover, this pathogen could be transmitted by the consumption of raw or undercooked meat following carcass contamination during slaughtering [17][28][29][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 [30][36]. This last scenario is mainly linked to other debilitating conditions, for instance, immunodepression, chronic and infectious diseases [31][37].
Massive movements of people and animals from rural to urban areas lead to changes in the environment that could affect the epidemiology of NTDs with the risk of spreading to areas not yet infected [43][60]. On the one hand, urbanization processes encourage social inclusion and economic development; on the other hand, some risk factors of infectious diseases might be exacerbated if not properly managed. This may be due in part to conditions in which the poorest people live in urban centers and to certain habitats that urban spaces offer that facilitate the ability of parasites to survive and spread. Most people confined to rural environments provide for their livelihoods through agriculture and livestock. A higher rate of B. coli infection was found at overcrowded farms due to insufficient space and in humans related to the presence of animals in the domestic environment due to the lack of separate breeding facilities [19][44][25,61]. Therefore, new urban spaces should certainly consider the need to improve housing. The lack of adequate sewage systems and the supply of drinking water in households are certainly prone to the spread of waterborne diseases such as B. coli [18][24]. As a water- and foodborne disease, B. coli transmission is also the result of environmental contamination with feces; therefore, reduction of household environments that represent potential infection hotspots such as open-air latrines and stagnant drinking water containers are relevant for parasite control. Furthermore, ending the practice of open defecation limits the spread of the parasite and contributes to achieving the aims of SDG 15 regarding land and soil degradation.
Despite the fact that since 1990, the extreme poverty rates have fallen by more than half, today, 150 million people still live in abject poverty, predominantly in South Asia and Sub-Saharan Africa [46][69]. Economic deprivation or precariousness triggers a vicious circle in which several basic services are lacking, favoring the spread and persistence of NTDs. Not by chance, NTDs are prevalent in low- and middle-income countries, especially in rural and remote areas or in conflict zones [16][15]. The causes of extreme poverty in the world related to NTDs are to be found far beyond the mere lack of income and resources.
Balantidium coli was particularly found among the poorest regions of the world where most of the people live in extreme poverty with less than $1.25 a day [47][13]. Balantidium coli infections in humans and animals were reported in Burkina Faso [48][70], Central African Republic [49][71], Ethiopia [50][72], Guinea [51][73], Liberia [52][53][74,75], Malawi [54][76], Mozambique [55][77], Nigeria [56][78], Sierra Leona [57][58][79,80], Somalia [59][81], and Yemen [60][82]. However, balantidiasis is not geographically linked to the poorest countries but must be considered a disease of “poverty”. In this regard, cases of human balantidiasis have been reported both in countries with lower-middle (e.g., India), upper-middle (e.g., China, Libya, Peru, Turkey, South Africa, Venezuela), and high-income (e.g., France, Greece, Italy) economies according to the latest World Bank classification [61][62][63][83,84,85]. The adverse effects of balantidiasis on the economy of the most vulnerable countries can occur when either the workforce or livestock is affected. The impact of balantidiasis on the health of the workforce negatively affects the capacity to work, support family, and contribute, by extension, to national development [16][15]. The decline in livestock productivity due to acute or chronic effects of balantidiasis can cause significant economic losses with potentially catastrophic repercussions in contexts where animals are the only source of income. The disease causes an increase in medical costs for diagnosis and treatment which can have a significant impact on the economic context of the poorest households, assuming that medical services are accessible. Diagnosis of balantidiasis does not require special means and a microscope analysis at low magnification is sufficient to identify cysts or trophozoites in a fresh stool sample [19][25]. Regarding treatment, tetracyclines have shown high efficacy for B. coli infections in both humans and animals [64][65][66][86,87,88]. In any case, even if health treatments were guaranteed to be free of charge, they could still be considered as economic losses since the prevention of NTDs is based on health and hygiene principles whose realization is certainly less expensive than the treatments required [67][89].