Zoonotic Parasites and Vector-Borne Parasitoses

Abstract

Zoonotic parasites and vector-borne zoonotic parasitoses of humans, especially when affecting immunocompromised persons mobilize researchers’ interest and increase parasitological, environmental, and interdisciplinary investigations worldwide. Climate, environmental and anthropomorphic influences had affected the distribution, occurrence, and adaptability of parasites in humans and animals, the level of environmental contamination with parasites and their developing forms, and the surge of vector competency. Knowledge of parasite biology and evolution shows that hybridization phenomena and adaptations may cause genetic diversity, affecting parasite virulence, antiparasitic drug resistance, acclimatization to new host species, and environmental conditions previously not recorded while leading to the emergence of new diseases and changing parasitism epidemiology. Many parasitic infections are emerging or re-emerging and are neglected with deliberating consequences for public and animal health as well as for food safety and security, especially in sub capacitated developing countries. Decrease of exposure of both animals and humans and negative consequences of zoonotic parasitoses requires raising awareness of researchers, policymakers, and the wider public. Modern diagnostic methods, surveillance, monitoring of parasitoses, and early detection systems followed by tailored containment and control actions provide grounds for sane assessments and investigation toward the cost-effective and efficient prevention programs for both human and animal populations.

1. Introduction

Parasitism is defined as when one organism (parasite) lives on or within another (host) in close biological and ecological dependence, lasting for a certain period of the parasite life cycle. Zoonotic parasites represent particular parasites to whom mainly animals are hosts, but can as well infect and cause disease in humans. To maintain a parasitic relationship with a host, parasites adapted in different ways as part of their evolutionary development parallel to the phylogenetic development of their hosts. Parasites are recognized for many species of hosts, including plants, vertebrates, and invertebrates, with currently rising concerns of hybridization phenomena as a threat to public health, still not fully understood. The risk posed by hybridization and introgression is recognized based on the biology and evolution of parasites, where resulting adaptations may bring significant genetic diversity, affecting parasite virulence, antiparasitic drug resistance, acclimatization to new host species, and environmental conditions previously not recorded while leading to the emergence of new diseases and changing of parasitism epidemiology. Also, research of parasitoses, particularly zoonotic and vector-borne, gains attention in light of enhanced emergence and re-emergence of pathogens affecting humans and animals where many represent a serious threat to the host’s health and wellbeing [1, 2].

As shown in Figure 1 this is primarily caused by anthropogenic influences and continuous modifications of the environment (climate changes, deforestation, disturbance of ecosystems, etc.), practices of food production and consumption (intensive vs. traditional agriculture, global animal movement, and trade), socio-demographic changes and globalization (population growth, urbanization, international trade, tourism, and transportation). Accordingly, our research aimed to provide an overview of the current trends regarding globally most important zoonotic parasites, diseases they cause, and associated influence factors.

Figure 1.

Published research on mammalian zoonoses; color-coded based on geographic region (a), proportional frequency of papers dealing with different hosts (b), different anthropogenic influences (c), and different pathogens (d) [3].

Globalization and global warming in the twenty-first-century increase probability of parasitic infections in humans and animals and enable the introduction of most zoonotic parasites in new biotopes thus increasing the risk of epidemics occurrence in different areas [4]. Attempts to control parasitoses by mass treatment or vaccination are changing the environments in which parasites and other pathogens evolve, adapt, or extinct. Advances in diagnostics, especially molecular methods enable better recognition and characterization of pathogens hence improving outbreak detection and predictions. Continuous monitoring of parasites, vectors, hosts, and natural habitats in endemic areas, as well as early recognition systems, provide grounds for sound and timely epidemiological assessment and investigation leading to cost-effective and efficient prevention programs for parasitoses in both human and animal populations.

2. Methodology

Research inputs were identified through bibliographic database search using keywords: “zoonoses”, “zoonotic pathogens”, “zoonotic parasitoses”, and “zoonotic parasites”. In the first run, we excluded case/case series reports, clinical trials (assessment of treatment), and test validation (assessment of diagnostics), as well as a publication based on narrow geographical area, specific pathogen, disease, or hosts. Inclusion criteria for publications were prioritized based on the type of publication (first considered were review papers and global reports) and the topic/subject of a publication (publications reporting and exploring trends, global influences, and epidemiology). More recent publications covering wider geographical areas and multidisciplinary approaches or by author’s affiliations were further considered. The selected literature review was oriented toward compiling and summarizing data on causative agents, distribution, life cycle, hosts, pathogenesis, symptoms, diagnostics, and therapy/treatment.

3. Zoonotic parasitoses in humans and animals

Numerous parasites found in animals, which represent final or intermediate hosts or vectors, are zoonotic or potentially zoonotic thus representing health risks for humans. In addition to direct and vector-borne transmission, an important source of human infections is the contaminated environment (i.e., geo-parasites, waterborne parasitoses), while some zoonotic parasites are foodborne. The majority of the common parasitic diseases of animals caused by helminths, trematodes, cestodes, pentastomids, and protozoa are zoonotic or have zoonotic potential. Toxoplasma gondii is the most widespread protozoan parasite worldwide. Estimates are that approximately one-third of the world’s population is affected [5]. In developed countries, parasitic water-borne protozoans such as Cryptosporidium and Giardia outbreaks are increasingly reported [6]. In addition to protozoan parasites, the FAO identified Taenia solium, Echinococcus granulosus, Echinococcus multilocularis, Trichinella, Opisthorchiidae, and Ascaris spp. as the main foodborne parasites [7]. Data show that 70% of the helminths population is hosted by 15% of the host population, and these individuals are a prime source of environmental contamination [8]. The tapeworm T. solium is a cosmopolitan parasite with global distribution, with most human cases found in Latin America, Asia, and Africa alongside emergence in recent years in the USA and Europe [9]. In addition to widespread E. granulosus, recently E. multilocularis has become very important because of its expansion from endemic areas to non-endemic areas in North America, Europe, and Japan, apparently by a displacement of fox populations [10]. Regarding Trichinella spp., during the period 1986–2010, 65,818 new cases were registered in 41 countries. Of these, 87% occurred in Europe associated with boar consumption [10]. Characteristics of selected, most important zoonotic parasitoses are shown in Table 1.

Disease	Causative agent	Intermediate host	Hosts	Transmission	Distribution
Fascioliasis	Fasciola hepatica; F. gigantica	Lymnaeid snails	Ruminants, horses, and pigs	Water and water plants	Parts of Europe, Middle East, Latin America, Caribbean, Asia, and Africa
Schistosomiasis	Schistosoma spp.	Freshwater snails	Various animals	Water (percutaneous penetration)	Africa, South America, Caribbean, Central, and West Africa, South-East Asia, and sub-Saharan Africa
Cystic echinococcosis	Echinococcus spp.	Sheep, cattle, moose, wallabies, camels, warthogs, reindeer, and pig	Carnivores (mainly dogs)	Water and food	Worldwide
Alveolar echinococcosis	Echinococcus multiocularis; E. vogeli; E. oligarthrus	Rodents	Carnivores, (red fox and dogs)	Water and food	Northern hemisphere
Taeniasis	Taenia spp.	Ruminants, pigs, rodents	Humans	Undercooked meat	Worldwide
Hymenolepiasis	Hymenolepis nana; H. diminuta	Arthropods	Rodents and humans	Water and food	Worldwide
Trichinellosis	Trichinella spp.	Many vertebrate hosts	Various animals	Animal tissues	Worldwide
Toxocariasis and other geo-helminthiases	Toxocara canis T. cati; Ascaris spp. Ancylostoma spp.; Uncinaria stenocephala Trichuris spp. Strongyloides stercoralis	Birds, cats, prairie dogs, rabbits, rodents, pigs, and other		Water, food, soil	Worldwide
Dirofilariosis	Dirofilaria spp.	Mosquitoes	Domestic dogs, coyotes, jackals, wolves, domestic cats, bobcats, ferrets, and foxes	Mosquitos	North and South America, Australia, Japan, and Europe
Capillariasis	Capillaria hepatica; C. the Philippines	Rodents, wild and domestic carnivores’ lagomorphs, swine, primates, fish	Humans, birds	Water and food	Thailand, and sporadic cases in other East and Southeast Asia
Trypanosomiasis	Trypanosoma cruzi; T. brucei rhodesiense; T. brucei gambiense	Invertebrate vector	Domestic pigs and cats, wildlife reservoirs include opossums, armadillos, raccoons, and woodrats	Kissing bugs	Mexico, Central, and South America
Leishmaniasis	Leishmania spp.	Sandflies	Cats, dogs, horses, and bats	Sand fly’s	Visceral leishmaniasis -Bangladesh, Ethiopia, India, Nepal, South Sudan, Sudan, and Brazil. Cutaneous leishmaniasis - South and Central America, the Middle East, and Central Asia
Giardiasis	Giardia spp.	Dogs, cats, ruminants, and pigs		Water, food, and surfaces	Worldwide
Zoonotic malaria	Plasmodium spp.	Anopheles mosquitoes	Wild macaque, chimpanzee, humans	Anopheles mosquitos	South Sahara and parts of Oceania
Toxoplasmosis	Toxoplasma gondii	Pigs, ruminants, poultry, and rabbits	Cats	Water and food	Worldwide except in South America
Cryptosporidiosis	Cryptosporidium spp.	Cattle, sheep, pigs, goats, horses, and deer		Water and food	Worldwide
Babesiosis	Babesia spp.	Tick	Rodents, and ruminants	Ticks	Worldwide
Amebiasis	Entamoeba hitolytica	Mammals		Water and food	Worldwide

Table 1.

Zoonotic parasitoses of humans including disease, causative agent, intermediate/definitive host(s), transmission, and distribution.

Fascioliasis is caused by parasites of the genus Fasciola. In animals, the disease leads to significant economic losses, especially in sheep and cattle farming. Until 1990 it was considered a secondary important disease, however, in the last three decades is on the list of Neglected tropical diseases (NTDs) due to increased incidence of human infections [11]. Adults of F. hepatica and F. gigantica are found in the liver and biliary system of ruminants, equids, and other herbivores, while humans are accidental hosts for both species. Fasciola development starts with eggs excreted in the faces of infected animals that come in contact with fresh water. Miracidia developed from eggs penetrating intermediate host; freshwater snail were through stages of sporocysts, cercaria exit snails and encysts on water plants developing into infectious metacercaria. Ingested by the final host they reach adult form and penetrate through the intestinal wall in the abdomen where they attach to the liver. Estimates are that worldwide between 2.4 and 17 million humans are infected [12]. In humans, an acute form of the disease is manifested by symptoms when parasites migrate through the abdominal cavity toward the liver. Symptoms of the acute and chronic phases of the disease include fever, weakness, abdominal pain, and hepatomegaly. Diagnosis is by direct parasitological or indirect serological tests (i.e., ELISA), magnetic resonance, ultrasound, and computerized tomography. Most people are treated successfully with triclabendazole, even though increased resistance of liver flukes to triclabendazole represents a threat to successful therapy and disease control in endemic areas.

Schistosomiasis is NTD, caused by a fluke of the genus Schistosoma. At least five species can infect humans out of which the most important are S. mansoni, S. haematobium, and S. japonicum. Estimates are that currently over 290.8 million people are infected by these parasites, while 779 million are potentially exposed. The disease has a high case fatality rate with 280.000 fatal outcomes and 3.3 million cases with permanently affected health as a consequence of the disease. The largest number of cases is found in areas of sub-Saharan Africa, the Middle East, India, China, Brazil, the Philippines, and Venezuela. In 2013, the disease is confirmed in Corsica. The occurrence and transmission of schistosomiasis are usually related to poor living and sanitary conditions [13]. The life cycle of the parasite starts with excreting eggs found in faces and urine into water. Asexual reproduction of shistoma evolves in snails until the stage of the cercaria, which through water penetrate through the skin into the venous system of the hosts, and parasite in different tissues depending on the species. The S. hematobium is found in the bladder and urinary system, S. japonicum in the small intestines, and S. mansoni parasites in both small and large intestines. Acute schistosomiasis is followed by fever, dermatitis, headache, myalgia, and respiratory symptoms. Infections by the S. hematobium are manifested by dysuria and hematuria due to injuries to reproductive organs alongside increased inclination of hosts to other infections. Infections by the S. japonicum and S. mansoni show symptoms of hematochezia, diarrhea, and obstipation, with ulceration, fibrosis, and hyperplasia of affected tissues in the chronic form of the disease [13]. If the parasite comes to the central nervous system, neuroshistomiasis as the most severe form of the disease develops with granulomatosis lesions of the brain leading to epileptic caesuras, encephalopathies, damaged sight, and ataxia. Diagnosis of schistosomiasis is by confirmation of eggs in feces and urine, by tests such as ELISA and PCR, together with diagnostic imaging techniques. Prevention of schistosomiasis includes snail population control and improvement of sanitary conditions. The vaccine is still unavailable, while praziquantel is used for treatment, efficient only for fully undeveloped forms of the parasite in migrating phase within the host organism.

Opisthorchiasis and clonorchiasis are diseases caused by species of the family Opisthorchiidae, most commonly by Opistorchis felineus, O. viverrini, and Clonorchis sinensis. The life cycle includes intermediate hosts (freshwater snails and cyprinid fish), while final hosts are humans, cats, dogs, pigs, rats, birds, and fish. Eggs excreted by faces develop through stages of sporocyst, redia, and cercaria, which leave snails to infect fish and become metacercaria. The life cycle ends with the consummation of infected fish by final hosts (raw or undercooked), and metacercaria migrates into biliary ducts, sack, and liver [14]. Currently, 45 million people throughout Europe and Asia are infected with 700 million potentially exposed. Even though estimates vary, clonorchiasis prevalence continues to grow compared to figures in 1990ties, especially in China. Data show that the prevalence in dogs and cats is high (0.8–48.5% and up to 64.1%, respectively). Mild forms of opisthorchiasis and clonorchiasis have nonspecific symptoms including eosinophilia and cholestasis. Chronic disease in humans may be accompanied by cholangiocarcinoma. Diagnosis is by parasitological tests through detection of eggs in host feces, serological tests, and molecular methods. Treatment with praziquantel is very efficient (90–95%), with still no evidence of resistance development.

Cystic and alveolar echinococcosis is caused by larval forms of tapeworms of the genus Echinococcus and it is considered one of the most important parasitic diseases in the world. E. granulosus s.l. and s.s., E. ortleppi, E. canadensis, and E. intermedius cause cystic echinococcosis (CE). E. multiocularis causes alveolar echinococcosis (AE), as well as in rare cases E. vogelii and E. oligarthus [15]. Most frequently final hosts for E. granulosus are dogs and wild Canidae, with ruminants, horses, and pigs as intermediate hosts. Humans can be an intermediate host for both species, infected most commonly by eggs. In 98% of cases, parasite inhabits the liver where cysts are developed. The WHO considers AE as the first of 20 foodborne NTDs, while E. multiocularis takes third place. Adult forms of the parasite inhabit the small intestines of the final host with eggs excreted by feces and consumed by intermediate hosts. Through stages of protoscolex, the cestode becomes infectious with the final stage of the cycle represented by the consumption of infected tissues of intermediate hosts by the final host [9]. The AE occurs exclusively in the northern hemisphere. An increase in prevalence is related to the growth of the fox population, especially in periurban areas. The global burden of disease is estimated to be 18.200 new cases annually, out of which 1.600 cases are reported in Europe [9]. The CE is distributed worldwide in both humans and animals, representing a serious threat, especially in the Mediterranean, South America, and Central Asia. The CE and AE are chronic and severe diseases most commonly affecting the liver. The E. multilocularis forms multilocular cysts, while E. granulosus forms one hydatid cyst. The E. granulosus cysts manifest in clinical symptoms correlated with their size and pressure on nearby organs. The prognosis for the CE depends on the parasite location most commonly in the liver or lungs, while 20% of infections are located in the spleen, peritoneum, kidneys, bones, and sometimes brain and spinal cord. Diagnosis in final hosts is by parasitological, serological, and molecular tests. Postmortem examination of small intestines is considered the “gold standard” test because it confirms the presence and enables the identification of the parasite species. In humans’ diagnosis is by imaging techniques, serological tests, and by histopathological examination. Benzimidazole is the sole appropriate therapy for the CE, while the AE treatment is by surgery, with limited success due to difficulties in the removal of parasitic cysts. Unfortunately, surgery can be performed only in 20–50% of cases, while in rest treatment is not recommended especially for chronic cases due to developed mass of the parasitic cysts and frequent metastasis of cysts into various other organs.

Hymenolepiasis is caused by cestode; Hymenolepis nana and H. diminuta, are distributed worldwide with endemic areas in parts of Asia, and central Europe. Central and South America and Africa. The disease is common in children living in poor hygiene and sanitary conditions, wherein some poor community’s prevalence can reach up to 58%. Epidemiolocal data show around 175 million people are infected throughout the world [16]. The disease commonly is asymptomatic, while in some cases symptoms such as chronic diarrhea, abdominal pain, anorexia, itching, and slow growth in children are recorded. Infections by the H. nana and H. diminuta in the final stages develop into severe clinical forms, sometimes life-threatening, especially in people with AIDS. The H. nana parasites in rodents, with direct human to human transmission and autoinfections. However, infection by the H. nana is still considered zoonotic due to widespread infections in rodents which serve as pathogen reservoirs. Humans can pose both intermediate and final hosts, while in the zoonotic transmission cycle arthropods have the role of intermediate hosts found in flour and grain. Accidental consumption of infected arthropods leads to the development of parasitic worms in humans. Diagnosis is made by confirmation of eggs in feces, while treatment includes praziquantel, nitazoxanide, and nicodamids.

Taeniasis is caused by the parasites of the genus Taenia. Species infecting humans are Taenia solium (pig tapeworm), Taenia saginata (cattle tapeworm), and Taenia asiatica (Asia tapeworm). Taeniasis is endemic in some developing countries, especially in Africa, South America, and Asia [17]. In countries of North America and Australia, disease occurs due to an increase in pig meat consumption, migrations, and travel. In epidemic form, taeniasis occurs in Spain and Portugal and sporadically in other countries of Western Europe. People are infected through consumption of undercooked pig or beef meat infected by the development form of the parasite (cysticercus), with the final location of the adult parasite in the small intestines. Also, in cases of feco-oral ingestion of T. solium eggs, the cysticercus develops in the human body causing neurocysticercosis (NCC) if development occurs in the central nervous system. The NCC is the most common form of taeniasis and raises great concerns in endemic areas. It causes about 50.000 death annually, and it is considered the most common cause of acquired epilepsy with about 2 million infections worldwide [17]. The symptoms are non-specific and include loss of weight, abdominal pain, vomiting, diarrhea, and obstipation. The symptoms of the NCC depend on the size, number, and location of cysts. The most common symptom of the NCC is epilepsy, followed by remittent headache due to increased intracranial pressure. If cysts are located in chambers of the brain, obstruction of cerebrospinal fluid flow causes hydrocephalus. Diagnosis is by parasitological, serological (ELISA), and molecular (PCR) methods. Albendazole and praziquantel are the most common antiparasitic drugs applied.

Trichinellosis is caused by the parasite of the genus Trichinella, transmitted through the consumption of raw or undercooked meat containing larva forms of the parasite [18]. There are at least 13 species/genotypes of Trichinella divided into two groups: incapsulated (Trichinella spiralis, T. nativa, T. britovi, T. nelsoni, T. murelli, and T. pathogenesis, T. chanchalensis, T6, T7, T8, and T9) and unencapsulated (T. pseudospiralis, T. papuae, T. zimbawensis). The life cycle starts with the enteric phase after larval ingestion (L1), which after several stages develop within 1–2 days in adult forms. After 30 h post-infection parasite starts to reproduce and newborn larvae start the parenteral phase by penetrating lymphatic and vascular systems. After reaching well-vascularized tissues, (skeletal muscles, myocardium, extraocular and intercostal muscles, and brain) they continue postembryonic development. Trichinellosis even though long known is still widely reported due to disturbances in the ecosystems caused by humans, where trichinella had successfully adapted and infects wild and domesticated animals, and humans in Eastern Europe, Asia, and South America [18]. Diagnosis is based on clinical examination, blood analysis (eosinophilia and increase in muscle enzyme levels), and epidemiological data. Direct diagnosis is made by PCR, digestion test, and histological examination of tissues collected by biopsy. Indirect diagnostic techniques include serological tests. Antiparasitic treatment includes benzimidazole, mostly albendazole with high therapeutic efficacy. Other antiparasitics such as ivermectin, nitazoxanide, quinfamide, and flubendazole are also good treatment alternatives.

4. Toxocariasis and other soil-transmitted helminthiases

Toxocariasis is a widely distributed zoonosis with a huge socio-economic impact, especially in poor countries. The disease is caused by the nematode of the genus Toxocara, which includes four species; Toxocara canis, T. cati, T. malaysiensis, and T. vitulorum able to infect a wide host range. Species T. canis, T. cati, and T. malaysiensis are common parasites of dogs, cats, and other carnivores with importance in veterinary and public health [19]. Toxocariasis in humans is manifested in four main clinical forms: visceral larva migrans, asymptomatic or common toxocariasis, and ocular and neuro-toxocariasis. The largest number of ocular toxocariasis is reported in Japan, Correa, France, Brazil, and the USA, while neuro-toxocariasis is dominant in Europe, Asia, and the Americas, and visceral larva migrans reports are coming from Spain, India, Argentina, and Brazil. In developed countries, humans are most commonly infected with Toxocara spp. Eggs contaminated soil, food, and water. Dogs and cats are the main source of contamination, especially in communities where these animals have free access to public parks and playgrounds. In some countries such as the United Kingdom foxes became a primary contaminant of the environment. Contamination of soil of public parks in most countries varies within a range of 17.4–60.3% according to reports from Brazil, 14.4–20.6% in the USA, 13.0–87.1% in Europe, 30.3–54.5% in Africa, and 6.6–63.3% in Asia [19]. Also, humans can be infected with embryonated eggs attached to the hair of dogs and cats. In accordance with the wide para-enteritis host range, some human cases are associated with the consumption of undercooked beef, lamb, and chicken. Besides Toxocara spp., other geo-helminths represent a significant problem in tropic and subtropic regions. Most important are Ascaris spp., Ancylostoma spp., Uncinaria stenocephala, Trichuris spp., and Strongyloides stercoralis. According to the WHO reports almost 1.5 billion people are exposed to these parasites. Infection occurs most commonly by ingestion of eggs, by feco-oral route, or penetration of larvae from the soil through host skin [20]. Geo-helminths in humans causes a range of different, non-specific symptoms, hypersensitivity, small intestine obstruction, volvulus or intussusception, cholecystitis, and pancreatitis. Anemia can occur due to mucosal bleeding from the upper gastrointestinal system. Patients with severe disease demonstrate eosinophilic pneumonia, urticaria, cough, dyspnea, hemoptysis, pleuritis, pleural exudate, hepatic abscesses, diarrhea, dermatitis, asthenia, abdominal pain, tachycardia, tachypnea, edema, hematochezia, and occasionally melena. Diagnosis is by parasitological examination and identification of eggs or adults in feces, sputum, bronchoscopy, endoscopy, basic blood analysis, serological tests, and imaging techniques. Treatment includes the administration of antibiotics and anthelmintics (albendazole, mebendazole, ivermectin). With small intestine obstruction, volvulus, or intussusception, surgical laparotomy is indicated.

Dirofilariosis is a mosquito-borne zoonotic disease caused by the nematode of the genus Dirofilaria. Several species of this genus may cause human infection; D. repens, D. immitis, D. tenuis, D. striata, D. ursi, and others. Adult forms of D. repens are parasites of skin and subcutaneous tissues of animals, while D. immitis, known as “heartworms”, is usually found in pulmonary arteries and right hearth of dogs and other carnivores. D. tenuis infects raccoons, D. striata wild felids and D. ursi is found in bears [21]. Animals are considered natural hosts while humans are accidental hosts. Increased occurrence of dirofilariasis is reported in Europe related to traveling in endemic areas. Human dirofilariasis is reported in 46 countries from five continents (Afrika, Amerika, Asia, Australia, and Europe). D. repens occurs in 39 countries from all continents but America, D. immitis is reported in 15 countries from all continents but Africa, D. tenuis is reported from USA and India, D. hongkongensis from China and Austria, D. striata from America and D. ursi from Japan [21]. The life cycle of Dirofilaria has five stages developing invertebrate hosts and mosquitos as vectors (dominantly Culex spp. and Aedes spp.). Mosquitoes transmit third-stage larvae. In the host body nodules are formed at different locations depending on which ocular, subcutaneous and pulmonal dirofilariasis is developed. Since symptoms are absent or non-specific diagnosis is complex. The most common signs are redness of the eye, irritation, and pain similar to allergy conjunctivitis. Diagnosis is by examination of nodules and by x-rays. Therapy consists of surgical removal of nodules from lungs and subcutis. In most cases, treatment with antiparasitic is not necessary.

Capillariasis is a globally distributed zoonotic parasitosis caused by nematode Capillaria spp. So far over 300 species of Capillaria had been identified with a wide host range, while the following species cause infections in humans; C. philippinensis, C. hepatica, and C. aerophila. Capillariasis is the first time described in rural areas of the Philippines and Thailand, following spread to Indonesia, Japan, Taiwan, India, and Egypt [22]. Cases reported in Europe are mostly imported through travel in endemic areas. The parasite is localized in the liver of mammal hosts, particularly rodents, while humans are accidental hosts. Final hosts—rodents represent a source of environmental contamination. They are transmitted by water or food. In the liver due to parasite migration necrotic lesions, inflammations, and tissue granulation is found. In humans, capillariasis can be intestinal, pulmonal, or hepatic. Symptoms are fever, hepatomegaly, eosinophilia, and an increase in liver enzymes. Complications of infection include lobular pneumonia, pulmonary abscesses, anemia, kidney damage, splenomegaly, and congestion. Diagnosis is made by identification of eggs from stool, liver biopsy, imaging techniques, serological tests such as ELISA, and Indirect immunofluorescence (IFA). Therapy is based on thiabendazole and albendazole.

Trypanosomiasis is caused by species of the genus Trypanosoma. Chagas disease (CD) or American trypanosomiasis is caused by protozoa T. cruzi, while T. brucei rhodesiense and T. brucei gambiense are causative agents of African sleeping sickness (African trypanosomiasis). T. cruzi is transmitted by insects of the sub-family Triatominiae, while T. brucei is transmitted by tsetse flies of the genus Glossina. Both diseases are connected with high morbidity and mortality and are difficult to control since many wild and domestic animals are natural reservoirs. During the life cycle, the parasite undergoes three stages; intracellular amastigote (proliferative form found in invertebrates), epimastigotes (proliferative form from invertebrate intestines), and extracellular trypomastigote. During feeding, hematophagy insects introduce trypomastigote which transforms into epimastigotes [23]. The CD is one of the leading public health issues in most South American countries. Due to continuous migrations of people from endemic areas disease is more and more frequently reported in non-endemic areas like North America, Europe, Australia, and Japan. Here transmission occurs through blood transfusion, organ transplantation, or vertical transmission from mother to child. The disease affects about 6–8 million people worldwide, causing 50.000 deaths, while 65–100 million people live in endemic areas. T. brucei is an extracellular parasite found in the blood, lymph, lymphatic nods, liquor, and interstitial fluid of the host. The acute form is often fatal to a host, however, if the patient survives, the disease becomes chronic followed by migration of the parasite to cerebrospinal fluid. The patient succumbs to septicemia or meningitis. T. cruzi invades macrophages, fibroblast, and epithelial cells. The acute stage of infection is accompanied by high parasitemia with no symptoms or showing as fever, anorexia, and tachycardia. Diagnosis in the acute stage is based on the detection of the parasite in blood or by PCR. In the chronic stage, serological tests are used. Therapeutics (nifurtimox, benznidazole) are efficient in the acute stage of T. cruzi infection. For treatment of T. brucei infection in acute form pentamidine (T. b. gambiense) and suramin (T. b. rhodesiense) are used, while for chronic stage melarsoprol and eflornithine.

Leishmaniasis is one of the most important protozoan diseases. Causative agents are of the genus Leishmania, within which zoonotic are L. infantum, L. donovani, L. peruviana, L. braziliensis, L. mexicana, L. major, and others. This is a vector-borne disease transmitted by sandflies, insects of the genus Phlebotomus and Lutzomyia. Most of the species cause disease in many mammals which represent the reservoir of the parasite (rodents, dogs, cats, wolfs, and primates) [24]. Dogs are the main reservoirs in urban areas, while foxes, jacals, and wolfs are important salivatic hosts. Leishmania has a heterosexual life cycle, including two morphologically different forms; amastigote found in macrophages of domesticated mammals and promastigote found in intestines of vectors. In humans, the infection starts when female Phlebotomus inoculates promastigote through the skin. The macrophages then intake promastigote by phagocytosis where the parasite transforms into a non-flageal form—amastigote. This form is further reproduced by binary fission within macrophages. Diseases in endemic in a large number of countries mainly in South and Central America, Africa, Asia, and Mediterranean countries. Annually 1.5 million cases of cutaneous leishmaniasis are confirmed and about 500.000 cases of visceral leishmaniasis alongside 30.000 fatalities [25]. Risk factors for leishmaniasis are related to urbanization and climate changes. An increase in the average temperatures delays the reproduction season of the vector species. Hence endemic areas for zoonotic leishmaniasis had spread to northern Italy, Germany, the United Kingdom, Hungary, and France. There are two clinical manifestations of leishmaniasis in humans. Visceral leishmaniasis in humans and dogs is caused by L. donovani and L. infantum. The other species most commonly cause cutaneous or mucocutaneous disease accompanied by papulose, muco-papulose, and nodular exanthema. The visceral form is accompanied by fever, hepatosplenomegaly, pancytopenia, weakness, and weight loss. If not treated, severe cases of visceral leishmaniasis are usually fatal, due to direct effects of the disease or due to secondary complications (bacterial infection and hemorrhage). Diagnosis is made based on clinical manifestation, parasitological, serological, and molecular tests. Therapy must be adjusted to individual cases and the most commonly includes amphotericin, pentamidine, pentavalent antimonial, ketoconazole, itraconazole, fluconazole, and miltefosine.

Giardiasis is a disease caused by Giardia duodenalis (formerly called G. lamblia or G. intestinalis), with at least eight genotypes (A-H) confirmed in humans and other mammals. Species of the genus Giardia are found in other hosts; G. agilis in amphibia, G. ardeae and G. psittaci in birds, G. microti and G. muris in rodents [26]. Giardiasis is globally distributed, yielding over 280 million cases caused dominantly by genotypes A and B [26]. Epidemics and increases in prevalence are related to exposure to contaminated food and water, public pools, and daycare establishments. The disease is important from a veterinary perspective since it causes serious symptoms in animals as well as death, while diseased animals are a source of infection for humans. The life cycle of Giardia includes two phases; trophozoite (replicating stage) and cyst (infectious stage). Infection can occur directly by ingestion of cysts or by the feco-oral route. The following infection in the duodenum, cyst transforms to trophozoite, which reproduces by binary division, forming the cysts then excreted by feces. Cysts are very viable and can maintain infectivity in the environment for weeks and months. The disease can be asymptomatic or in acute form followed by dehydration, abdominal pain, nausea, vomiting, and weight loss. In the chronic form, the disease can manifest as the syndrome of irritable colon and chronic fatigue. Laboratory diagnosis of Giardia spp. Is mainly based on the detection of cysts or trophozoite in fecal samples by serological and molecular methods. Treatment is adjusted to anamnesis and clinical findings and includes metronidazole, tinidazole, nitazoxanide, paromomycin, quinacrine, and furazolidone.

Malaria is a disease caused by the parasites of the genus Plasmodium. Species found in humans are P. malariae, P. falciparum, P. vivax, P. ovale, and P. knowlesi. The disease is transmitted by mosquitoes of the genus Anopheles which transmit disease to humans and other vertebrates [27]. Malaria is still one of the most severe diseases affecting hundreds of million people worldwide causing over 400.000 deaths annually. P. vivax, in most cases considered the cause of re-emergent malaria occurrence, is an ancient and common zoonosis originating from apes. The occurrence of other zoonotic malaria agents (P. knowlesi, P. cynomolgi, and P. simium) additionally accentuates the severity of this disease. Malaria is the most common in Africa and some Asian countries. Species found in America and Europe are P. vivax and P. malariae, while in Africa dominant species is P. falciparum. The life cycle is very complex and evolves in two stages; sexual in mosquitoes and asexual in vertebrates including humans [27]. Clinical symptoms of malaria; fever, nausea, and weakness are related to every cycle of merozoite exiting and leaving erythrocytes. Diagnostic tests for malaria include microscopic analysis of blood smears (golden standard), PCR, IFA, and ELISA. Treatment of malaria is based on anti-malaria drugs; chloroquine phosphates, with increasing reports of resistance to this drug from around the world. Other drugs are used in addition such as primaquine, and quinine sulfate alongside doxycycline and mefloquine.

Toxoplasmosis is an important disease in animals and humans globally, especially due to resulting in stillbirths and miscarriages in humans [28]. The causative agent, Toxoplasma gondii can be found in many species of animals and humans. More than a billion people in the world are infected by T. gondii, with very high seroprevalence in some countries (Brazil, 77.5%; St. Thomas and Principe, 75.2%; Iran, 63.9%; Columbia, 63.5%; and Cuba, 61.8%). Only in the USA, the annual cumulative incidence is 9.832 new cases; out of which 2.169 are ocular form and 1.399 cerebral forms of toxoplasmosis as the most common form of the disease [28]. Humans and most warm-blooded animals and intermediate hosts, while domestic and other cats are final hosts. In the final host’s intestines, parasites reproduce sexually, resulting in forming of the oocyst, which matures by sporulation to an infectious form. People get infected by consumption of raw or undercooked meat (mainly lamb and pork) containing bradyzoites or ingestion of the sporulated oocysts found on vegetables, water, in cat feces, transmission from mother to a child, or by organ transplantation. In most patients, primary infection or mild form when parasites are found in different organs, mainly the heart and skeletal muscles, brain, and retina. Alongside three standard forms of toxoplasmosis (ocular, congenital, and cerebral), a latent infection occurs characterized by behavioral changes and neurologic symptoms. Diagnosis is made by imagining techniques, histopathology, and serological test. Dormant parasites in tissues are the main obstacle to successful treatment since no drug available can reach the parasites encapsulated in cysts. Currently available drugs are efficient for acute and reactivated infections caused by tachyzoites. If treatment is not timely, a fatal outcome is inevitable in immunocompromised individuals. Therapy includes derivates of pyrimethamine in combination with sulfadiazine or clindamycin.

Cryptosporidiosis is caused by the species of the genus Cryptosporidium resulting in intestinal infections in a large number of vertebrates including humans, wildlife, reptiles, birds, amphibian, and fish [25]. Species the most commonly found in humans are C. parvum and C. hominis, causing over 90% of cases of cryptosporidiosis, and also C. meleagridis along with other parasite species. C. parvum has a range of hosts that includes over one hundred mammal species demonstrating the excellent adaptation of the parasite [29]. Cryptosporidium can be found in water, food, and surfaces contaminated with feces. The infection comes with ingestion of contaminated water, food, or by direct contact (community and hospital infections). The Cryptosporidium due to its morphological features can persist for longer periods outside the host and is very resistant to many desificants. Development of the C. parvum starts with sporulated oocytes, which after ingestion begin asexual (merogonial) and sexual (gametogonia) reproduction in small intestines. The significance of this infection reflects in high incidence especially in children, immunocompromised parsons (AIDS patients) with the highest case fatality rate in younger individuals. The most common symptom is diarrhea followed by dehydration, nausea, vomiting, increased temperature, and weight loss [29]. All domestic and wild animals, as well as humans, can serve as potential reservoirs resulting in contamination of food and water, while feco-oral transmission is also possible. The disease is globally distributed and, in the USA, Canada, Australia, and Europe it is considered one of the most common water borne pathogens. Diagnosis is established by examination of dyed fecal smears, serological tests, and PCR. The USA Food and Drug Administration approved nitazoxanide for human therapy.

Babesiosis is a tick-borne disease caused by the parasites of the genus Babesia. Over 100 species of Babesia are described, most causing high morbidity in animals, while only some are competent human pathogens. Disease transmission occurs by bite of an infected tick, blood transfusion, or via the placenta. Babesiosis is confirmed on all continents with B. microti (rodents) found in North America, B. divergens (cattle) most commonly found in Europe, and some infections by B. duncani and B. venatorum [30]. The occurrence of babesiosis is related to tick distribution and competent vector species of ticks are Ixodes scapularis, I. ricinus, and I. persulcatus. Babesia can be found also in tick species Dermacentor reticulatus, D. marginatus, D. silvarum, Haemaphysalis longicornis, H. punctata, H. concinna, H. leporispalustris, H. japonica, H. sulcata, Hyalomma marginatum, Amblyomma variegatum, Argas (Carios) vespertilionis, Rhipicephalus simus, R. turanicus, R. bursa, R. microplus, and R. sanguineus. Global annual prevalence is 12.45%; largest in North America (27.81%), Europe (9.88%), Asia (9.30%) and Africa (8.55%) [30]. Human infection is mostly asymptomatic, sometimes with fever, headache, lethargy, loss of appetite, nausea, and dyspnea. Older and immunocompromised individuals are at greater risk of developing more severe symptoms such as hepatomegaly and kidney failure. Diagnosis is made by macroscopical examination of blood smears. Patients with mild disease receive therapy of atovaquone and azithromycin, while in severe cases clindamycin and kinin are used. Since currently there is no vaccine available, recommendations are to avoid tick bites using repellents and appropriate clothing. Babesiosis gains more priority for control due to the risks of its spread influenced by climate changes, vector distribution, and a huge impact on public health.

Amebiasis is a disease caused by Entamoeba hystolitica leading to dysentery in humans. It is transmitted by contaminated food, and water and results in a high case fatality rate especially in children from poor countries [31]. In addition to humans E. histolytica can be found in primates, cats, dogs, and other animals such as mice and pigs serving as reservoirs. Besides E. hystolitica other parasitic species are recorded; E. dispar, E. moshkovskii, E. coli, E. hartmanni. E. histolytica is globally distributed, with the highest occurrence in tropical and sub-tropical regions of South America, Africa, and Asia, especially in rural areas with poor sanitary conditions and malnutrition. Amebiasis follows giardiasis and campylobacteriosis is the leading cause of gastrointestinal disease in humans. The life cycle of E. histolytica is relatively simple and has two stages; cysts and vegetative trophozoite. Mature cysts as an infectious form of the parasite are found in feces, while trophozoites invasive form are in epithelial cells of the intestine. By feco-oral route and ingestion by food and water infectious cysts of E. histolytica passage through the stomach, mature in the ileum into trophozoite which colonizes the large intestine and destroys epithelial cells causing inflammation and dysentery. Parasites can by portal vein reach the liver and cause extraintestinal infection followed by liver, lung, or brain abscesses [32]. Clinical symptoms vary from diarrhea to severe dysentery accompanied by abdominal pain, and watery or bloody stool. Diagnosis by symptoms is difficult, hence parasitological, serological, and molecular tests are used. The ELISA antigen test is available, while out of molecular assays conventional and multiplex PCR are used as well as Loop-mediated isothermal amplification test (LAMP). Treatment includes amebicides such as metronidazole, emetine, chloroquine, diloxanide-furoate, and some antibiotics (tetracycline, paromomycin, erythromycin).

5. Prevention and control of parasitic diseases

The constant increase in numbers of human parasitoses is being reported worldwide, while zoonotic parasites are among the most important causes of human infectious diseases, especially in undeveloped and developing countries [8]. Parasitoses make up the majority of the WHO/FAO lists of the NTDs, affecting 1000 million people in endemic areas, including 149 countries [7]. Causes for a surge of zoonotic parasitic infections in humans and the emergence of zoonotic parasites are various, such as overpopulation, migrations due to natural or man-made disasters, inadequate food and water supplies, encroachment leading to human interaction with new animal and/or parasite species and global warming influencing distribution and survival of parasites with resultant overflow infections [32, 33]. The consideration that parasitic diseases are exclusively associated with tropical and/or undeveloped countries with deficient hygienic and sanitary conditions in recent years has been widely challenged. The developed countries have witnessed an unprecedented increase of some parasitosis due to migrations, tourism, changing alimentary customs, and internationalization of commerce [34]. Parasitic infections are even more a threat to immunocompromised people due to genetic, iatrogenic, or infectious causes.

The surveillance of zoonotic parasites is important for common health and begins with an investigation of the presence of known and potentially zoonotic parasites in both human and animal populations and the environment. Estimating the extent of the parasites worldwide is hampered since in many countries they are not notifiable diseases, while in addition, the parasitosis can be asymptomatic or with an unspecific symptom that makes its diagnosis difficult [34]. The traditional approach to the prevention of parasitic infection in animals is based on chemoprophylaxis and treatments are commonly not scheduled, nor they are regular or specific and rely on owners’ awareness and initiative. In humans particularly in endemic areas regular and mass treatment is considered the main approach for infection control [4]. However, costs associated with diagnosis and prevention in animals and animal origin food are lesser than the mass treatment and diverse consequences of parasitic infections in humans [35]. Unselective treatment with anti-parasitic drugs has also brought to the light issue of resistance. According to Moleto [36] use of the broad spectrum anthelmintics started in the early 60s had superior outcomes, but the present situation is worsening with alarming consequences arising from the development of the multidrug-resistant parasite population. Currently, other means of parasitic infection control in animals are developed such as vaccination, breeding for resistance, biological control, and grazing management [36].

Since the animals and the environment are the main sources of infection for humans, control of zoonotic parasitoses needs to be primarily addressed at these levels. Rapid, simple, and available diagnostic methods are available for the detection of parasites in both companion and food animals and environmental samples, thus enabling early detection and specific treatment. Alongside investigations of parasitic infection in hosts, vectors require investigation and control (i.e., ticks, mosquitoes, sand flies, etc.). The trends toward an increase in vector populations are, in part, due to landscape fragmentation and an increase in the abundance of hosts. This, along with warming temperatures, has enabled the gaining vector competency, development, and survival of many vector species not as earlier limited by the season (temperatures and precipitation), altitude, and geographical distribution [37]. In the past dominant source of parasite infection in humans was infested animal origin food, which still is important but the majority of human infection nowadays is linked to companion animals and outdoor activities (contaminated environment and vectors).

Further down the food chain control of food-borne parasitoses in animal origin food needs to be part of sanitary and quality control in food processing establishments (i.e., slaughterhouses) [35]. In addition to regulated meat inspection, other methods have become available such as commercial serologic detection kits (for screening antibodies in milk) and near-infrared hyperspectral imaging (for animal carcasses inspection) [35, 38]. Besides direct consequences on human health through parasite-infested food, parasitic diseases such as gastrointestinal parasitoses in food animals are the single most important cause of production losses [36]. Parasite infections are shown to significantly affect milk yield, lower milk protein content, impair fertility, and contribute to a more frequent onset of metabolic disorders in animals as well as cause condemnation of affected organs (i.e., liver) [38]. Considering traditionally low animal productivity in undeveloped and developing countries, simultaneously struggling with many animals health issues, further decrease in the availability of animal protein due to parasitism is a serious threat to food security, nutrition-related deficiency, and both the health and economic wellbeing of humans (Figure 2). Also, in developed countries, changes in production due to animal welfare perspectives (i.e., pasture access) and an increase in organic farming led to altered patterns of parasite prevalence in farmed animals. For example, an increase in F. hepatica prevalence and/or an increase in the geographical spread of this parasite alongside recognition of its zoonotic potential has been observed in some European countries during recent years [38].

Figure 2.

Impact of parasite infection in food animals [39].

Control of parasitic infections is difficult for various reasons. First, many of these parasitoses are zoonosis, which requires collaboration between the human and animal health sector. It was long recognized that many emerging zoonoses arise from complex, diverse, and constantly evolving factors related to the environment, people, and animals. Zoonotic parasitoses with emergence and adaptability, wide host range, and various means of transmission all highly influenced by the environment need One Health approaches in both investigations, health regulations, prevention, and control measures [40]. On the other hand, the socio-economic conditions of developing countries make it difficult to apply measures to prevent or combat these diseases. Research on vaccines is yet expected to produce applicable results, while sophisticated molecular diagnostics on a routine basis are not even done in developed countries.

6. Conclusion and recommendations

Parasitoses of humans and animals contribute significantly to a global burden of infectious diseases, public health, animal health, and production, especially considering current trends of disease emergence and re-emergence and the high and increasing dominance of zoonotic pathogens. Research shows that exposure and increased risk of zoonotic pathogens are influenced by global environmental, social, and economic trends mainly man-made. Understanding, predicting, addressing, and preventing diseases with fast-evolving virulence, host range, pathogenesis and epidemiology require multidisciplinary approaches and reactions. Genesis as well as consequences of novel and re-emerging pathogens is complex, hence it needs to be addressed in its entirety to be proactive. Researchers, international bodies, governments, and the entire global community are called to adopt and adapt in their efforts to combat common health and wellbeing threats either current or those inevitably looming over the horizon.