Review Article | Open Access
Mramba Nyindo, Abdul-Hamid Lukambagire, "Fascioliasis: An Ongoing Zoonotic Trematode Infection", BioMed Research International, vol. 2015, Article ID 786195, 8 pages, 2015. https://doi.org/10.1155/2015/786195
Fascioliasis: An Ongoing Zoonotic Trematode Infection
Zoonotic trematode infections are an area of the neglected tropical diseases that have become of major interest to global and public health due to their associated morbidity. Human fascioliasis is a trematode zoonosis of interest in public health. It affects approximately 50 million people worldwide and over 180 million are at risk of infection in both developed and underdeveloped countries. The one health paradigm is an area that seeks to address the problem of zoonotic infections through a comprehensive and sustainable approach. This review attempts to address the major challenges in managing human and animal fascioliasis with valuable insights gained from the one health paradigm to global health and multidisciplinary integration.
Fascioliasis is a disease of ruminants caused by two major parasitic trematodes, Fasciola hepatica and F. gigantica. Over the past two decades human fascioliasis has gained notice as a disease of primary importance. Human fascioliasis is currently classified as a plant/food-borne trematode infection, commonly acquired by eating metacercaria encysted on leaves that are eaten as vegetables . There is a high prevalence of fascioliasis among herding communities in low income countries because of their constant close association with livestock that they keep.
Fascioliasis was first recorded as early as 2000 BC. Animal fascioliasis causes significant disease among sheep and cattle, causing severe physical wasting. It contributes to losses of over $2 billion dollars per annum in the livestock industry in North and South America. Human fascioliasis also causes significant illness and morbidity, mainly among low income, farming communities. To date, no human deaths have been directly associated with fascioliasis. This fact accords the disease a low priority and contributes to its neglect as a significant cause of public health concern. Human fascioliasis is currently ranked under the food/plant trematode zoonoses as a neglected tropical disease (NTD) .
2. Materials and Methods
We conducted a literature search on human and animal fascioliasis in the past 15 years. We searched PubMed/MEDLINE resources, HINARI/PubMed, local, regional, and institutional e-libraries such as NIH, CDC, WHO, and IHI (Ifakara Health Institute, Tanzania) e-lib, East African Medical Journal, and African journals of public health as well as Vectors and Zoonoses for the following major keywords: “fascioliasis,” “human fascioliasis,” “Zoonoses,” “fasciola liver fluke,” “fasciola hepatica,” “fasciola gigantica,” “fascioliasis, F. hepatica,” “fascioliasis F. gigantica,” “human fascioliasis epidemiology,” “human fascioliasis distribution,” “trends in fascioliasis research,” and “fascioliasis outbreaks.” We searched published literature from 2000 to 2015. Also we referenced recognized full textbook articles as well as summaries and abstracts containing discernible content. We selected references that fitted to being included in the review. We excluded non-English translated articles and papers/publications that only focused on animal disease without a zoonotic aspect. This search allowed us to include 92 most relevant references out of 300.
3. Current Status
Fascioliasis is primarily a disease of ruminants, although over the past two decades human fascioliasis has gained significance as an important disease in humans . Human fascioliasis is commonly characterized by a hypoendemic pattern, with low and stable levels of prevalence among a defined population, and generally shows a focal endemic distribution. However, to date, there have been reports from every continent except the Antarctica, thereby showing a wide cosmopolitan distribution .
Among the zoonotic parasitic diseases, human fascioliasis is currently classified as a plant/food-borne trematode infection, with higher prevalence seen among farming communities in low income countries [3, 4]. The plant/food-borne trematodes comprise Fasciola hepatica, F. gigantica, and Fasciolopsis buski (family Fasciolidae), Gastrodiscoides hominis (family Gastrodiscidae), Watsonius watsoni, and Fischoederius elongatus (Family Paramphistomidae). Fasciola hepatica and F. gigantica infect the liver .
The fasciolids and the gastrodiscid cause important zoonoses distributed throughout many countries, while W. watsoni and F. elongatus have been only accidentally transmitted to humans. Present climate and global changes appear to increasingly affect the distribution of snail-borne helminthiases . This provides a good example of emerging/reemerging parasitic diseases in many countries as a consequence of various phenomena related to climatic and environmental changes as well as human socioeconomic activities [5, 7].
Despite the recent developments in diagnostic and surveillance techniques, some countries are still completely lacking in data on human fascioliasis. This may be because the disease is not endemic but is more likely due to underreporting/diagnosis especially in the resource limited settings. The underestimated global burden of the disease to date is approximated to be between 35 and 72 million people, with an additional 180 million at risk of infection [8–10]. Abundant data supporting animal Fasciola infections are available in many tropical developing countries and regions, with the corresponding presence of snail species responsible for transmission. Therefore, the possibility of transmission of animal fascioliasis to humans is high where close proximity of humans with domestic animals is common [3, 6].
Although suitable environment and interactions for transmission have been established in many potentially endemic areas, reliable diagnostic and surveillance methods to establish presence of human fascioliasis are usually lacking [2, 11, 12]. The apparent rarity of human fascioliasis infection in such areas underestimates the prevalence of the disease . Because local physicians may not be fully informed about human fascioliasis, they may mistake fascioliasis for other diseases with similar clinical picture [3, 13].
3.1. Distribution of Human Fascioliasis
To date, human fascioliasis has been identified in many countries. The highest prevalence has been reported in Bolivia, Peru, Cuba, China, Spain, Nile Delta in Egypt, central areas of Vietnam, and Northern Iran [1, 14]. Bovine fascioliasis accounts for the majority of transmissions and is evenly spread around the world causing 29% of zoonoses . Hyperendemicity of human fascioliasis has been noted in the Middle East and North African (MENA) region [16, 17] particularly in Egypt [10, 18], Ethiopia , Iran [14, 20], Iraq , Syria , and Saudi Arabia .
The highest prevalence has been reported in the South American highlands of Bolivia and Peru [9, 22]. High prevalence of human fascioliasis has been associated with recent climate changes, human settlement, and socioeconomic activities [4, 7, 23]. Also in South America, Argentina , Brazil , and Mexico  have recently reported epidemics of human fascioliasis. In South East Asia (SEA) and the Indian subcontinent, Cambodia , China [26–28], Vietnam , Singapore , Philippines, and India [30–32] have also recently reported rising case numbers of the disease that were previously unseen at country or regional health systems.
3.2. Human Fascioliasis in Europe and America
Europe has also had a long history of the disease in Italy [33, 34] and Spain [1, 11], Turkey [35–37], Britain [38, 39], France , and Greece . Scattered cases have also been reported from North America  and Cuba [42, 43]. According to recent reviews [1, 44, 45], fascioliasis is probably the most widespread parasitic infection worldwide. With increased travel, open free trade, coupled with economic activities, and rural-urban human migration, fascioliasis is set to become a major disease of interest in public health, travel, and trade medicine [15, 45–48].
3.3. Life Cycle of Fasciola
Knowledge of the life cycle of a parasite may contribute to control strategies focusing on either the mammalian host or the vector. Infected mammals including not only cattle, sheep, buffaloes, donkeys, and pigs but also horses, goats, dromedaries, camels, llamas, and other herbivores pass ovulated eggs in stool into fresh-water sources [12, 19]. Since the Fasciola worm lives in the bile ducts of such animals, its unembryonated eggs reach the intestine with bile and are voided with feces. Fresh water is required for the development of intermediate stages of the Fasciola species in the snail. The ciliated miracidium hatches from the egg. It bores a snail in the genus Lymnaea and develops into a sporocyst. The next developmental stages are redia and cercaria [5, 9] which later vacate the snail. The cercaria can infect the definitive mammalian host, including humans passively when the host drinks infected water, or it can encyst on leaves and the mammalian host becomes infected when it eats leaves containing the metacercariae .
The ingested metacercariae excyst in the duodenum and migrate into the peritoneal cavity and finally reach the liver. They bore through the liver capsule and in about 12 weeks enter the bile ducts where they start to lay eggs. Infected persons develop hyperplasia of the bile ducts. Clinically, patients lose appetite and have nausea and diarrhea. Urticaria, acute epigastric pain, jaundice, eosinophilia, and hepatomegaly are common findings. In the chronic phase of the disease, hyperplasia of the gall bladder and biliary epithelium occurs and this leads to biliary tract obstruction. When live adult worms in an infected liver lodge in the throat region, they cause discomfort. After a period of about one to two months, a hypersensitivity reaction in the pharyngeal area develops. The term Halzoun syndrome describes the resulting suffocative immunological reaction at the pharyngeal area [6, 11, 16].
Factors noted to contribute to increased human transmission of fascioliasis include (i) high density of both human and animal populations living in close proximity, (ii) the presence of abattoirs and wet markets operating with rudimentary hygiene, limited cold chain for distribution, and low levels of meat inspection and biosafety measures, (iii) widespread consumption of raw/undercooked blood, meat, organ tissues, and offals and consumption of raw leaf vegetables, and (iv) the use untreated water sources for household use and/or use of untreated wastewater and sewage for agriculture [5, 6].
3.4. Snail Vectors and Distribution of Fascioliasis in Africa
The distribution of the F. hepatica and F. gigantica parasites is ubiquitous, mainly attributed to and associated with the equally global distribution of the viable, intermediate fresh-water snail hosts [3, 5]. Species distribution of the lymnaeid snails may be generalized as mainly temperate, at a higher altitude over 2500 m above sea level for Lymnaea truncatula, L. rubiginosa, and their associated parasite, F. hepatica, while L. rupestris and L. natalensis alongside their typical parasite F. gigantica have a more tropical/subtropical distribution at lower altitudes, below 2000 m [17, 49, 50].
In several countries in Africa and Asia it should be considered that F. hepatica and F. gigantica coexist, notably in areas of the Nile drainage, the great lakes mountain ranges, and the rift valley arms. In such environments, alternating altitudes and climatic conditions favour the respective snail vectors [4, 11, 50]. The differential specific diagnosis relating to eggs and specific antigens is of interest because of their different transmission, epidemiology, and control measures . Mixed infections and hybridization have also been cited recently [52–54].
Surveys done in the hyperendemic Nile Delta valley in Egypt [4, 18] and river Tana basin in Ethiopia  found a high association between fascioliasis and schistosomiasis as well as myriad other intestinal parasites . A gender distribution skewed in both intensity and prevalence towards girls in the age group of 9–11 years among a young key population was also noted. The coinfection and childhood distribution raise a further differential in the clinical presentation and etiology of parasitic illnesses on the continent especially in rural, animal rearing areas [4, 19].
Other African countries reporting scattered cases of human fascioliasis include Cameroon , Chad , Senegal , South Africa , and Zimbabwe . Animal fascioliasis on the other hand has been extensively reported in almost all countries in the African equatorial belt  and east, central, west, and southern Africa [4, 49, 50, 60, 61]. A favourable climatic and environmental picture further presents for easy human transmission (Figure 1).
On the other hand, it is strange that no published studies or reports on the disease in humans have emerged from these potentially endemic regions.
Triclabendazole (TCBZ) is the drug of choice in the treatment of fascioliasis. However, in addition to the changing pattern of disease, reports of resistance to TCBZ have appeared in the literature [62–64], although they may not all represent genuine cases of resistance. Nevertheless, any reports of resistance are a concern, because TCBZ is the only drug that has shown high efficacy against the migratory and juvenile stages of infection to date [1, 3]. Resistance to the drug could potentially set back any recent gains made in the efforts to combat and manage human and animal fascioliasis.
The diagnosis of fascioliasis has changed considerably in the 3 decades since it became a disease of primary human importance. Detection of eggs in patients’ stool samples is still considered the most conclusive diagnosis at the clinical level [2, 9, 11]. New, improved coprologic antigen tests , serological and ELISA tests [52, 66], radiological and imaging diagnostics [30, 67, 68], and highly specific molecular techniques [26, 69] have been developed and are the current hallmark of sound and scientific studies in the field [1, 70]. Detection of resistant strains, differentiation of the acute stages from chronic stages of infection, and identifying reinfections after treatment still remain a challenge at the clinical level.
Geospatial distributions of snail vectors and parasite transmission [59, 71, 72] and of zoonotic epidemiology [3, 27] are recent areas of development in anticipating and planning for epidemics of human fascioliasis. Model drugs and interventions [62, 73] are also areas of novel research into the effective management of human and animal fascioliasis.
4. Issues of Immediate Concern about Fascioliasis in the Least Developed Countries
Although fascioliasis has been established as a disease of human importance, it is still considered primarily an animal disease, particularly of sheep and cattle . Lack of awareness presents a major obstacle in the effective management of human fascioliasis [1, 2]. Unfortunately in many of the least developed countries burdened by poverty and infectious diseases, human fascioliasis is not a recognized and reportable disease. Awareness and sensitization are key first steps to any planned intervention strategies.
Fortunately to date there have been no reported deaths directly associated with human fascioliasis infection. This inevitably attributes a low emergency health priority to the disease, making it one of the most neglected tropical diseases . The disease has also been reported to have a much higher prevalence among the female children of school going age. The associated morbidity and Disability Adjusted Life Years (DALY) impact of the disease are thus of more significant concern [16, 36]. The consequent morbidities on chronic disease significantly contribute to poor quality of life, expectancy, and productive output since the adult worm can live for over 10 years in a suitable host [4, 19].
There have been only scattered reports of outbreaks of fascioliasis in irrigated agricultural areas free from domestic animals [18, 19]. The highest proportions of reported cases are zoonotic in nature, and so any intervention strategies should ideally address the problem at the veterinary level as well. Human fascioliasis is hardly reported in those countries where animal fascioliasis is highly prevalent [4, 76, 77]. Vigilant surveillance and screening programs should be implemented in such areas, with an emphasis on interdisciplinary involvement across various professions [5, 54].
The global awareness and one health approach to zoonoses are by far the most comprehensive approach to fascioliasis . Sustained efforts are still required including control measures for trade and travel to curb the spread of infected animals from one country to another. Improved water and food hygiene programs are further important components of control programs [44, 74]. Stakeholder involvement and the political will to back such strategies are crucial to the effective uptake of these interventions.
Definitive reports of drug resistance to triclabendazole  should be rigorously investigated and alternative treatment options sought. Vaccine development should also be an area of future research. Mixed infections with other trematode or intestinal parasites [17, 79–81] confound early detection of fascioliasis. Delayed and missed diagnoses especially among the young key population magnify the DALY impact of the disease [82, 83].
5. Future Challenges
The 21st century has seen a dawning in the knowledge on human fascioliasis evidenced by the number of publications on the subject over the last 10 years. The complete implementation of this new knowledge and its translation into tangible results remain a challenge in the least developed countries (LDCs). Populations in LDCs are the highest at risk of disease because of the following reasons: (i) poor access to this new body of knowledge, (ii) limited resources to put it into practical use, or (iii) having these limited resources dedicated to “more threatening” problems than fascioliasis [1, 2, 45]. The poverty-disease cycle is indeed a vicious, autocatalytic cascade.
A typical complicating infection control scenario of zoonotic infections including fascioliasis in sub-Saharan Africa includes: (a) global warming and civil unrest, (b) close proximity to domestic animals, (c) rural-urban migration with poor personal, water, and food hygiene, and (d) lax biosafety and surveillance systems. Therefore, control programs of human fascioliasis should have an integrated approach whereby all factors that contribute to the presence of the disease are considered [44, 75].
Cutting edge advances in diagnostic, surveillance, and management techniques of fascioliasis have been made. Yet the developing countries and particularly the lowest income communities are not able to access these advances because of poverty. Heavily burdened by diseases, civil unrest, and competition for scarce resources, it is not surprising that there are hardly any reports on human fascioliasis from these regions [2, 4]. Control programs should first consider rigorous awareness campaigns and sensitization on both the magnitude and impact of human fascioliasis in humans and animals .
The current “One Health Integrated Global Approach to Disease’’ presents by far the most comprehensive and participatory solution, not only to human fascioliasis but also to the bulk of zoonotic diseases at large [44, 85]. A classic example of the problems it tackles can best be elaborated in the recent drive to “Go Green,’’ as a healthy approach to the modern artificial lifestyle. Compartmentalized to specific sections like nutrition and preventive medicine, agriculture, and industry, this has seen an unprecedented increase in the consumption of fresh, raw/green fruit and vegetables [86, 87]. This is however poorly backed by water safety, fertilizer-pesticide use control, and waste management. The consumption of poorly monitored, produced, and stored fresh green vegetables has contributed to the increased spread of plant/food-borne trematodiases including fascioliasis, among many other health problems [48, 83].
Controlled clinical trials to investigate reported cases of triclabendazole and bithionol resistance of Fasciola are areas of immediate research interest. Further development of chemotherapeutic options like the Myrrh-derived Mirazid and nitazoxanide [19, 73, 88], as well as other novel interventions aimed at the intermediate snail hosts [71, 89], may provide much needed alternative chemotherapy. Control strategies aimed at the animal reservoirs and active surveillance for disease hotspots allow early intervention while improved food and water safety combined with possible vaccine development is vital to prevention strategies of human fascioliasis. In order to succeed, all this needs to be backed by rigorous awareness, sensitization campaigns and political will to maximize uptake [75, 90].
Human fascioliasis is perceived as a low significance “Neglected Tropical Disease of Poverty” [16, 42, 45, 87]. As interventions and solutions to the disease are developed in the more developed countries/communities, support structures, basic amenities, and simple interdisciplinary collaborations degenerate equally fast in the lowest income communities at particularly high risk of infection [74, 75]. A case in point is observed in the abundance of veterinary reports on animal fascioliasis out of sub-Saharan African countries, countered by an almost total disregard for the human zoonoses among the medical and public health community [49, 50, 53]. It is surprising that human fascioliasis is still not a reportable disease in many of these countries.
However, because of easy and fast global travel currently prevailing, open markets and free trade, cultural tourism, and massive cultural and national integration, the problems of the developing countries may spill to more developed countries [39, 45, 46]. The dawn of unpredictable climate changes and their effect on ecobiology, civil unrest, and the simple natural laws of evolution are factors that have altered the patterns of spread of zoonoses [47, 48]. For example, the recent global threat from the West African Ebola outbreak is a fresh reminder of the far reaching ramifications of unexpected disease outbreaks on the continent [75, 91]. Human fascioliasis is still nonfatal and results from interventions used in most hyperendemic regions prove that it can be effectively controlled, if not eradicated. As an NTD, this should be a tangible target [74, 87].
The fact that human fascioliasis reporting in the least developed nations is lacking presents a particularly difficult challenge. These countries are already heavily burdened by different diseases and lack access to adequate resources. Therefore, despite major progress in the diagnosis and control of human fascioliasis in the more developed countries, the disease continues to be a significant public health problem [84, 92].
The breakdown of interdisciplinary collaborations, coupled with political and civil unrest, further perpetuates the prevalence of many diseases including fascioliasis in the developing countries. We propose that control measures of fascioliasis should include (i) general and clinical awareness, (ii) integrated and multidisciplinary collaborations, (iii) sustained interventions backed by political will, and (iv) vaccine and drug development.
Conflict of Interests
The authors declare that there is no conflict of interests.
Both authors contributed equally to the paper formulation.
- S. Mas-Coma, M. A. Valero, and M. D. Bargues, “Fascioliasis,” in Digenetic Trematodes, vol. 766 of Advances in Experimental Medicine and Biology, chapter 4, pp. 77–114, Springer, 2014.
- S. Mas-Coma, M. D. Bargues, and M. A. Valero, “Diagnosis of human fascioliasis by stool and blood techniques: update for the present global scenario,” Parasitology, vol. 141, no. 1, pp. 1918–1946, 2014.
- R. Mera y Sierra, V. H. Agramunt, P. Cuervo, and S. Mas-Coma, “Human fascioliasis in Argentina: retrospective overview, critical analysis and baseline for future Research,” Parasites & Vectors, vol. 4, no. 1, article 104, 2011.
- M. F. M. Soliman, “Epidemiological review of human and animal fascioliasis in Egypt,” The Journal of Infection in Developing Countries, vol. 2, no. 3, pp. 182–189, 2008.
- J. J. Carrique-Mas and J. E. Bryant, “A review of foodborne bacterial and parasitic zoonoses in Vietnam,” EcoHealth, vol. 10, no. 4, pp. 465–489, 2013.
- S. Mas-Coma, M. D. Bargues, and M. A. Valero, “Fascioliasis and other plant-borne trematode zoonoses,” International Journal for Parasitology, vol. 35, no. 11-12, pp. 1255–1278, 2005.
- P. J. Bless, F. Schär, V. Khieu et al., “High prevalence of large trematode eggs in schoolchildren in Cambodia,” Acta Tropica, vol. 141, no. 1, pp. 295–302, 2015.
- C. J. McDaniel, D. M. Cardwell, R. B. Moeller, and G. C. Gray, “Humans and cattle: a review of bovine zoonoses,” Vector-Borne and Zoonotic Diseases, vol. 14, no. 1, pp. 1–19, 2014.
- M. A. Valero, I. Perez-Crespo, M. V. Periago, M. Khoubbane, and S. Mas-Coma, “Fluke egg characteristics for the diagnosis of human and animal fascioliasis by Fasciola hepatica and F. gigantica,” Acta Tropica, vol. 111, no. 2, pp. 150–159, 2009.
- M. V. Periago, M. A. Valero, M. El Sayed et al., “First phenotypic description of Fasciola hepatica/Fasciola gigantica intermediate forms from the human endemic area of the Nile Delta, Egypt,” Infection, Genetics and Evolution, vol. 8, no. 1, pp. 51–58, 2008.
- S. Mas-Coma, M. A. Valero, and M. D. Bargues, “Climate change effects on trematodiases, with emphasis on zoonotic fascioliasis and schistosomiasis,” Veterinary Parasitology, vol. 163, no. 4, pp. 264–280, 2009.
- M. W. Robinson and J. P. Dalton, “Zoonotic helminth infections with particular emphasis on fasciolosis and other trematodiases,” Philosophical Transactions of the Royal Society B: Biological Sciences, vol. 364, no. 1530, pp. 2763–2776, 2009.
- J. D. Lapook, A. M. Magun, K. G. Nickerson, and J. I. Meltzer, “Sheep, watercress, and the internet,” The Lancet, vol. 356, no. 9225, p. 218, 2000.
- M. Saberinasab, M. Mohebali, G. Molawi, E. Beigom Kia, M. Aryaeipour, and M. B. Rokni, “Seroprevalence of human fascioliasis using indirect ELISA in Isfahan district, central Iran in 2013,” Iranian Journal of Parasitology, vol. 9, no. 4, pp. 461–465, 2014.
- K. E. Jones, N. G. Patel, M. A. Levy et al., “Global trends in emerging infectious diseases,” Nature, vol. 451, Article ID 06536, pp. 990–993, 2008.
- P. J. Hotez, L. Savioli, and A. Fenwick, “Neglected tropical diseases of the middle east and north africa: review of their prevalence, distribution, and opportunities for control,” PLoS Neglected Tropical Diseases, vol. 6, no. 2, Article ID e1475, 2012.
- A. I. Youssef and S. Uga, “Review of parasitic zoonoses in Egypt,” Tropical Medicine and Health, vol. 42, no. 1, pp. 3–14, 2014.
- M. A. Mekky, M. Tolba, M. O. Abdel-Malek, W. A. Abbas, and M. Zidan, “Human fascioliasis: a re-emerging disease in Upper Egypt,” The American Journal of Tropical Medicine and Hygiene, vol. 93, no. 1, pp. 76–79, 2015.
- T. Fentie, S. Erqou, M. Gedefaw, and A. Desta, “Epidemiology of human fascioliasis and intestinal parasitosis among schoolchildren in Lake Tana Basin, northwest Ethiopia,” Transactions of the Royal Society of Tropical Medicine and Hygiene, vol. 107, no. 8, Article ID trt056, pp. 480–486, 2013.
- J. Abdi, R. Naserifar, M. R. Nejad, and V. Mansouri, “New features of fascioliasis in human and animal infections in Ilam province, Western Iran,” Gastroenterology and Hepatology from Bed to Bench, vol. 6, no. 3, pp. 152–155, 2013.
- H. A. Hassan, R. A. Majid, N. G. Rashid et al., “Eosinophilic granulomatous gastrointestinal and hepatic abscesses attributable to basidiobolomycosis and fasciolias: a simultaneous emergence in Iraqi Kurdistan,” BMC Infectious Diseases, vol. 13, no. 1, article 91, 2013.
- J. G. Esteban, C. González, M. D. Bargues et al., “High fascioliasis infection in children linked to a man-made irrigation zone in Peru,” Tropical Medicine and International Health, vol. 7, no. 4, pp. 339–348, 2002.
- M. M. Cabada, M. R. Goodrich, B. Graham et al., “Fascioliasis and eosinophilia in the highlands of Cuzco, Peru and their association with water and socioeconomic factors,” American Journal of Tropical Medicine and Hygiene, vol. 91, no. 5, pp. 989–993, 2014.
- S. C. Bennema, R. G. C. Scholte, M. B. Molento, C. Medeiros, and O. D. S. Carvalho, “Fasciola hepatica in bovines in Brazil: data availability and spatial distribution,” Revista do Instituto de Medicina Tropical de São Paulo, vol. 56, no. 1, pp. 35–41, 2014.
- J. L. Zumaquero-Ríos, J. Sarracent-Pérez, R. Rojas-García et al., “Fascioliasis and intestinal parasitoses affecting schoolchildren in Atlixco, Puebla State, Mexico: epidemiology and treatment with nitazoxanide,” PLoS Neglected Tropical Diseases, vol. 7, no. 11, Article ID e2553, 2013.
- J.-X. Chen, M.-X. Chen, L. Ai et al., “An outbreak of human Fascioliasis gigantica in Southwest China,” PLoS ONE, vol. 8, no. 8, Article ID e71520, 2013.
- W. S. Gu, H. Y. Zou, J. Li et al., “Clinical diagnosis and treatment in an outbreak of Fasciola gigantica infection in Yunnan Province,” Chinese Journal of Parasitology & Parasitic Diseases, vol. 30, no. 6, pp. 455–459, 2012.
- X. N. Zhou, L. V. Shan, G. J. Yang et al., “Spatial epidemiology in zoonotic parasitic diseases: insights gained at the 1st International Symposium on Geospatial Health in Lijiang, China, 2007,” Parasites &Vectors, vol. 2, no. 10, 2007.
- S. H. Ahamed, J. Ho, and S. K. Venkatesh, “A fluke diagnosis,” Annals of the Academy of Medicine Singapore, vol. 42, no. 7, pp. 368–370, 2013.
- V. Kumari, T. Banerjee, N. Negi, M. L. Gupta, K. Tiwari, and M. Gupta, “Human fascioliasis with biliary complications,” The Journal of Communicable Diseases, vol. 45, no. 1-2, pp. 91–93, 2013.
- J. P. Ghildiyal, D. P. Singh, and R. K. Goyal, “Cutaneous images of interest of fascioliasis from India,” Indian Journal of Gastroenterology, vol. 5, no. 3, pp. 499–500, 2014.
- J. Ramachandran, S. S. R. Ajjampur, A. Chandramohan, and G. M. Varghese, “Cases of human fascioliasis in India: tip of the iceberg,” Journal of Postgraduate Medicine, vol. 58, no. 1, pp. 150–152, 2012.
- S. Gabrielli, P. Calderini, L. Dall'Oglio et al., “Parasitological and molecular observations on a little family outbreak of human fasciolosis diagnosed in Italy,” The Scientific World Journal, vol. 2014, Article ID 417159, 5 pages, 2014.
- D. Otranto and M. L. Eberhard, “Zoonotic helminths affecting the human eye,” Parasites & Vectors, vol. 4, article 41, 2011.
- M. K. Karahocagil, H. Akdeniz, M. Sunnetcioglu et al., “A familial outbreak of fascioliasis in Eastern Anatolia: a report with review of literature,” Acta Tropica, vol. 120, no. 1-2, pp. 119–29, 2011.
- B. Tavil, I. Ok-bozkaya, H. Tezer, and B. Tunç, “Severe iron deficiency anemia and marked eosinophilia in adolescent girls with the diagnosis of human fascioliasis,” The Turkish Journal of Pediatrics, vol. 56, no. 2, pp. 307–309, 2014.
- R. Beştaş, K. Yalçin, and M. Çiçek, “Cholestasis caused by Fasciola gigantica,” Turkish Society for Parasitology, vol. 38, no. 3, pp. 201–204, 2014.
- N. J. Fox, P. C. L. White, C. J. McClean, G. Marion, A. Evans, and M. R. Hutchings, “Predicting impacts of climate change on fasciola hepatica risk,” PLoS ONE, vol. 6, no. 1, Article ID e16126, 2011.
- M. A. Chand, J. S. Herman, D. G. Partridge, K. Hewitt, and P. L. Chiodini, “Imported human fascioliasis, United Kingdom,” Emerging Infectious Diseases, vol. 15, no. 11, pp. 1876–1877, 2009.
- S. F. Assimakopoulos, A. Psilopanagioti, A. Michail, C. Papakonstantinou, C. Gogos, and C. Labropoulou-Karatza, “Severe eosinophilia and hepatic lesion: a rare case of fascioliasis from Greece,” Journal of Gastrointestinal and Liver Diseases, vol. 19, no. 2, p. 125, 2010.
- S. A. Weisenberg and D. E. Perlada, “Domestically acquired fascioliasis in northern california,” The American Journal of Tropical Medicine and Hygiene, vol. 89, no. 3, pp. 588–591, 2013.
- S. Mas-Coma, “Human fascioliasis,” in Waterborne Zoonoses: Identification, Causes and Control, J. A. Cotruvo, A. Dufour, G. Rees et al., Eds., vol. 9, pp. 305–322, World Health Organization (WHO), International Water Association Publishing, 2004.
- A. A. Vázquez, J. Sánchez, J.-P. Pointier, A. Théron, and S. Hurtrez-Boussès, “Fasciola hepatica in Cuba: compatibility of different isolates with two intermediate snail hosts, Galba cubensis and Pseudosuccinea columella,” Journal of Helminthology, vol. 88, no. 4, pp. 434–440, 2014.
- S. Bidaisee and C. N. L. Macpherson, “Zoonoses and one health: a review of the literature,” Journal of Parasitology Research, vol. 2014, Article ID 874345, 8 pages, 2014.
- K. Ashrafi, M. D. Bargues, S. O'Neill, and S. Mas-Coma, “Fascioliasis: a worldwide parasitic disease of importance in travel medicine,” Travel Medicine and Infectious Disease, vol. 12, no. 6, pp. 636–649, 2014.
- N. C. Banks, D. R. Paini, K. L. Bayliss, and M. Hodda, “The role of global trade and transport network topology in the human-mediated dispersal of alien species,” Ecology Letters, vol. 18, no. 2, pp. 188–199, 2015.
- D. A. Travis, P. Sriramarao, C. Cardona et al., “One Medicine One Science: a framework for exploring challenges at the intersection of animals, humans, and the environment,” Annals of the New York Academy of Sciences, vol. 1334, no. 1, pp. 26–44, 2014.
- O. Lev and B. Rager-Zisman, “Protecting public health in the age of emerging infections,” The Israel Medical Association Journal, vol. 16, no. 11, pp. 677–682, 2014.
- J. D. Keyyu, N. C. Kyvsgaard, J. Monrad, and A. A. Kassuku, “Effectiveness of strategic anthelmintic treatments in the control of gastrointestinal nematodes and Fasciola gigantica in cattle in Iringa region, Tanzania,” Tropical Animal Health and Production, vol. 41, no. 1, pp. 25–33, 2009.
- A. Howell, L. Mugisha, J. Davies et al., “Bovine fasciolosis at increasing altitudes: parasitological and malacological sampling on the slopes of Mount Elgon, Uganda,” Parasites & Vectors, vol. 5, no. 1, article 196, 2012.
- F. Curtale, Y. A. W. Hassanein, P. Barduagni et al., “Human fascioliasis infection: gender differences within school-age children from endemic areas of the Nile Delta, Egypt,” Transactions of the Royal Society of Tropical Medicine and Hygiene, vol. 101, no. 2, pp. 155–160, 2007.
- G. B. Santana, J. P. Dalton, F. V. Camargo, M. Parkinson, and M. Ndao, “The diagnosis of human fascioliasis by enzyme-linked immunosorbent assay (ELISA) using recombinant cathepsin L protease,” PLoS Neglected Tropical Diseases, vol. 7, no. 9, Article ID e2414, 2013.
- H. I. Necati, G. Aktas, H. Savli et al., “A Fascioliasis case: a not rare cause of hypereosinophilia in developing countries, present in developed too,” Mediterranean Journal of Hematological Infectious Diseases, vol. 4, no. 1, 2012.
- F. Curtale, A. Y. Hassanein, A. E. l. Wakeel et al., “Distribution of human fascioliasis by age and gender among rural population in the Nile Delta, Egypt,” Transactions of the Royal Society of Tropical Medicine and Hygeine, vol. 101, no. 2, pp. 155–160, 2008.
- J. V. Mbuh and J. Mbwaye, “Serological changes in goats experimentally infected with Fasciola gigantica in Buea sub-division of S.W.P. Cameroon,” Veterinary Parasitology, vol. 131, no. 3-4, pp. 255–259, 2005.
- V. Jean-Richard, L. Crump, A. A. Abicho et al., “Prevalence of Fasciola gigantica infection in slaughtered animals in south-eastern Lake Chad area in relation to husbandry practices and seasonal water levels,” BMC Veterinary Research, vol. 10, article 81, pp. 1646–1648, 2014.
- M. M. Ka, M. Mbengue, B. M. Diop et al., “Two unexpected cases of hepatobiliary fascioliasis in Dakar,” Dakar Médical, vol. 47, no. 2, pp. 202–205, 2002.
- J. Black, N. Ntusi, P. Stead, B. Mayosi, and M. Mendelson, “Human fascioliasis in South Africa,” South African Medical Journal, vol. 103, no. 9, pp. 658–659, 2013.
- U. B. Pedersen, M. Stendel, N. Midzi et al., “Modelling climate change impact on the spatial distribution of fresh water snails hosting trematodes in Zimbabwe,” Parasites & Vectors, vol. 7, article 536, 2014.
- N. Maingi, R. O. Otieno, E. H. Weda, and V. M. Gichohi, “Effects of three anthelmintic treatment regimes against Fasciola and nematodes on the performance of ewes and lambs on pasture in the highlands of Kenya,” Veterinary Research Communications, vol. 26, no. 7, pp. 543–552, 2002.
- J. M. Kithuka, N. Maingi, F. M. Njeruh, and J. N. Ombui, “The prevalence and economic importance of bovine fasciolosis in Kenya: an analysis of abattoir data,” Onderstepoort Journal of Veterinary Research, vol. 69, no. 4, pp. 255–262, 2002.
- Q. Liu, N. Cheng, Y. Zhou, and X.-N. Xu, “Research progress on fascioliasis,” Chinese Journal of Parasitology & Parasitic Diseases, vol. 31, no. 3, pp. 229–234, 2013.
- I. Fairweather, “Reducing the future threat from (liver) fluke: realistic prospect or quixotic fantasy?” Veterinary Parasitology, vol. 180, no. 1-2, pp. 133–143, 2011.
- C. Boulliat, A. Wolf, K. Gaillard, and M. Oliver, “Triclabendazole,” Médecine Tropicale, vol. 70, no. 4, pp. 341–342, 2010.
- M. A. Valero, M. V. Periago, I. Pérez-Crespo et al., “Field evaluation of a coproantigen detection test for fascioliasis diagnosis and surveillance in human hyperendemic areas of Andean Countries,” PLoS Neglected Tropical Diseases, vol. 6, no. 9, Article ID e1812, 2012.
- M. B. Rokni, J. Massoud, S. M. O'Neill, M. Parkinson, and J. P. Dalton, “Diagnosis of human fasciolosis in the Gilan province of Northern Iran: application of cathepsin L-ELISA,” Diagnostic Microbiology & Infectious Disease, vol. 44, no. 2, pp. 175–179, 2002.
- A. Dusak, M. R. Onur, M. Cicek, U. Firat, T. Ren, and V. Dogra, “Radiological imaging features of Fasciola hepatica infection—a pictorial review,” Journal of Clinical Imaging Science, vol. 2, article 2, 2012.
- C. Behzad, F. Lahmi, M. Iranshahi, and A. H. M. Alizadeh, “Finding of biliary fascioliasis by endoscopic ultrasonography in a patient with eosinophilic liver abscess,” Case Reports in Gastroenterology, vol. 8, no. 1, pp. 310–318, 2014.
- Y. Dar, S. Amer, A. Mercier, B. Courtioux, and G. Dreyfuss, “Molecular identification of Fasciola spp. (Digenea: Fasciolidae) in Egypt,” Parasite, vol. 19, no. 2, pp. 177–182, 2012.
- R. K. Prichard, M.-G. Basáñez, B. A. Boatin et al., “A research agenda for helminth diseases of humans: intervention for control and elimination,” PLoS Neglected Tropical Diseases, vol. 6, no. 4, Article ID e1549, 2012.
- U. B. Pedersen, N. Midzi, T. Mduluza et al., “Modelling spatial distribution of snails transmitting parasitic worms with importance to human and animal health and analysis of distributional changes in relation to climate,” Geospatial Health, vol. 8, no. 2, pp. 335–343, 2014.
- X.-N. Zhou, S. Lv, G.-J. Yang et al., “Spatial epidemiology in zoonotic parasitic diseases: insights gained at the international symposium on geospatial health in lijiang, China, 2007,” Parasites & Vectors, vol. 2, no. 1, article 10, 2009.
- I. Fairweather and J. C. Boray, “Fasciolicides: efficacy, actions, resistance and its management,” The Veterinary Journal, vol. 158, no. 2, pp. 81–112, 1999.
- D. Molyneux, Z. Hallaj, G. T. Keusch et al., “Zoonoses and marginalised infectious diseases of poverty: where do we stand?” Parasites & Vectors, vol. 4, no. 1, article 106, 2011.
- S. Welburn, I. Beange, M. Ducrotoy, and A. Okello, “The neglected zoonoses—the case for integrated control and advocacy,” Clinical Microbiology and Infection, vol. 21, no. 5, pp. 433–443, 2015.
- S. M. Walker, A. E. Makundi, F. V. Namuba et al., “The distribution of Fasciola hepatica and Fasciola gigantica within southern Tanzania—constraints associated with the intermediate host,” Parasitology, vol. 135, no. 4, pp. 495–503, 2008.
- E. S. Swai and E. Ulicky, “An evaluation of the economic losses resulting from condemnation of cattle livers and loss of carcass weight due to Fasciolosis: a case study from Hai town abattoir, Kilimanjaro region, Tanzania,” Livestock Research for Rural Development, vol. 21, no. 11, 2009.
- J. A. Winkelhagen, T. Mank, J. P. De Vries, and R. Soetekouw, “Apparent triclabendazole-resistant human Fasciola hepatica infection, the Netherlands,” Emerging Infectious Diseases, vol. 18, no. 6, pp. 1028–1029, 2012.
- M. Kaya, R. Beştaş, and S. Çetin, “Clinical presentation and management of Fasciola hepatica infection: single-center experience,” World Journal of Gastroenterology, vol. 17, no. 44, pp. 4899–4904, 2011.
- T. A. Karabuli, M. A. R. Shaikhani, S. H. S. Karadaghi, and K. H. Kasnazan, “Hepatobiliary and pancreatic Fascioliasis,” Journal of Gastroenterology and Hepatology, vol. 24, no. 7, p. 1309, 2009.
- H. H. Garcia, P. L. Moro, and P. M. Schantz, “Zoonotic helminth infections of humans: echinococcosis, cysticercosis and fascioliasis,” Current Opinion in Infectious Diseases, vol. 20, no. 5, pp. 489–494, 2007.
- M. Lopez, A. C. White Jr., and M. M. Cabada, “Burden of Fasciola hepatica infection among children from Paucartambo in Cusco, Peru,” The American Journal of Tropical Medicine and Hygiene, vol. 86, no. 3, pp. 481–485, 2012.
- T. Fürst, J. Keiser, and J. Utzinger, “Global burden of human food-borne trematodiasis: a systematic review and meta-analysis,” The Lancet Infectious Diseases, vol. 12, no. 3, pp. 210–221, 2012.
- Bio Ventures for Global Health, 2015, http://www.bvgh.org/Current-Programs/Neglected-Disease-Product-Pipelines/Global-Health-Primer/Diseases/cid/ViewDetails/ItemID/23.aspx.
- C. J. Standley, A. P. Dobson, and J. R. Stothard, “Out of animals and back again: schistosomiasis as a zoonosis in Africa,” in Shistosomiasis, pp. 209–230, InTech, 2012.
- A. Broglia and C. Kapel, “Changing dietary habits in a changing world: emerging drivers for the transmission of foodborne parasitic zoonoses,” Veterinary Parasitology, vol. 182, no. 1, pp. 2–13, 2011.
- P. J. Hotez, M. Alvado, M.-G. Basáñez et al., “The global burden of disease study 2010: interpretation and implications for the neglected tropical diseases,” PLoS Neglected Tropical Diseases, vol. 8, no. 7, Article ID e2865, 2014.
- M. Yakoot, “A short review of the anthelmintic role of mirazid,” Arquivos de Gastroenterologia, vol. 47, no. 4, pp. 393–394, 2010.
- R. M. Atlas, “One health: its origins and future,” in One Health: The Human-Animal-Environment Interfaces in Emerging Infectious Diseases, vol. 223 of Current Topics in Microbiology and Immunology, Springer, Berlin, Germany, 2012.
- N. M. Hung, H. Madsen, and B. Fried, “Global status of fish-borne zoonotic trematodiasis in humans,” Acta Parasitologica, vol. 58, no. 3, pp. 231–258, 2013.
- J. Keiser and J. Utzinger, “Food-borne trematodiases,” Clinical Microbiology Reviews, vol. 22, no. 3, pp. 466–483, 2009.
- C. M. Adema, C. J. Bayne, J. M. Bridger et al., “Will all scientists working on snails and the diseases they transmit please stand up?” PLoS Neglected Tropical Diseases, vol. 6, no. 12, Article ID e1835, pp. 1–2, 2012.
Copyright © 2015 Mramba Nyindo and Abdul-Hamid Lukambagire. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.