Fasciolosis

John Pius Dalton, John Dalton

• Publisher: CAB International
• Year: 2021
• ISBN:
  9781789246186
• Edition: 2
• Topic: Médecine
• Subtopic: Microbiologie et parasitologie médicales

Fasciolosis is a major global infection of livestock causing both huge losses to the agricultural community and affecting human health as a food-borne disease. Fully updated throughout, this new edition continues to cover the life cycle, biology, and development of the parasite; clinical pathology, immunology, diagnosis and vaccine development; and emergence, cause and mechanisms of drug resistance. It reviews the temperate liver fluke Fasciola hepatica, together with molecular, biochemical, control, and epidemiologial aspects of the tropical liver fluke F. gigantica. Many fundamental advances have taken place in the last two decades, but of particular importance has been the mapping of the draft genome of Fasciola. In addition, comprehensive advances in transcriptomics, proteomics and glycomics have been made, and the book therefore pays particular attention to these developments with the addition of brand-new chapters. Also covering the impact these parasites have had on the global human population, their distribution and their ecology, this book provides a comprehensive and accessible resource for scientists, researchers and students of medical and veterinary parasitology.

1 The Discovery of Fasciola hepatica and its Life Cycle

Stuart J. Andrews¹, Krystyna Cwiklinski² and John Pius Dalton^2*

¹Independent Consultant, Kent, UK; ²Molecular Parasitology Laboratory, Centre for One Health and Ryan Institute, National University of Ireland Galway, Republic of Ireland

1.1 Introduction

Fasciolosis is a parasitic disease of humans and their livestock caused by digenean trematodes of the genus Fasciola, referred to as liver flukes. The two species most commonly implicated as the aetiological agents of fasciolosis are F. hepatica and F. gigantica (subfamily Fasciolinae, family Fasciolidae). Fasciola species are located within the Digenea subclass of the class Trematoda, phylum Platyhelminthes.

The Digenea are characterized by a complex life cycle involving one or more intermediate hosts. Many variations on the life cycle exist, but each typically includes a molluscan primary or intermediate host in which larval asexual multiplication occurs, and a vertebrate final or definitive host in which sexual reproduction occurs. Members of the family Fasciolidae are hermaphroditic and self-fertilization can occur, although preferential cross-fertilization is usual.

Fasciolosis has the widest longitudinal, latitudinal and altitudinal distribution of any helminth disease; it is present on every continent excluding Antarctica (Mas-Coma et al., 2019). F. hepatica has a worldwide distribution but predominates in temperate zones, while F. gigantica is found on most continents but primarily in tropical regions, in particular Asia and Africa. However, where climatic conditions favour both parasites, they can coexist and hybridize. Recent animal trade has also influenced their distribution, especially in Asia and Africa (Mas-Coma et al., 2005, 2019). The two species are believed to have diverged 5 million years ago close to the Miocene–Pliocene boundary (Choi et al., 2020).

Fasciolosis is an economically important disease of domestic livestock, particularly cattle, sheep and water buffalo, and the cost of the disease to the global farming community is conservatively estimated at more than US$3 billion (Spithill et al., 1999; Beesley et al., 2018). The parasite also infects many wild animals, such as rabbits, hares, deer, coypu, rats, horses and camels, some of which can be regarded as important reservoir hosts. The potent immunomodulatory effects of Fasciola spp. on the host immune system may compromise the host’s ability to resist other microbial infections, such as tuberculosis, salmonella and clostridiosis (Claridge et al., 2012; Cwiklinski et al., 2016), adding further impairment to animal health, welfare and productivity.

Since the 1990s, fasciolosis has emerged as an important food-borne disease of humans and a major public health issue in a growing number of countries. Estimates of human infections are still very approximate and range from 2.4 to 17 million people (Mas-Coma et al., 2019), with 91–180 million people at risk of infection (Mas-Coma, 2005; Keiser and Utzinger, 2009). Countries where human infections are highest are Bolivia, Peru, Ecuador, Egypt, Iran, China, Vietnam and, less so, Portugal and Spain. Recently, the World Health Organization has classified fasciolosis as a ‘Neglected Tropical Disease’ (WHO, 2020).

The disease caused by F. hepatica and F. gigantica is known within the literature under various synonymous names, namely fasciolosis and fascioliasis. In keeping with the World Association for the Advancement of Veterinary Parasitology standardized nomenclature of parasitic diseases, the term fasciolosis will be used within this text (Kassai, 2006).

1.2 The Discovery of the Life Cycle

An overview of the historical discovery of the life cycle of F. hepatica is given below, together with the main biological factors relevant to the successful completion of the cycle. Further information and perspectives can be found in past literature, including Taylor (1937, 1964), Reinhard (1957), Jefferies and Dawes (1960), Pantelouris (1965), Dawes (1968), Smyth and Halton (1983), Andrews (1999) and Wilson (2020).

A list of the principal discoveries in the life cycle of Fasciola is shown in Table 1.1. The earliest description of fasciolosis in the literature is contained in a book entitled Black Book of Chirk, published circa 1200, in which reference is made to liver fluke in sheep (Froyd, 1969). Within this book, a reference is drawn from an earlier text that may describe fasciolosis in the Gwentian Code of Wales, describing the laws enacted by Howel the Good in the 10th century (Froyd, 1969).

Table 1.1. Milestones in the discovery of the life cycle of Fasciola hepatica.

Person/year	Milestone
De Brie, 1379	First to observe the liver fluke F. hepatica
Redi, 1688	Disproved the theory of spontaneous generation
Swammerdam, 1737	First to see cercariae dissected from a snail (see Swammerdam, 1758)
Müller, 1773	Observed cercariae swimming in water
Zeder, 1803	Described a miracidium hatching from fluke egg
Nitzsch, 1807	Observed cercariae encysting
Bojanus, 1818	Described redia and development of cercariae
Steenstrup, 1842	Published theory of alternation of generations (see Steenstrup, 1845)
La Valette St George, 1855	Observed infection of a snail by a miracidium
Wagener, 1857	Observed penetration of a snail by miracidium and subsequent development of redia
Weinland, 1875	Suggested that the larval stages of the liver fluke occur in Lymnaea truncatula
Leuckart, Thomas, 1882	Confirmed L. truncatula as intermediate host and worked out life cycle of F. hepatica
Lutz, 1892; Lutz, 1893	Confirmed that herbivorous animals acquire adult fluke by ingestion of metacercariae
Sinitsin, 1914	Confirmed route of migration of F. hepatica to the liver

The first observation of liver fluke was made by Jean de Brie in 1379. While he was preparing a treatise on wool production and sheep management for Charles V of France, de Brie made mention of the disease ‘liver rot’ in sheep, though he did not actually describe the appearance of the worm in this treatise (Huber, 1890). Unfortunately, the original account of his work has been lost and his observations are only known from various editions published between 1542 and 1594. Like many other early writers, de Brie did not associate the liver fluke with the disease ‘liver rot’, but thought that this was a consequence of the liver being affected by toxic substances produced by certain plants eaten by the sheep.

According to Cole (1944) another recognizable description of liver fluke appeared in a book entitled A newe Tracte or Treatyse moost profytable for all Husbandemen which was published in 1523 by Sir Anthony Fitzherbert. Twenty-six years later, in 1549, reference was made in a book entitled De lumbricis alvum occupantibus to an observation made by an Italian physician by the name of Fanensi Gabucinus who described worms resembling pumpkin seeds in the blood vessels of the liver of sheep and goats. Additional observations on liver fluke disease were recorded during the second half of the 16th century, namely those of Conrad Gesner (1551) and Cornel Gemma (1575). Nevertheless, it was still commonly thought at the time that the feeding of particular plants to sheep was responsible for the disease.

It was not until 1688 that this theory was challenged by Francesco Redi, after whom the redia stage in the digenetic life cycle was named. He was a physician in Italy, who, by showing that parasites lay eggs, destroyed the false doctrine of spontaneous generation, i.e. the hypothetical process by which living organisms arise from inanimate matter. It is uncertain in which parasite this observation was first made, as Redi described a number of different types of worms from many kinds of animals, but he was the first to publish a picture of the liver fluke – a sketch from a specimen removed from the liver of a castrated ram.

The rejection of the theory of spontaneous generation was a significant breakthrough and was to stimulate a new wave of research. Prominent in this new research was Govert Bidloo, a professor of anatomy at The Hague and physician to William III. Bidloo (1698) observed worms in the bile ducts of sheep, stags and calves and recalled having seen similar worms in the livers of humans. This followed the observation by John Faber in 1670, who was the first to state that the liver fluke lives in the bile ducts, not in the blood vessels (Reinhard, 1957). Bidloo also observed eggs inside the living worm and thought that sheep probably became infected by swallowing the worms or their eggs and that the worms got to the liver in the blood rather than by passing via the small intestine. His results were reported in the form of a memoir to Antony van Leeuwenhoek, which stimulated Leeuwenhoek to investigate further. Leeuwenhoek thought that the worms lived in water and that sheep became ill by drinking this water, but he could not explain why he was unable to find such creatures in water samples taken from ditches in fields near the city of Delft. His observations were recorded in letters sent to the Royal Society that were subsequently published in the Philosophical Transactions (Leeuwenhoek, 1700, 1704).

It was not until the end of the 18th century that reference was made in the scientific literature to the intermediate stages of the life cycle. It was a chance observation by a Dutchman named Johann Swammerdam (1758) who, while dissecting a snail (Paludina vivipara) in order to examine its internal structure, saw living things that he thought were not of snail origin. Examination of his illustrations of these ‘worms’ clearly shows them to be the cercariae of some trematode. Later, in 1755, Frank Nicholls, a physician and prominent anatomist in England, presented a report to the Royal Society in which he remarked that the bile ducts in the livers of bullocks infected with ‘liver rot’ were blocked by ‘a wall of stone’ arou...