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Food-Borne Trematodes: Liver, Lung, and Intestinal Flukes
Abstract
Food-borne trematodes (FBTs) are a group of liver, lung, and intestinal flukes that typically infect humans through the ingestion of freshwater fish, crustaceans, and plants contaminated by encysted forms of the parasites. FBTs are prevalent throughout the world, with countries in Asia bearing the highest burden of infection. Transmission of FBTs is fostered by local culinary practices of consuming raw or undercooked fish and aquatic plants, the presence of freshwater snails that serve as intermediate hosts in the parasite life cycle, and contamination of surface water by untreated fecal waste from infected humans and mammalian reservoir hosts. In addition to occurring in residents of endemic regions, FBTs may also be found in those living in nonendemic areas who immigrated from countries where FBTs are prevalent, among international travelers who consume foods containing encysted larvae, or in those exposed to contaminated food imported from endemic regions. Acute fluke infections can manifest with gastrointestinal or pulmonary symptoms and eosinophilia, while chronic infections may be relatively asymptomatic. Two liver flukes are strongly associated with cholangiocarcinoma, a bile duct cancer. This chapter focuses on the FBTs of greatest medical importance: the liver flukes Clonorchis sinensis , Opisthorchis viverrini , Fasciola hepatica and Fasciola gigantica , the lung fluke Paragonimus spp., and the intestinal fluke Fasciolopsis buski .
Clinical Vignette
A 66-year-old woman with a history of chronic hepatitis B presented with intermittent epigastric and right upper quadrant pain that started several weeks after a trip to Vietnam to visit relatives. She denied fevers but reported anorexia and was noted to have lost 15 pounds. Physical examination revealed mild epigastric and right upper quadrant tenderness but no hepatomegaly. Laboratory evaluation was notable for leukocytosis (white blood cell count 20,200/μL) with 45% eosinophilia (absolute eosinophil count of 9090). Her aspartate aminotransferase and gamma glutamyl transferase levels were elevated, but the rest of her liver tests were normal. Stool examination was negative for ova and parasites. Right upper quadrant ultrasound revealed multiple ill-defined lesions in the liver. Magnetic resonance imaging of the abdomen found several areas of T2 hyperintensity with T1 hypointensity in the right lobe of the liver, diffuse gallbladder wall thickening, pericholecystic fluid, and no evidence of biliary ductal dilatation. Biopsy of a liver lesion demonstrated microabscesses, eosinophils, and Charcot-Leyden crystals. Serology for Fasciola hepatica performed at the Centers for Disease Control and Prevention was positive. She received triclabendazole 10 mg/kg as a single dose and her symptoms resolved within 2 weeks of treatment. Her eosinophilia resolved several weeks later, and a follow-up liver ultrasound 8 months after treatment was normal.
Geographic Distribution
According to the World Health Organization (WHO), more than 56 million people worldwide are infected with FBTs and approximately 750 million people are at risk of infection. The actual burden of disease is higher because of underdiagnosis and underreporting, and FBTs have been considered among the most neglected of the world’s neglected tropical diseases (NTDs). FBTs have a global distribution but the greatest burden of disease occurs in Asia, with an estimated 12 million people infected with Clonorchis sinensis in China and 8 million with Opisthorchis viverrini in Thailand. F. hepatica is present in six continents while Fasciola gigantica is found predominantly in Asia and Africa. Multiple Paragonimus species are found throughout Asia, Africa, and the Americas (e.g., Paragonimus kellicotti is endemic in the Mississippi River basin of the United States). FBTs are transmitted mostly in rural agricultural communities, but their global dispersal is broadening due to the growth of aquaculture, increased globalization of the world’s food supply, and increased human migration.
Life Cycle
Humans and animals become infected with FBTs when they ingest raw or undercooked freshwater fish, crustaceans, or plants that are contaminated with the encysted metacercariae of the flukes. Fasciola infections may also be transmitted through contaminated water. Humans serve as definitive hosts of FBTs, meaning that the parasites become sexually mature adults within the body of the human host. Adult liver and intestinal flukes produce ova (eggs) that exit the body in feces, while the ova of lung flukes may be expectorated in the sputum or swallowed and then excreted in the stools.
The life cycle of the intestinal fluke Heterophyes , a fish-borne trematode, is shown in Fig. 82.1 and serves as a model for understanding the life cycle of other fish-borne flukes such as C. sinensis , O. viverrini , and Metagonimus yokogawai . After contamination of freshwater environments by feces from infected mammalian hosts, Heterophyes eggs are ingested by suitable snail hosts (the first intermediate host) and hatch, with the emergence of parasite forms called miracidia . After going through further developmental stages in the snail gut, free-swimming parasite forms called cercariae are released by the snails into the water. The cercariae attach to and penetrate fish (the second intermediate host), transforming into encysted metacercariae in the flesh of the fish. The metacercariae are the infectious stage for mammalian hosts, and after infected fish are eaten by humans or other mammals, the Heterophyes metacercariae excyst and develop into adults in the small intestine, where they mature to become adult flukes.
After ingestion of fish containing encysted metacercariae of the liver flukes C. sinensis and O. viverrini , the parasites excyst and the larvae migrate through the duodenum, the ampulla of Vater, and the extrahepatic bile ducts, eventually reaching the intrahepatic bile ducts, where they mature into adults. Adult Clonorchis and Opisthorchis flukes can survive in the human host for more than 20 years.
In the life cycle of the liver flukes F. hepatica and F. gigantica , cercariae shed by snails attach to freshwater plants (e.g., watercress) and become encysted metacercariae. After ingestion, Fasciola larvae excyst in the duodenum, enter the intestinal wall to reach the peritoneal cavity, penetrate Glisson’s capsule, migrate through the liver parenchyma, and ultimately reach the bile ducts where the flukes mature and live for years.
In F. buski infections, the larvae excyst and then attach to the walls of the duodenum and jejunum, where they remain firmly attached as they develop into adults. Compared with other FBTs, F. buski has a relatively short lifespan (1 year) but adults can produce more than 20,000 eggs per day.
Freshwater crabs and crayfish serve as the second intermediate host of the lung fluke Paragonimus . After ingestion, metacercariae excyst in the small intestine and the larvae penetrate the intestinal wall, migrate through the peritoneal cavity, pass through the diaphragm into the pleural space, and then migrate into the lung parenchyma where the parasites mature into adults and produce eggs. The eggs are then expectorated in the sputum or swallowed and passed in the stool. Ectopic Paragonimus infections can result in the migration of the parasite into the brain or subcutaneous tissue.
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