Tuesday, August 7, 2012

Lung Flukes: Paragonimiasis


This week at Infection Landscapes we will cover the last of the trematodes included in the extended series on helminths. Paragonimiasis is caused by several species of the genus Paragonimus. Paragonimus westermani causes most human infections, and is commonly known as the lung fluke. Lung flukes are probably the most widely distributed trematodes in the world.

The Worm. Paragonimus westermani is a trematode helminth and, because it is responsible for most human infections, this species will be the focus of the current discussion:

Adult Paragonimus westermani

This helminth's life cycle requires 2 intermediate hosts and a definitive host, the latter of which includes many mammal species including humans.

Unembryonated ova are expunged in the sputum or feces of an infected definitive host, which may be a human or one of several mammal species. The ova embryonate in freshwater, thus after being expunged from the host they must come into contact with an appropriate water source in the environment. After approximately three weeks, the eggs hatch and the miracidia emerge, which are motile and subsequently seek their first intermediate host. Freshwater snails of the Melanoides, Semisulcospira, and Thiara genera are the most common first intermediate hosts, depending on the the local biogeography and ecology. After penetrating the snail, the miracidia migrate to the hepatopancreas where the develop first into sporocysts, then into rediae, and finally into cercariae. The cercariae then exit the snail returning to the aquatic environment. As with the other trematodes we have covered, these cercariae are motile but they are not swimmers. Instead the cercariae of P. westermani are crawlers and seek out their second intermediate hosts by crawling along the bed of their local body of water. Crustaceans serve as the second intermediate host, particularly freshwater crabs or crayfish. The cercariae penetrate their crustacean hosts and then encyst (usually in muscle tissue, but also under the shell), subsequently developing into metacercariae, which is the stage that is infectious to their definitive hosts. When raw or undercooked crabs or crayfish are eaten by humans (or other definitive hosts), viable metacercariae are ingested with the crustaceans. These metacercariae excyst in the small intestine, penetrate the epithelium of the gut, and enter the abdominal cavity where they develop into immature flukes. The immature flukes migrate up to and penetrate the diaphragm and enter the lungs. In the lungs the flukes complete their development, form adult pairs, and encapsulate in peripheral lung tissue. The mature adult pairs begin cross-fertilization and subsequent release of eggs into the lung tissue surrounding the trematode capsule. Approximately one months is required from the time of ingestion of the metacercariae to the time when adult flukes begin releasing eggs into host tissue. These eggs eventually reach the bronchioles and are coughed up with sputum, which may also contain blood. The eggs can contaminate water directly by the introduction of the sputum to the relevant water source, or they can be swallowed and passed in the feces of the host. The graphic below developed by the Centers for Disease Control and Prevention nicely depicts this life cycle:


The Snail. Species in the Melanoides, Semisulcospira, and Thiara genera are the preferred first intermediate host for Paragonimus spp. These are all freshwater snails that can exploit lentic and lotic aquatic environments, and some (Melanoides) are burrowers:

Melanoides tuberculata

These snails are widely distributed throughout the world. Melanoides tuberculata, in particular, is distributed as a native species across most of sub-Saharan Africa and many micro-environments of North Africa, and most countries of South, Southeast, and East Asia. The species has been introduced into the western hemisphere and is now also widely distributed across North, Central, and South American, and across many islands of the Caribbean.

The Crustacean. Where most human infections occur by consumption of undercooked crab meat (East Asia), species in the Eriocheir, Potamon, Potamiscus genera are important second intermediate hosts for Paragonimus spp. These are freshwater crabs that also are widely distributed and serve as food species for humans.

Eriocheir sinensis

Crayfish, which are crustaceans in the superfamilies Astacoidea and Parastacoidea, are also important second intermediate hosts for Paragonimus spp. As these crustaceans also serve as food items, these too can be important sources of transmission to humans.

 Austropotamobius pallipes

The Disease. The adult stage of P. westermani forms cysts in pulmonary tissue, which can breach the bronchioles.

Dog lung with many P. westermani cysts (From the Web Atlas of Medical Parasitology)

Light infections are often asymptomatic. However, symptomatic cough is not uncommon even in low volume infections. With higher volume infections, cough can become chronic with hemoptysis. Chest pain and difficulty breathing can also present, which are often more common following secondary bacterial infection and abscess development. With severe infections, particularly in the presence of frequent secondary bacterial infection, pneumothorax and pleural effusion are significant complications.

Arrows pointing to the position of Paragonimus flukes in lung tissue


The Epidemiology and the Landscape. Paragonimus spp. are the most widely distributed trematode helminths in the world. These flukes are endemic in a great diversity of reservoir hosts across South, Southeast, and East Asia, the Pacific Islands, North and sub-Saharan Africa, and North and South America. Definitive reservoir hosts include dogs and cats, pigs, leopards, tigers, foxes, wolves, opossums and minks. Lung flukes constitute an incredibly adapted helminth capable of exploiting a great diversity of ecologic niches across incredibly varied geography. There are approximately 22 million human infections worldwide, but most occur in East and Southeast Asia. In some communities in China, the prevalence of human infection approaches 20%. The map below, produced by the Imaging of Tropical Diseases, depicts the global distribution of human infection with P. westermani:


You can see in the map that most human cases are concentrated in South, Southeast, and East Asia, with additional clusters in the tropical and subtropical belts of Africa and Central and South America. Nevertheless, given the extremely wide geographic distribution of this and other Paragonimus species, these areas of endemicity do not define strict limits of occurrence.

The landscape epidemiology of lung flukes in general, and P. westermani in particular, shows that these trematodes require a second intermediate host, which transfers the infectious metacercariae passively (through consumption) to the definitive host. This means that the point of intersection between pathogen and host in the landscape derives from a complex and layered ecologic framework. Paragonimus trematodes require a nuanced and specific engagement of the definitive host with the aquatic environment, i.e. through the harvesting of food from the water. However, this landscape, as narrowly described so far, is not sufficient by itself for infection transmission to humans. For human transmission to occur, the physical landscape that defines the geography and structure of Paragonimus ecology must intersect the human social landscape. This is because human, or other animal reservoir, feces (or, less likely, sputum) must first contaminate the same water sources that humans then subsequently harvest for food. This happens primarily through 1) poor sanitation and water infrastructure, and 2) contamination of water sources by domestic or sylvan animals that serve as the natural reservoirs for this trematode. Regardless, even given the correct environmental circumstances for transmission to humans, eating the metacercariae-infested crustaceans need not transmit the infection to humans. It does so only because of the method of preparation of the crustaceansIn many places where P. westermani is endemic, raw crab or crawfish is a key ingredient in some local delicacies (e.g. drunken crab), so food preparation, as determined by cultural preference, becomes a key aspect of the social landscape that converges with the physical landscape to effect transmission.


Control and Prevention.

Snail Control

Early (and some ongoing) attempts at lung fluke elimination focused on gastropod control in various surface water sources. Typically, these control campaigns have involved the chemical treatment of freshwater sources to eliminate the local snail population, thus blocking the transmission of P. westermani at the first intermediate host. However, two important problems make gastropod control unrealistic in many settings. 

First, the chemical treatment of water sources can have much broader ecologic impact than what is intended by the public health initiative. Introducing toxic agents into surface water may kill the snails, but it can also harm other organisms in the aquatic ecosystem and result in unanticipated and detrimental ecologic effects. Some investigations have explored the possibility of introducing biologic mechanisms of control to supplant chemical treatment with more "natural" mechanisms. However, these approaches can also be dangerous if the natural biologic mechanisms involve the introduction of non-native invasive species into the aquatic environment.

Second, whether chemical or natural, snails in most areas prove robust to elimination. Both their high reproductive capacity and diffuse distribution within the aquatic system usually allow some members of the population to survive, which can then re-populate the local environment fairly quickly.

Food Preparation

Thorough cooking of all freshwater crustaceans is very important for blocking transmission of P. westermani to humans. Cooking kills the metacercariae and, thus, directly prevents infection in humans. Cooking is probably the most effective method of control and prevention of P. westermani infection. However, in many places where this helminth is endemic, certain local delicacies require raw crustaceans as central ingredients. As such, consistent cooking of crustaceans in each household becomes an individual choice that may be superseded by cultural dietary norms and preferences. 




3 comments:

  1. This is actually the first time that I heard about lung fluke, even though I had been living in Hong Kong, a southeastern city in Asia, before I came to America. The epidemiology of this disease is not complicated, but it is a great example to demonstrate how multiple factors, including our social environment, physical landscape, and the mode of transmission of a pathogen, intertwine to form a disease. As a result, there are usually multiple levels in any disease prevention. In this case, prevention strategies can focus on the 2 intermediate hosts, the environment (i.e., water), or the social infrastructures. I personally believe that snail control is not an ideal prevention method because we should not break the equilibrium of an ecosystem. On the other hand, advising people to cook crustaceans thoroughly is a feasible strategy, although people who have raw crustaceans as their daily ingredients may not follow. Cultural habits are difficult to modify, but if people realize that raw crustaceans can be dangerous to their health, then maybe they will accept the new idea. Assuring a reliable water infrastructure is probably the most important prevention method after all, but it will be a big challenge to poor or resource-lacking countries in Africa.

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    1. I am from South Asia as well (Bangladesh) and I have also never heard of these particular types of lung fluke worms either. Judging from the picture of the dog lung in this article however, I am quite glad I have not encountered this particular parasite either firsthand or secondhand. I agree with you completely about killing snails in order to prevent the spread of P. westermani. It seems a bit odd to kill off one species to try to get rid of a parasite. That would not only be impractical as the article mentions, but may also throw off the equilibrium of the ecosystem that it is a part of. It seems thoroughly cooking the sea food that we eat will go a long towards preventing human infections. It may not prevent the proliferation of P. westermani however, since it has so many other definitive hosts that can act as a reservoir.

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  2. If the ova embryonate must come into contact with fresh water, I wonder if one exit point (feces or sputum) has a higher chance of success. I’m also curious why many parasites prefer the liver as the first spot to invade. What about hepatocytes is attractive to parasites?
    It’s interesting that definitive reservoir hosts include dogs, cats, pigs, leopards, tigers, etc. If 22 million humans are infected worldwide, I’m curious how many total mammals are infected worldwide. Even if we were able to change food preparation methods to eliminate human infections, the parasite would still exist because of the abundance of other definitive reservoir hosts. It would then only be a matter of time before humans are infected again. From this logic, improving sanitation would also not work as you cannot prevent wild tigers or leopards from defecating near fresh water sources. It seems like this lung fluke is going to be with us for very long time.

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