While many associate the spread of rat lungworm disease with rodents, slugs and snails, new research from the University of Hawaii at Manoa offers an extensive list of other creatures that may transmit the parasite that causes the illness.

Think freshwater prawns, crabs, frogs, toads and centipedes, which are present in Hawaii.

Researchers from UH- Manoa and the University of London combed through nearly 140 scientific studies published between 1962 to 2022 and found 32 species that can act as carriers of the rat lungworm parasite.

Of these 32, at least 13 species, including prawns and shrimp, crabs, flatworms, fish, frogs, toads, lizards and centipedes have actually been associated with causing rat lungworm disease in humans.

The idea was to comb through information scattered throughout scientific literature for 40 years and pull it all together into a one-stop source on paratenic hosts, which can act as carrier hosts or transport hosts if they eat a snail or slug and become infected.

“It’s a list of all known paratenic hosts and then a list of those of that broader list that’s actually involved in human disease transmission,” said Robert Cowie, senior author and faculty member of UH-Manoa’s School of Ocean and Earth Science and Technology.

Rat lungworm disease, which is caused by a roundworm parasite called Angiostrongylus cantonensis, is a disease that affects the brain and spinal cord, according to the state Department of Health. Symptoms vary but include nausea, vomiting and abdominal pain in the first few hours to days after ingestion followed by headache and other neuralgic symptoms, as well as neck stiffness and pain.

People can get rat lungworm disease by eating raw or undercooked snails or slugs, or raw produce that contains a small, infected snail or slug or part of one.

While the majority of cases in the state have occurred on Hawaii island, according to DOH, they have occurred on other isles as well.

Last year, there were four confirmed cases of rat lungworm reported in residents statewide, including three on Hawaii island and one on Oahu, plus one in a visitor to Maui, according to DOH. So far this year, there has been only one reported case in a Hawaii island resident.

Cowie, who has been researching rat lungworm for 20 years, has been aware of these paratenic hosts for some time. Paratenic hosts present in Hawaii include flatworms, centipedes, coqui frogs and cane toads.

“While people in Hawaii are unlikely to eat these animals, it is not unknown for people to do so on a dare and become seriously ill,” he said in a news release. “Elsewhere, certain paratenic hosts are eaten for supposed health reasons — frogs in Taiwan and Japan, or to enhance virility — lizards in Thailand.”

The rat lungworm has a complex life cycle, according to Cowie, that naturally takes place in rats, snails and slugs in a pattern that goes round and round.

The “definitive” hosts are rats, in which the worms mature and reproduce. Infected rats can pass larvae of the worm in their feces, which is ingested by snails and slugs, which are “intermediate” hosts. The cycle continues as rats become infected upon eating an infected snail or slug.

Humans and pet dogs who become infected when they eat an infected snail or slug are “accidental” hosts who do not transmit infection to others. Infections in humans can lead to serious illness and occasional death.

“But people can also get infected if they eat so-called paratenic hosts, which are also known as carrier hosts,” said Cowie. “These are animals that become infected by eating infected snails or slugs, but in which the worms cannot develop to maturity as they do in a rat. However, in such hosts the worms become dormant but still capable of causing infection. And if one of these hosts, or part of one, is then eaten raw by a person — an accidental host — development can continue, but only up to a point.”

Rat lungworm development happens in the person’s brain, Cowie said, where they are moving around, feeding and growing, but then the worms die without completing their life cycle.

The symptoms of rat lungworm disease are primarily caused by damage to the brain and the massive inflammation that results when the worms die.

Some of the most frequently mentioned paratenic hosts of rat lungworm are freshwater prawns, known scavengers of snails and slugs, according to the study.

Rat lungworm larvae were first recovered in 1962 from prawns in Tahiti, which are believed to be the main source of local human infection, according to a study in the Canadian Journal of Zoology.

A popular food in Tahiti, taioro, consists of grated coconut and prawn juice, the study noted, while freshwater prawns are commonly eaten raw by Tahitians and some local Europeans.

However, in Hawaii, prawns collected from the wild and grown domestically at farms tested negative for rat lungworm.

Another study on Hawaii island detected infective larvae in 21 out of 24 coqui frogs, the invasive frogs that have also been detected on Oahu.

Preventing infection includes awareness of which species may harbor the parasite, according to Cowie, who said they should not be consumed raw.

Also, people should continue to wash all fruits and vegetables well under running water and inspect them for slugs and snails — and possible other hosts such as flatworms — to avoid inadvertently eating them or parts of them. Baby flatworms could easily be hidden among lettuce leaves, he said.

“It is important to know not only that snails and slugs can transmit rat lungworm parasites to humans but also which other animals — which paratenic hosts — can also do so,” said Cowie. “The goal of the study was to pull all the information on paratenic hosts and their role in transmission of rat lungworm disease, previously scattered in diverse publications and obscure reports, together into one place and develop a global understanding of their diversity and role in disease transmission.”

Helena Turck, University of London graduate student, was the first author of the study, which she did remotely as her master’s degree thesis research under supervision from Cowie. Professor Mark Fox of the Royal Veterinary College also collaborated on the study.