Angiostrongylus vasorum - Canine Lungworm Larvae in Snails, Slugs, and Slime

Is this the face of a killer? This slug, Arion rufus, has
been shown to carry Angiostrongylus vasorum larvae.
Image by Guillaume Brocker; CC BY-SA 3.0.

The roundworm Angiostrongylus vasorum goes by many common names: canine lungworm, canine heartworm, French heartworm – all descriptive labels acknowledging the fact that the adult worms reside in the heart and pulmonary artery (the blood vessel that carries blood from the heart to the lungs) of domestic dogs and wild canine species.

Life Cycle of Angiostrongylus vasorum

The life cycle of A. vasorum is complex:

• Adult worms produce eggs that are carried to the lungs by the blood circulation.
• The eggs hatch in the lungs, releasing larvae, which break through into the air space of the lungs, travel up the airways to the throat and are swallowed.
• Passing through the intestine, larvae are deposited in the environment with feces.
• Slugs and snails feeding on dog feces either ingest the larvae or the larvae penetrate the mollusk’s foot and undergo further development in the mollusk’s tissues.
• Infective larvae are released in the slime secretions left behind by snails and slugs, or are ingested with the mollusk when it is eaten by something (frogs, dogs, etc.)
• It is thought that dogs swallow the larvae and become infected when they eat snails and slugs, when they eat frogs or other animals that have eaten infected snails and slugs, or when they eat or lick things that are contaminated by slug or snail slime.
• Larvae migrate to lymph nodes, where they develop further, and then move to the heart and pulmonary artery.

Dogs Eat Snails and Slugs

Dogs eat slugs and snails, and frogs. While many dog owners will readily agree with this statement, it leaves others, like me, scratching our heads.

Would my dog eat a slug or snail? She has never shown the slightest interest in doing so (and there are lots where we live).

Would she eat a frog? Sniff it maybe. Play with it maybe. Step on it by accident; yes, I’ve seen this. Eat it? No.

Would she eat a food item left lying on the ground and possibly crawled over by slugs and snails (or with slugs and snails still on its surface)? Definitely.

And that is one of the reasons why I was particularly interested in this video of the movements of snails in a British garden at night.


I had no idea they traveled so far and so fast.

Risk of Angiostrongylus vasorum Infection

A lot is still unclear about A. vasorum.  We don’t know what the most common route of infection is: snails, slugs, slime, frogs etc. We don’t know how many dogs have the parasite but exhibit no symptoms. We don’t know how many larvae a dog would need to ingest to become ill.

And of course, different species of slugs and snails are likely to differ in the distance they travel and the number of larvae they leave in their wake. Clearly, however, wherever A. vasorum occurs, all dog owners should take the threat seriously. As Eric Morgan et al write, the infection “is associated with coughing, dyspnoea [shortness of breath], exercise intolerance, weight loss, vomiting, abdominal pain, lumbar pain, neurological signs, heart failure, bleeding diathesis [tendency to bleed], and sudden death.”

Sources

 

Barcante, Thales Augusto, et al. "Angiostrongylus vasorum (Baillet, 1866) Kamensky, 1905: emergence of third-stage larvae from infected Biomphalaria glabrata snails." Parasitology Research 91.6 (2003): 471-475.

Fletcher, Damien. "Snails Can Travel at One Metre an Hour and Piggy-back on Others' Slime to Save Energy." Mirror News. Aug 23, 2013.

Morgan, Eric R., et al. "Angiostrongylus vasorum: a real heartbreaker." Trends in Parasitology 21.2 (2005): 49-51.

Bed Bugs in New Products, Retail Stores, Imported Goods

In his Aug 22, 2013 blog post for the Huffington Post, Andrew Rennie describes a bed bug encounter. “Plainly visible on our brand-new sheet set, purchased at a big-box retail chain,” he writes, “was a bed bug. Dead, thank God, but its tiny, contorted legs twisting skyward still filled me with… dread” ("Parasites and Profiteering," Huffpost Living). 

Yes, that would fill me with dread as well. Suddenly we’ve gone from “don’t buy (or otherwise salvage) used furniture” to “nothing is safe.” Even brand new products, apparently, straight from the store, can be infested with bed bugs. 

At its actual size – about 5 millimeters long – this female bed bug would resemble other insect species to the untrained eye. Image by Gilles San Martin from Namur, Belgium. CC BY-SA 2.0

Where Bed Bugs Come From

Rennie’s post was not about bed bugs: it was about lousy customer service, and on that topic I agree with him one hundred percent. By the time I finished reading, however, I was more focused on the whole bed-bug-in-the-new-sheets thing. How ironic – that an adult bed bug would be found neatly packaged in sheets that had never seen a bed! Sort of like getting a free sample of dishwasher detergent with your new dishwasher... only, not.

I wonder, was that bug identified as a bed bug by someone who really knows their bugs? An awful lot of insects look superficially like a bed bug (and if those sheets were imported, we’re not just talking North American insects). If the bug had turned up in a box of cereal, would it have been a weevil? Or a grain beetle of some kind? If it had arrived in a flower pot from the local garden center, would Rennie have given it a second glance? What's the probability that new sheets are now coming complete with a bed bug infestation?

It’s not impossible that Rennie’s nemesis was a bed bug. Bed bugs certainly can travel in shipments from other countries. Bed bugs have been found in retail stores. They could be present in a sheet factory, sure, but unless the employees of that factory are sleeping there too, you wouldn’t expect that to be a very happy home for a bed bug – lots of places to hide when the lights are on, granted, but not much to feed on in the dark.

Bed Bugs in Retail Stores and Products

Bed bugs can’t recognize new sheets as pay dirt and plan ahead. They don’t know an unused sheet from a windsock, a pillow from a bag of marshmallows. It’s us they recognize, not items we have never used. A dead bug in a package of new sheets is no more likely to be a bed bug than one in a package of computer paper.

The University of Minnesota tells us where bed bugs are most likely to be found in a clothing store (unsurprisingly, they don’t specifically mention the linen department of a big-box store). High-risk locations include fitting rooms, returns areas, seating areas, cloth bags attached to shopping carts etc. These locations have something in common: they are exposed to the (used) clothing and belongings of numerous people who could potentially bring bed bugs into the store ("Let’s Beat the Bed Bug," 2012).

As David Emery points out in Urban Legends: “Email: Bedbug Infestations Due to Imported Clothing,” imported products have not been associated with bed bug infestations in retail stores (About.com, 2010). Similarly, unused manufactured products are unlikely to introduce bed bugs into our homes. 

Is it a Bed Bug? Be Sure

Anyone who suspects they have found a bed bug should have it properly identified before spending time and money on a problem that may not exist. I suspect Rennie’s “bed bug” was an innocent look-alike, left with “its tiny, contorted legs twisting skyward” when it got caught up in whatever process folds new sheets and jams them into plastic packaging.

Manure and Latrines = Farming and Parasites

Pig sties are notoriously smelly places, but aged
pig manure makes excellent fertilizer.
 Image by MontagZen; CC BY-SA 3.0.

Almost twenty years ago, Jared Diamond wrote about the domestication of plants in Discover  ("How to Tame a Wild Plant," Sept 1994). "Human latrines," he wrote, "may have been a testing ground for the first crop breeders."

How so? Many plants get spread around when their seeds are eaten, passed through the digestive tract of the forager intact, and deposited in feces. Because humans tend to use latrines - designated outdoor toilets that they return to again and again - the seeds of the plants that early humans liked to eat got deposited in a concentrated area, and the wastes deposited with them provided fertilizer. Voila! Latrines would have effectively selected the choicest food items of early humans and aided their reproduction.

Because I'm interested in parasites, I couldn't help thinking that this very process also aided the transmission of intestinal parasites: choice food plants growing in areas used as latrines means people gathering food there, with resulting exposure to the eggs and larvae of intestinal worms (and probably protozoa as well).

"Our ancestors' garbage dumps," Diamond pointed out, "undoubtedly joined their latrines to form the first agricultural research laboratories." This, because larger seeds, roots and other plant parts that might reproduce would end up in the midden, or garbage dump, along with all the other food waste (think compost) and animal manure (if they had livestock), gaining a survival advantage in virtually the same way.

And now, in his article "Early Farmers and Manure: Stone Age Europeans Were More Advanced Than We Thought," (Decoded Past, July 3013) Frank Beswick reports on evidence that stone age people used animal manure as fertilizer as long ago as 6000BC. Beswick wonders "is it possible that the use of manure was a precondition of the development of agriculture?"

And I wonder how much it contributed to the parasites we share with domestic animals, particularly cattle and pigs.

The Candiru vs Peer Review

This is reportedly a candiru.
       It's a big one.
Image by em_j_bishop: CC BY 2.0

I think sometimes our faith in a system, and our love of a colourful story, deadens our common sense. Take the candiru, for example – Vandellia spp., the vampire catfish.

“This little charmer normally lives inside the gills of other fish to suck their blood, but is attracted to urine and reputedly able to wriggle up human's urinary tracts, where it lodges itself with sharp spines and can only be removed by surgery.”

Hogwash.


The quote above came from the 2002 Lonely Planet guide to Brazil (pg. 75). First of all, these little catfish do not live in the gills of their fish hosts. They visit there to feed for all of about two minutes – more like a mosquito, really, than a parasite.

There is no scientific proof that they are attracted to urine. If one ever wriggled up a human urethra it wouldn't lodge itself so much as become stuck as a result of those spines, designed for a different situation entirely. Finally, there is only one published case – semi-documented and unconfirmed – and it was reportedly resolved by cystoscopy rather than surgery. (Samad, Anoar. "Candiru Inside Urethral." Urology Clinic.)

The Candiru in Academic Literature

While we'd like to expect better of Lonely Planet, it's only fair to excuse this case of bad information – the candiru has been reported widely and legitimized in publications that normally hold themselves to an even higher standard. For example:

• From The New Encyclopedia Britannica 15^th ed. Vol 2. (1990): “... parasitizes man and has been known to enter the urethras of bathers and swimming animals. Once inside the passage, it erects the short spines on its gill covers and may thereby cause inflammation, hemorrhage and even death...” (“Candiru”).

• From a 1991 article by J. L. Breault in the Journal of Wilderness Medicine (2): “Forced extraction may cause lacerations of the urethral mucus membranes, which has caused death by exsanguination. Remedies have ranged from penile amputation and suprapubic cystostomy to application of a native herb that softens the spines” (“Candiru: Amazonian Parasitic Catfish”).

Judging by these sources and others published by academic presses and peer reviewed journals, subject as they are to editorial scrutiny, peer review, and fact checking, one would think that the consequences of a personal encounter with the candiru were well documented medical knowledge.

The library website at the University of Victoria says “Peer review ensures that an article-and therefore the journal and the scholarship of the discipline as a whole-maintains a high standard of quality, accuracy, and academic integrity. When you consult peer-reviewed sources, you are tapping into a wealth of established, verified knowledge” ( library.uvic.ca, accessed July 1, 2013).

A 2013 Review of the Evidence for Candiru Attacks

Nonetheless, Dr. Irmgard Bauer, in her 2013 investigation of two centuries of literature describing the candiru, found little in the way of verification. “...most reports are...repeated again and again,” she writes, “based on the same stories already described elsewhere... After careful distillation, very little [evidence] remains and of that little, even accounts sounding like first-hand descriptions become suspect.” (“Candiru – A Little Fish With Bad Habits: Need Travel Health Professionals Worry? A Review.” Journal of Travel Medicine; 20:2.)

What happened here? In 200 years, did no one go to the trouble to verify candiru reports until now? The candiru is like the Sasquatch's rich city cousin: in contrast to the Sasquatch, consistently disinherited by science because there is no evidence for it, the candiru has been repeatedly legitimized by science and reputable publishers despite the lack of evidence. All we really have for sure is a translucent little fish that takes a blood meal from a fish larger than itself, and a bunch of anecdotes. It really isn't even a parasite.

And we wonder why it's important to consult original sources?

I wrote about what we know about the Candiru for Decoded Science: "Candiru- A "Don't Pee in the Water" Horror Story Debunked."

Parasites and Networks - Food Webs, Epidemiology

When we think about how parasites fit into nature - their close interaction with their hosts, their reliance on specific hosts in a specific sequence, their ubiquitous presence in the environment - a network (or web) context makes sense. Recently, two articles  have come to my attention; they represent parasites in webs in similar ways but for different reasons.

Parasites Affect Food Webs

This food web for a mosquito would be much
more complex - and of much more relevance
to humans - if it included parasites.
Illustration by Tyler Rubley. CC BY-SA 3.0

 

 

The first is "Parasites Affect Food Web Structure Primarily Through Increased Diversity and Complexity." by J. Dunne and co-authors (PLoS Biol 11(6): e1001579), published on June 11, 2013. These researchers added parasites to aquatic food webs and asked whether the changes that resulted (a much more complex food web) could have been caused by the addition of any large group of organisms, or whether food web structure was altered by parasites in unique ways.

Beyond the central findings of that study, the article raised (or re-raised) a question for me: if we know that parasites are an important component of an ecosystem, if we know that they affect food webs in both generic and unique ways, why do they never appear on endangered species lists? For every endangered species, there should be a list of parasites that depend on that host species for survival. And why do conservationists routinely rid endangered animals in captivity of their parasites, knowing that if that species ever returns to the wild, it will do so without its specialist parasites, potentially to its detriment?

Parasites Predict Disease

 

The other paper is "Centrality in Primate–parasite Networks Reveals the Potential for the Transmission of Emerging Infectious Diseases to Humans" by José María Gómez and co-authors , published in PNAS (110:19 2013).  Like the paper by Dunne et al, this research builds a food web, but this web has parasites as the main consumers - a network of nonhuman primates that share parasites (or that are consumed by the same parasites, to look at it from the parasites' viewpoint).

The point is to examine whether this web can predict where diseases of primates are likely to jump to humans. The authors "found that primate species having higher values of centrality in the primate–parasite network harbored more parasites identified as EIDs [emerging infectious diseases] in humans and had parasite communities more similar to those found in humans." These species, then, are more likely to be the source of emerging infectious diseases in humans. Another good reason to include parasites in food webs.

Food webs tell us where parasites fit, and I think that is something we really need to understand, for our own sake and for theirs.

Disseminated Strongyloidiasis - Interesting Things to Note

A recent case of disseminated strongyloidiasis, reported by the New England Journal of Medicine highlighted a couple of intriguing features of this catastrophic disease: in the absence of an effective immune response, worms can mature in the lungs as well as the intestine, and, there's something special about corticosteroid drugs that makes an unfortunate success of the worm.

Adult Strongyloides stercoralis in the Lungs

The case report of disseminated strongyloidiasis by Schroeder and Banaei describes adult worms, both rhabditiform and filarifom larvae, and ova containing active larvae in a tracheal aspirate. A similar case is reported by Bava et al. Typically, you'd find only filariform larvae in the lungs, and adults are almost never seen, even in the stool, because the adult females spend their time migrating through the tissues of the intestinal lining (and there are no parasitic males).

A larva of Strongyloides stercoralis. At a later stage, this larva would
be capable of penetrating and migrating through tissues like skin, or the
lining of the intestine. Image: CDC

I assumed that the adults found in this case had actually matured in the lungs rather than migrating there from the intestine. A 2004 paper in Clinical Microbiology Reviews agrees. Keiser and Nutman write “...findings suggest that filariform larvae develop into adults in the lungs... This hypothesis is supported by... autopsy studies showing adult worms in lung tissue.” In this scenario, the parasite could be multiplying very rapidly with new worms originating not only in the intestine, but in the lungs as well. One can only imagine the numbers of parasites that could be present within a short period of time.

Corticosteroids and Strongyloides stercoralis

We know that corticosteroids can initiate disseminated strongyloidiasis. But do they just give the worms a green light by suppressing immune response, or do they actually favor the parasite? Corticosteroids prevent production of eosinophils and cause the rapid destruction of eosinophils that already exist; these cells are part of the body's immune response to parasites. But it's thought that corticosteroids actually contribute to the success of S. stercoralis in another way. Gary Simon writes in Medical Parasitology that “they may stimulate female worms to increase larval output and promote molting of rhabditiform larvae into the invasive filariform larvae.”

Eosinophils in the blood are part of the
immune response to parasites. Image by
Iceclanl. (cropped)  CC BY-SA 3.0

So it looks like giving corticosteroids to a patient with S. stercoralis expands the “territory” in which the parasite can reproduce, hobbles the immune system's attempts to control it, and boosts the worms' fecundity and maturation. Given all of this, it's easy to see why it might be difficult to save a patient suffering from disseminated strongyloidiasis, unless the problem is discovered quickly. It also sheds some light on why other types of immunosuppression are relatively less catastrophic.

 

Sources

Bava  BAJ, Cecilia D et al. “Adult Female of Strongyloides stercoralis in Respiratory Secretions.”, Asian Pacific Journal of Tropical Biomedicine 3:4, April 2013, Pages 311–313

Keiser PB, and Nutman TB. “Strongyloides stercoralis in the Immunocompromised Population.” Clinical Microbiology Reviews. 17:1, January 2004, 208–217.doi:10.1128/CMR.17.1.208-217.2004

Castelletto ML, Massey HC Jr et al. "Morphogenesis of Strongyloides stercoralis Infective Larvae Requires the DAF-16 Ortholog FKTF-1." , PLoS Pathogens 5(4): e1000370. doi:10.1371/journal.ppat.1000370

Schroeder L, and Banaei N. “Strongyloides stercoralis Embryonated Ova in the Lung.” New England Journal of Medicine: March 21, 2013; 368:e15 http://www.nejm.org/doi/full/10.1056/NEJMicm1204579

Simon, G. “Strongyloidiasis.” In: Medical Parasitology. Satoskar AR et al eds. Austin: Landes Bioscience; 2009, pg 31

Beauveria bassiana - A Fungus That Kills Bed Bugs

Beauveria bassiana is a fungus that is well known for killing insects. Spores of B. bassiana adhere to the cuticle (the outer protective covering) of the insect, begin to grow, and work their way through to the inner tissues. There the fungal growth continues, taking nutrients from the host's body until the insect dies. Because B. bassiana is lethal to many insects, including their larvae, it has been grown and distributed commercially for use in agricultural control of insect pests. It makes sense to wonder whether it could be used to control bed bugs as well.

Beauveria bassiana is grown for control of agricultural
pest insects. Image courtesy of Keith Weller.

Beauveria bassiana Kills Bed Bugs

A study by Alexis Barbarin et al tested B. bassiana against bed bugs, and the results indicate that the fungus is lethal to the pests: not only does it kill virtually all bugs that come in contact with it, infected bugs can carry it back to daytime hiding places and pass it on to other bugs that have not been otherwise exposed. Barbarin el al propose that B. bassiana might rid a bed bug infested building of its bugs.

Bed Bug Traps Using Beauveria bassiana

In their study, Barbarin et al exposed bed bugs to a mixture of oil and fungal spores on various surfaces, and found that jersey knit cotton transmitted the infection most effectively. Though further research is required, they propose that a fabric bed skirt impregnated with B. bassiana spores might be an efficient means of infecting a resident bedbug population. Presumably any trap designed so that all bedbugs climbing onto or leaving the bed would have to pass through it could be used to infect them with the fungus.

Is Beauveria bassiana Safe for Humans?

Beauveria bassiana is generally regarded as safe for humans and it's already being used for insect control applications all over the world without dire consequences for human health. This fungus is already naturally occurring in the environment. However, there's reason to be cautious with this approach. A study that tested fungi isolated from poultry barns found that B. bassiana has several virulence factors that potentially “increase [its] survival, growth, and propagation... in animal tissue.” Authors Taira el al comment, quite correctly, that otherwise harmless fungi can cause serious infections in people whose immune systems are already compromised. Such people include AIDS patients and organ donor recipients among others.

These grasshoppers were killed by Beauveria bassiana.
Fungal growth is visible on the insects' remains.
Image courtesy of Stefan Jaronski.

Cases of both deep tissue infection and skin infection caused by B. bassiana have been reported in the medical literature (Figueira et al). The possibility of skin infection, in particular, prompts second thoughts. Beauvaria bassiana does not wipe out bed bugs on contact: it takes time for the infection to kill. Therefore, bugs that have contacted the fungus will still visit the sleeping host to feed. And while feeding, they will create a break in the skin, often with severe irritation resulting, and possibly introduce fungal spores. This does not seem like a good plan.

Beyond the possibility of skin infection arising from contact with the bugs, a spore impregnated bed skirt would presumably contaminate a living space with fungal spores pretty thoroughly, and fungal spores are as hardy and as hard to eliminate as bed bugs are. Under the right conditions, they could remain viable for a very long time, possibly protecting against reinfestation by bed bugs, but also a potential hazard for the immunocompromised occupant of, or visitor to, the space.

Sources

Barbarin AM, Jenkins NE et al. “A Preliminary Evaluation of the Potential of Beauveria bassiana for Bed Bug Control.” Journal of Invertebrate Pathology 111 (2012) 82–85

Figueira L, Pinheiro D et al. “Beauveria bassiana Keratitis in Bullous Keratopathy: Antifungal Sensitivity Testing and Management.” European Journal of Ophthalmology 22:5 (2012) 814-818

Taira CL, Marcondes NR et al. “Virulence Potential of Filamentous Fungi Isolated From Poultry Barns in Cascavel, Paraná, Brazil.” Brazilian Journal of Pharmaceutical Sciences 47:1 Jan./Mar. 2011