A Fluke, a Tapeworm, and a Roundworm Walk into a Sushi Bar...

I know what you are thinking. You are thinking, "I can't read this blogpost because I LOVE sushi and she WILL NOT ruin it for me!" Don't worry, I'm a big fan of sushi too, and I certainly don't want to diminish the amazingness that is this Japanese delicacy. Let me start off by saying that most of the time, especially here in the U.S. or in countries with well-regulated sushi bars (such as is the case in Japan), you are not at risk for contracting parasites from eating sushi. I'll end this post with a brief discussion about raw fish regulations just to ease your troubled mind. That being said, let's talk about the parasites that you can get from eating raw fish that hasn't been properly processed.

There are many different species of parasites that use fish as one of their hosts. Any of these parasites has the potential to infect humans if accidentally eaten. You can pick up a variety of flukes, tapeworms, and roundworms from a variety of marine and freshwater fish. To keep this blogpost to a reasonable size, we will only look at one representative from each of these three groups. We will talk about the fluke Clonorchis sinensis, the tapeworm Diphyllobothrium latum, and the roundworm Anisakis simplex.

Because we are looking at three different worms under the theme of "can be in sushi", I won't go into the detail that I normally do. I've never blogged about C. sinensis or about A. simplex, but you can find a previous blogpost about D. latum here. (Perhaps I'll blog about the other two in later posts.)

Clonorchis specimens from a patient.

These three parasites not only represent three different classes of organisms (and two different phyla if you are keeping up taxanomically), they also represent parasites found in different types of fish. C. sinensis is typically found in freshwater fish or in fish that prefer brackish waters (a mix between freshwater and marine ecosystems). This parasite is really only found in East Asia, where it utilizes a snail for its first intermediate host and a fish as its second intermediate host. The parasite has been known to be problematic in regions that import fish from East Asia in addition to popping up in local populations where it is endemic. It is also interesting to note that this parasite has been identified in mummies and coprolites from Korea. This tells us that humans have a long history of association with this particular parasite.

The fish tapeworm, D. latum, also boasts a long association with humans. Coprolites from both North America and from South America have tested positive for this parasite. Some of the earliest New World human populations were infected with fish tapeworms, which makes sense given their proximity to water sources and diets that often integrated fish. A diet that included fish is evidenced by the existence of bones and scales in macroscopic remains from coprolites as well as in artifacts constructed from fish bones. This parasite infects freshwater fish, such as trout, and can be found just about anywhere in the world. It is often diagnosed in campers/fishermen who do not properly cook their catches and in sweet little old Jewish ladies who taste test tainted gefilte fish before the dish is fully cooked.

Anisakis worms embedded in a herring.

The last of the three, A. simplex, is by far the most notorious. This roundworm is cosmopolitan in nature, like D. latum, but prefers for its hosts to be marine fish as opposed to freshwater fish. It is most often associated with mackerel and herring, which has earned it the common name of "herring worm". Apparently it can infect many other marine fish and even things like squid. It has been contracted from dishes around the world including sushi/sashimi, cod livers, fermented herring, and ceviche. Though a person can experience mild to moderate abdominal pain after contracting one of the other two parasites mentioned here, a person contracting A. simplex will experience much more violent abdominal pains. These pains are sudden and severe by comparison because these worms actually die when they fail at their attempts to burrow into your intestines.  This often instigates an IgE-mediated immune response (i.e. an allergic reaction, sometimes even anaphylaxis), making this parasite by far the most dangerous of the three discussed in this blogpost.

Ceviche

There are a great variety of symptoms to look out for if you think you may have picked up one of these parasites. Because they affect the digestive system, you may experience things like abdominal pain, vomiting, nausea, loss of appetite, and diarrhea. The first of the three parasites, C. sinensis, primarily affects the liver and may lead to hepatomegaly (enlarged liver) and jaundice. The fish tapeworm, D. latum, can cause irritability or muscle weakness in addition to numbing or tingling of the skin. It may also manifest as an elevated heart rate. The most prominent symptom for an A. simplex infection is the sudden and severe abdominal pain. As the parasites die, they can also cause anaphylactic shock or they can leave behind intestinal granulomas, which many times mimic the symptoms of people with Crohn's disease.

Now that I have you thoroughly terrified, let's talk about how much effort we go through to prevent ourselves from being infected. In the U.S. (and probably many other places), we have regulations pertaining to the serving of raw fish. Raw fish, no matter where it comes from, must be processed to make sure that parasites are killed. This is done by freezing and/or treating with salt and/or chlorine. The FDA states that freezing temperatures and times vary with the nature of the fish to be frozen and the parasites to be killed. It seems that they recommend between -4 degrees F or less for 7 days and -31 degrees F or less for 15 hours for most cuts of fish. Thicker cuts need to be kept colder longer. The FDA goes on to say that brining and pickling are not safe ways to control for fish parasites as they are not effective methods for reducing parasite threats. Recent studies have shown that while not optimally effective alone, treatment of fish with chlorine in conjunction with ultrasound processing significantly reduces parasites in fish meat. Using an ultrasound for at least 30 minutes is another method for controlling for fish parasites that seems to work pretty well. The only other method that this author knows about is treating the meat with at least 15% NaCl (salt) after 7 days of storage. The paper I read about that bit pointed out that 20% NaCl was better and could be used after only 6 days of storage. I'm sure there are other methods, but these seem to be the most prominent as far as I can tell.

The risk of actually contracting these parasites in the United States is low. The liver fluke (C. sinensis) is extremely rare in the U.S. with most reported cases demonstrating patients who contracted the parasite in another country before coming to the US. Infections with D. latum are also rare in the U.S. despite once being common in people living around the Great Lakes. Recent cases have popped up from the West Coast, but are still not very prevalent. There are less than 10 cases of anisakiasis reported each year in the U.S.

The other bit of good news is that if you happen to contract any of these by some off chance of bad luck, they are almost never fatal. Additionally, they are rather easy to treat with drugs readily available here in the states.

The Moral of the Story
Don't ever let anyone make you feel bad for eating sushi...unless you are in a country with poor food regulations and the food looks sketchy, then you should definitely not eat the sushi. Use good judgement and know the warning signs just in case. You should be able to get plenty of good sushi, sashimi, gefilte fish, and ceviche here in the US of A since we make it a point to be especially careful when handling raw fish. Go celebrate with a dragon roll or some ebi!!!

Mmmmm!!!

Here's Lookin' at You, Giardia

Oh, Hi!

Arguably one of the most adorable of the diarrhea-causing protozoans would have to be members of Giardia. Sure, they cause terrible fatty stools, intestinal pain, and dehydration, but hey, at least it looks cute while doing it. I used to think that this parasite caused bloody stools, but I recently learned that this is not the case with Giardia. Rather, stools become "fatty". You see, as these parasites feed on mucous secretions within the intestinal walls of their hosts, they cause considerable damage to the microvilli and make it difficult for the intestine to absorb fats and other nutrients. This causes diarrhea and the aforementioned "fatty" stools. This parasite has been infecting humans for many, many years. Not many years ago we discovered that Giardia played a role in causing much of the dysentery contracted by the Crusaders in the 12th and 13th centuries as they invaded Palestine. The parasite didn't make its
grand appearance onto the world stage  until 1681, when Van Leeuwenhoek saw it for the first time. He found it as he examined his own stool during a bout of diarrhea exclaiming:

"My excrement being so thin, I was at divers times persuaded to examine it; and each time I kept in mind what food I had eaten, and what drink I had drunk, and what I found afterwards. I have sometimes seen animalcules a-moving very prettily..."

But I suppose I'm getting a bit ahead of myself. Let's start with the basics.

Taxonomy
As with any discussion of protozoan systematics, please keep in mind that as researchers discover more about these creatures their taxonomic categorizations tend to change. It is likely that even the upper taxonomy I am about to describe has since changed and I myself could easily be behind the times as I don't study this parasite exclusively and am not familiar with the latest taxonomic literature regarding this group of organisms. Like many other things, protozoan taxonomy exists in a state of perpetual flux. Disclaimers aside, this group belongs to Phylum Retortamonada as it lacks both dictyosomes and mitochondria. Members of this group are all flagellated and are either intestinal parasites or live freely in anoxic kinds of environments. They further belong to Class Diplomonadea and to Order Diplomonadida. Members of this order have two karyomastigonts (nuclei and associated organelles) and twofold rotational symmetry. Giardia further belongs to the Family Hexamitidae for having two equally-sized nuclei arranged beside one another. This morphological feature gives them that endearing "looking at you" feature that's made them so famous.

Interestingly, there have been more than 40 species described from this genus, but many of these have now been rendered invalid with the advent of molecular biology. Today, only five species are considered valid species within this genus. Two species within this genus infect birds, one infects amphibians, and two infect mammals. Of those two, only one causes disease in humans: G. duodenalis (formerly known as both G. intestinalis and G. lamblia).

From an evolutionary standpoint, Giardia duodenalis is interesting to study. It's simplistic life and primitive  morphology tells us that it is among the oldest of the protozoans. These guys are a basal group of protozoans existing before the development of mitochondria found in other protist groups. They also possess many flagella, which is also thought to be an ancestral condition.

Life Cycle
The life cycle of this parasite is simple. Fecal-oral contamination. Something that is infected poops in a place where the parasites won't dry out. At this point the parasites are in a cyst stage of their life cycle. When someone eats food that has been accidentally contaminated or drinks from a Giardia-rich water source, they pick up these cysts. Once in the body, the cysts transform into feeding stages known as "trophozoites". Trophozoites attach onto host intestinal tissues and feed off of the mucous linings causing all sorts of problems as it does so.

Giardiasis (a.k.a. "Beaver Fever" or "Recreational Water Illness")

We are just hangin' out...
munchin' on some mucous, yo!

Infection with this parasite is highly contagious. It spreads rapidly in areas where sanitation is not G. duodenalis either. These parasites can be passed by dogs, cats, sheep, and even beavers (hence the first common name for the disease).  Infections are easily acquired from water parks, lakes, and even resorts (hence the second common name). It can also be contracted from unwashed fruits and vegetables, or from contaminated drinking water.

Much of the time, cases of giardiasis are so mild that they show no clinical symptoms. However, some cases include symptoms like incapacitating diarrhea, intestinal pain, weight loss, flatulence, dehydration, and excess mucous production. In severe cases, patients present with colic or jaundice caused by infections of the gallbladder. Because the parasites disrupt fat and nutrient absorption, dietary diseases can also be come an issue if left untreated long enough. There are very few fatalities, but the disease is certainly no picnic.

Diagnosis
Most of the time giardiasis can be confirmed by examining a stool sample for cysts and trophozoites. Immunological techniques are also useful today. Things like ELISA testing or the use of PCR have been helpful in diagnosing giardiasis. In rare cases, duodenal aspiration is required to demonstrate these life stages if a person is not regularly passing the parasites. Now, I had never heard of duodenal aspiration, but it sounded like it wouldn't be much fun. Looking it up confirmed my suspicions. This involves passing a tube orally into the duodenum (part of the small intestine) and aspirating to dislodge the parasites for a proper sample. Nope. Not fun at all. Then again I don't know if that would be worse than the alternative, which would be an intestinal biopsy. Pick your poison.

Treatment
Lucky for us, being diagnosed is more difficult than determining how to treat a person with giardiasis. Metronidazole and quinacrine are the two drugs most often chosen to combat infection. This completely cures the patient in only a few short days. Because it is highly contagious, it is good practice to dose all immediate family members/roommates as well to avoid reinfection. It is equally good practice to determine the source of infection to take the measures needed to prevent future infections.

Seriously, even with all the symptoms, you have to admit these are adorable little guys!

A Colorful History

I want one!
(The plush, obviously.
Not the actual parasite
despite its cuteness.)

After appearing on Leeuwenkoek's microscope stage in 1681, this parasite went on to  pop up in many places around the world. Giardiasis outbreaks have occurred in many countries with a variety of impacts, ranging from small, localized epidemics to large-scale contamination of major city water supplies. As archaeoparasitology extends its reach into the realm of molecular biology, ELISA and other techniques are being utilized to reveal more about the effects of these parasites in both historic and prehistoric human populations. As mentioned earlier, a 2008 study pegged this parasite as part of the reason that Crusaders suffered from dysentery. How cool is that?! Other studies have revealed Giardia's presence in places far away, such as ancient Peru, as well as in places closer to home, such as a cemetery in Kansas dating from 1860 to 1900.

Moral of the Story
These ancient parasites are beginning to reveal to us more about the daily lives of people in both ancient and historic times the world over. They are teaching us that our ancestors suffered from some of the same things we struggle to combat even today despite our vast improvements in sanitation. Once again, here is a parasite to be admired...to be marveled at for its ability to survive this long as a species without something as fundamental as mitochondria. It's an easy parasite to love...it doesn't typically cause much more than discomfort, it's easy to treat, and let's face it, its morphology makes it kind of cute. (Plus you are very unlikely to die from it unless you refuse to get yourself treated.) Here's lookin' at you, Giardia.

Behaviors, Diets, and Parasites in Antiquity: Hymenolepids in the Grain Bins

Over the course of this semester, I've come to truly appreciate the interplay of diet, behavior, and parasitism. As a biologist, I find it fascinating to think about how the parasitism of a population is affected by the behaviors and the diets of host species. As a budding archaeoparasitologist, I find it even more fascinating to look at how human diets and behaviors have played significant roles in the diversity and prevalence of parasites that have wormed their way into our bodies (and of course our hearts...mostly in a metaphorical sense...).

 One of the many parasites that is brought up in discussions of behavior, diet, and parasitism is a little tapeworm sometimes called the "dwarf tapeworm". It's name has been changed several times in the parasitological literature (Taenia nana, Hymenolepis fraterna, and my personal favorite, Vampirolepis nana), but is currently called Hymenolepis nana. Another closely related parasite that can be brought up in such discussions is Hymenolepis diminuta.




Taxonomy
Like all tapeworms, these little dudes are classified as flatworms (Phylum Platyhelminthes) and belong to class Cestoda. They further belongs to the order Cyclophyllidae since they have four acetabula on their scoleces, hooked rostellae, and since they possess a single, compact postovarian vitelline gland. Other famous members of this order include the notorious taeniids (beef and pork tapeworms as well as Echinococcus sp.) and Dipylidium caninum, the double-pored dog tapeworm. H. nana and H. diminuta both fall within the family Hymenolepididae and are the only members of this family known to infect humans. Other members infect other mammals or birds instead. Most of the hymenolepidids require an arthropod as their intermediate host.

Life Cycles
The life cycles for these tapeworms are very similar. They begin with eggs being shed in the feces of an infected person or rat. These eggs are eaten by beetles, such as grain beetles (Tribolium spp.), and then hatch within the beetle's intestine. A cysticercoid with a tail develops within the beetle's hemocoel and waits to be eaten by the definitive host. A rat or human eats the beetle and the parasites are released in their new host's duodenum. From here, the parasites become oncospheres by shedding their tails and burrowing into the intestinal villi. The tapeworms absorb nutrients through their teguments as they grow and eventually little gravid proglottids snap off to release the tapeworms' eggs out of the host's body via defecation. With H. nana, the beetle is not a needed host, but is utilized from time to time. This species of tapeworm can actually infect definitive hosts via direct contact with contaminated feces.

Human Infection
We've already said that these guys can infect rats and humans alike, but we will just focus on humans for the sake of this post. (Sorry rats, another day!) As far as I can tell, there are rarely any major types of pathology related to infections with either of these tapeworms. It seems that the only real problems occur when a person is heavily infected with these worms...at which point the symptoms are similar to those for other tapeworm infections (e.g. abdominal pain, diarrhea, nausea, dizziness, anemia, etc.). When one is infected with either H. nana or H. diminuta, it is easy to cure with a dose of our old friend, Praziquantel. This drug is quick acting and does not typically require multiple doses.

Hymenolepis sp. in Archaeoparasitology
These tapeworms are found intermittently in coprolites from a variety of areas in the New World. Most cases are thought to have come from humans accidentally ingesting grain beetle gunk that got ground up when grains containing the beetles were being processed with stone tools. Since many rockselters where coprolites have been excavated make suitable habitat for small rodents, it is also possible that rats may have contaminated food sources or may have been a contaminated food source themselves. There is also the possibility that people were eating other kinds of beetles that housed one of these tapeworms. This could be especially true for H. diminuta, which has experimentally demonstrated that it can utilize over 90 different species of arthropods as intermediate hosts! It may sound weird today, but beetles and their grubs were great sources of protein for our ancestors. It would not be surprising to learn that they were eating infected beetles picked fresh from the vine or dug up with roots of tasty plants.

Archaeoparasitologists have demonstrated the presence of these tapeworms in coprolites from a number of archaeological sites. From Arizona, H. nana was found in Antelope House dating between 1175-1250AD. From nearby, Hymenolepis sp. was reported from Elden Pueblo, which dates from 1070-1250AD. From further south comes a report of Hymenolepis sp. from Santa Elina, Mato Grosso in Brazil that dates from 4000-2000BP. Such finds make it evident that these parasites have been opportunistically associated with humans for quite some time.


Moral of the Story
It is interesting to think of how behaviors such as no longer eating beetles on a regular basis or being perfectly content to crush grain beetles into our food have changed the type of parasites we as a society contract. Such simple changes in our diets and in how meticulous we've become in terms of food inspections have made cases of human infections with these parasites extremely rare occurrences in today's world.  It is amazing to think that not only what we eat, but what the things we eat are eating, can have an impact on our parasite burdens as a society. This dance between parasites, host behaviors, and dietary preferences is a wondrous one to behold. I'm hoping to soon get funding to further explore this balance along with how these things had effects on the development of the human immune system. I hope the grant proposal gets accepted...this would be quite an amazing dance to watch as the mysteries of our ancestors unfolds before my eyes. Here's to hoping the reviewers feel the same way!

Of Ants and Ungulates: The Notorius Dicrocoelium dendriticum

Greetings all! First and foremost, I must apologize for the entire month of November. I didn't post anything because I was caught up in the madness that was NaNoWriMo 2013! (I wrote a sequel to my NaNo2012 novel, but it is going to need LOTS of work to be anywhere near ready for publication, in case you were wondering.) And for more lame excuses for abandoning you, I've been busy working on a grant proposal and on generally trying to wrap up this roller coaster of a semester. My distractions aside, I decided today was a good day to pick back up where I left off with blogging.

Today, I present to you a parasite that has been studied exhaustively because of its commercial significance and because of its interesting life cycle. This parasite is a liver fluke most often found in ungulate (sheep, goats, cows, pigs, etc.) mammals. It has a blade-like tapered body giving it the common name of "lancet fluke". I'm speaking of course, of Dicrocoelium dendriticum.

Taxonomy
The lancet fluke belongs to the phylum platyhelminthes ("flatworms") along with free-living turbellarians (planarians), cestodes (tapeworms), and other members of class trematoda, (a.k.a. "trematodes" or "flukes"). Within class trematoda lies subclass digenea, a group characterized by life cycles with two or more hosts (typically including a molluscan host). D. dendriticum belongs to order plagiorchiformes within this subclass. The adults of this order are quite diverse, but the larval and juvenile stages are fairly conserved among its members. Members of this order have small eggs that are often eaten by a snail and cercariae are simple with a finfold on the dorsal side. The family of this parasite is family dicrocoeliidae, which is one of the three major families of liver flukes (along with fasciolidae and opisthorchiidae). Members of this family rarely parasitize humans, but are known to parasitize other mammals, especially domestic animals. All members possess a subterminal oral sucker and an anterior acetabulum.

 Life Cycle
The life cycle of this parasite is an eloquent complex of evolutionary wonder. It begins, as many life cycles do, with the feces of an infected mammal falling to the grass laden with Dicrocoelium eggs. Along comes a hungry snail, which devours the delicious droppings. Inside of the snail, the miracidium hatches from the egg and undergoes a variety of bodily transformations. The parasite then finds its way (at this point in the form of a cercaria)  into a slimeball that gets excreted by the snail. Snail slimeballs make tasty snacks for unsuspecting ants. After ingesting the cercaria, the parasite forms a metacercarial cyst within the body of the ant. This is when the most interesting aspect of this life cycle comes into play. The parasite, through processes not completely understood, is able to manipulate the behavior of its new host in order to continue its life cycle. For whatever reason, infected ants will climb onto tall vegetation in the evenings and lock their mandibles onto plants. This behavior is totally uncharacteristic of uninfected ants. The next day, the ants are eaten accidentally by grazing ungulates. Within the bile duct of the ungulate, the parasite joins thousands of other liver flukes and matures into adulthood. From there, the parasite mates with another and after about a month begins releasing eggs to perpetuate the life cycle and preserve the species.

Dicrocoeliiasis
Infection with this parasite typically presents as general dysfunction of the bile ducts due to irritation and over population in a finite area. Symptoms often include inflammation of the bile ducts, liver cell death, and fibrosis. Many types of ungulates, including sheep, deer, goats, pigs, and cattle, have been reported as having this parasite, making it agriculturally important to study.

There have been reports of D. dendriticum infections in humans, but most were instances of false parasitism. This means that people passed eggs after eating an infected liver but did not actually become infected themselves. True infections have been reported from Asia, Africa, Europe, and one case in New Jersey.

Treatment
There is not currently a good method for preventing the spread of this disease. After all, land snails and ants are never in short supply in the pastures where livestock are allowed to graze. For treatment of infected livestock, praziquantel and various benzimidazoles are the drugs of choice. Unfortunately, without adequate control measures, infection rates will continue to be high, meaning that treatment might not be economical for ranchers. With human infections, praziquantel is most often prescribed to take care of the infection.

 Moral of the Story
As with so many other fascinating parasites, behavioral modification of hosts continues to be a critical survival strategy. Ants must be easy targets for such manipulation due to their abundance and reliance on chemical stimuli. This is demonstrated time and again with how easily parasites seem to be able to zombify these colonial insects! More to the credit of the lancet fluke, the evolutionary processes involved in the development of its life cycle are impressive, to say the very least. The fact that this fluke not only managed to dupe ants into becoming kamikaze vessels for the benefit of the fluke's species, but the fluke also evolved beyond the reliance on water that is so commonly seen amongst other trematodes. What a beautifully crafted life cycle for such an interesting and unique organism! Just for funzies, here's a link to a sweet comic about this parasite from The Oatmeal. (You know a parasite is cool if it makes The Oatmeal! :p) Enjoy!

Why Captain Higgins is My Favorite Parasitic Flatworm