Oy Vey!: Pig Tapeworm in the Orthodox Jewish Community

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A few months back, Carl Zimmer published a short article on the startling widespread prevalence of neurocysticercosis; the larval infective form of the pig tapeworm Taenia solium that just so happens to infect the human brain. Check it out, but beware!, you will be learning about a parasite that gives unwelcome deep tissue massages in your gray matter and you will see photographic evidence of it.

The real trouble with this pig parasite, aside from it’s distressing appearance in your cerebral headquarters, is that you can acquire neurocysticercosis even if you don’t consume pork products. This is the surprise kicker, the coal in your Christmas stocking.

The mouth of the adult pork tapeworm, Taenia solium. The tapeworm typically lives in the intestines of pigs but may infect those that eat undercooked pork. The larva produced by the adult worm are passed in the feces and may go on to infect the organs and tissues of humans. Image: Dennis Kunkel Microscopy, Inc.

This is understandably alarming for people who choose to not eat pork but what if your culture and religion prohibits its very consumption? What does it mean to those that belong to a group with strongly delineated food taboos which just so happen to include those of the swinish variety? Say, Jews that are kosher and adhere to kashrut, Judaism’s set of dietary laws, that forbid consumption of pork because pigs don’t ruminate, or “chew the cud” (Leviticus 11:7, Deuteronomy 14:8)?

Sadly, this went beyond being a thought exercise to a reality for Orthodox Jews living in New York City in the early ’90s when isolated cases of neurocysticercosis arose in their community. These are not the sort of folk contemplating whether to include bacon bits into the dinner salad or debating whether to add just one more strip to a breakfast sandwich so just how exactly did they find themselves infected with a pig parasite? This sounds like an far-fetched urban tale but is rather a cautionary story that speaks to fascinating socioeconomic implications that appear in many developed cities worldwide.

In the summer of 1991, three practitioners of the Orthodox Jewish faith appeared on separate occasions in local NYC hospitals with recurrent seizures. Radiology showed evidence of brain lesions that were soon identified as cysticerci, the larval form of the pig tapeworm that had formed protective cysts within the brain. Most peculiarly, the patients were all absent of any of the risk factors that increase susceptibility to neurocysticercosis – consumption of undercooked pork products and/or traveling to foreign countries with endemic taeniasis (1). Examining related family members of the original three patients identified an additional seven people from two families that showed positive antibodies to the infection (known as seropositivity), including a fourth person that had experienced a seizure sending them to the ER.

The life cycle of the pork tapeworm. Infection with the tapeworm is strongly associated with pig husbandry along with poor hygiene. Accidentally ingested eggs can result in larva that migrate throughout the body eventually forming cysts. Image. CDC. Click for source.

After some epidemiological sleuthing, the culprit was soon identified – the families of these patients employed housemaids, all recent emigrees from Latin and Central American immigrants that were infected with the adult tapeworm infection and had transmitted the infective eggs to their employers. Other housemaids fled from investigators after being asked for blood and stool samples, presumably terrified of being implicated in the spread of an epilepsy-causing wormy. A common practice in this Orthodox Jewish community, these families had employed an average of over three housemaids from endemic countries in the past five years (1).

Shortly after this unusual crop of cases, a group of researchers from the CDC in Atlanta and the Maimonides Hospital in Brooklyn conducted a study of the Orthodox Jewish community to identify how prevalent neurocysticercosis had embedded itself in the community. Between November 1992 and February 1993, over 7000 households comprising a total of 35,000 people were examined for infection (2). An impressive number culled for a study into brain parasites, amirite? They must have had a powerfully persuasive representative to sell everyone on relinquishing blood samples.

Thankfully, only 23 people, representing a slim 1.3% of the population, showed positive antibodies to the parasite. Though this seems like a negligible prevalence rate – 1% that’s it?! – consider that populations with a 1% prevalence rate are deemed hyper-endemic regions in the public health world (3). The researchers, in fact, deemed “exposure to T. solium in this community [to be] unexpectedly high” (2). The researchers confirmed that infected Latin housekeepers in Orthodox Jewish households were the etiological cause of local cases of neurocysticercosis. They also found that housemaids originating from Central America and those charged with child care responsibilities were highly correlated with spread of the disease (2).

These women were raised in countries with exemplary levels of pork consumption, along with endemic pig tapeworm, or taeniasis, infection, and physically transported the parasite to non-endemic regions. Though taeniasis and neurocysticercosis is a disease of poverty, it will gladly ascend the socioeconomic ladder given the opportunity. The parasite is a social climber that arises from inauspicious beginnings – wallowing in the pigpen, if you will. But invite it into your home and it will climb another rung.

The global distribution of cysticercosis infection. Hot spots of infection, areas of high endemicity, are found in regions with high rates of pig product consumption. The WHO estimates that the disease affects 50 million people worldwide and causes an estimated 50,000 deaths a year. Image: WHO. Click for source.

A 2005 study documented this particular phenomenon in Peru, looking at housemaids that had left endemic towns to work for the more affluent in cities where the infection is scarce. These ladies migrate from areas that often lack modern amenities, such as closed sewage systems, potable water supplies and electricity, and in nearly 75% of cases, with households that rely on raising pigs to boost home income. In doing so, they carry the tapeworm into unsuspecting homes – investigators found that 1.2% of these women suffered from taeniasis infection. And, yes, the infection is transferred to their employers. Of those Peruvian employers that acquiesced to blood samples and CAT scans, 23% showed antibodies for infection. These Peruvian housemaids are the Typhoid Marys of T. solium.

In the Peruvian study, 60% of families were found to use housemaids to cook, assist with kitchen duties or to help with childcare (3). These services all greatly increase the chances of transmitting neurocysticercosis if proper food and sanitary hygiene isn’t practiced, which may be compromised if you hire someone who hasn’t been raised with, say, tiled bathrooms with flushing toilets and porcelain sinks. Hygiene is a learned luxury that only a few of us in this grimy world are accorded and, lemme tell ya, running water and hand sanitizer really help with these sorts of things. Hygiene has a price.

In the early 1990s, Orthodox Jew’s discovered this principle. Despite their best intentions in diligently adhering to strict dietary laws, rituals and rules that have protected their physical and spiritual health for millennia, they found that they were alarmingly susceptible to a porcine disease owing to their practice of employing people from outside their own cultural and socioeconomic strata.

We all have our own salubrious observances and rituals that we like to think maintain our health and well-being, from washing our hands, splashing bleach around the bathroom and kitchen, or even following certain dietary restrictions. But however aseptic and sanitized you live your day-to-day life, the reality is that we live in a world with other people – our coworkers, our friends, the people who serve us food in restaurants, the people we drink with at the bar, the children our kids play with, in short, everyone else.

Resources

The Wikipedia page devoted to “Taboo food and drink” is a superbly fun and fascinating read.

In a similar vein, this free academic paper on “Food taboos and their origins” is also enjoyable. Get it here. An article in the journal Radiology details a case of neurocysticercosis in an Orthodox Jewish woman. She had employed a Mexican housekeeper who had been infected with taeniasis for several years before presenting with seizures on the left side of her face and arm before being diagnosed in 1999. A handy guide for Jewish family that keep mitzvah, the commandments of the Torah, while employing non-Jewish housekeepers.

References

1. PM Schantz et al. (1992) Neurocysticercosis in an Orthodox Jewish community in New York City. N Engl J Med 327: 692–695

2. AC Moore et al. (1995) Seroprevalence of Cysticercosis in an Orthodox Jewish Community. Am J Trop Med Hyg 53(5):439-442 3. BN Huisa et al. (2005) Taeniasis and cysticercosis in housemaids working in affluent neighborhoods in Lima, Peru. Am J Trop Med Hyg. 73(3): 496–500 ResearchBlogging.org

Moore AC, Lutwick LI, Schantz PM, Pilcher JB, Wilson M, Hightower AW, Chapnick EK, Abter EI, Grossman JR, & Fried JA (1995). Seroprevalence of cysticercosis in an Orthodox Jewish community. The American journal of tropical medicine and hygiene, 53 (5), 439-42 PMID: 7485700

Everything You Didn’t Want to Know About Cockroaches

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Amongst its many epicurean, architectural and otherwise louche charms, New Orleans has another infamous, uncelebrated one: a problematically vibrant cockroach population. Every summer (oh, let’s be honest here: they’re here spring, summer and fall), the German brown cockroach can be seen snatching its way around your house, flitting on sidewalks at dusk, and intimidating the locals.

They fly down here in the Deep South, did you know?

One Saturday night back in August, one such creature dive-bombed into my cleavage. After one spilled G&T (Oh God, not my drink!) and many sputtered expletives, the critter was ousted and a friend graciously stomped it into a unrecognizable smear into the pavement.

And so with the impending cockroach population explosion coming any summer day now, I figure why not have a chat about what diseases they can harbor and spread on your tabletops. Hmmm? And lest you think that this article is a paean extolling their overlooked virtues – alas! – they really are as filthy as everyone thinks they are.

A colored scanning electron micrograph of Periplanta americana, the American cockroach, one of the smallest known species. Note the ubiquitous hairs covering the insect, allowing for microbes to be picked up during its feedings. Image: Dr. Biology, Arizona Board of Regents. Click for source.

I’ll try to make this as painless as possible.

Out of the 4000 species of cockroach that exist, there are three major species that plague humanity – Periplaneta americana, Blattella germanica and Blattella orientalis. They feed on just about anything, even their deceased brethren, but they do have a sweet tooth and prefer to eat sugary and starchy items such as sweets, cardboard and book-bindings (1). Included in their rather diverse diet is their consumption of human detritus such as feces, sputum, toe nails, and bodily residue on surgical swabs. These unseemly dietary choices lead to their contamination of food, utensils and surfaces for food prep and have direct consequences on human health in three interrelated ways – their arbitrary feeding habits, eating both human excrement and human food; their indiscriminate defecation habits; and the fact that they regurgitate digestive fluids in the process of eating (2). Endearing, no?

Roaches also serve as an important source of infectious pathogens. They serve as a sort of public transit for the busy microbiological world, a bus ferrying bacteria, viruses, fungi and parasites between filth and human comestibles; really, every buggy imaginable rides on this double-decker of an arthropod. Bacteria and viruses settle into the crevices and cracks between thorax and head, and begin to multiply. There are so many fissures and clefts and crannies on a cockroach. Everywhere there are hairs, but especially on the six legs that escort these scuttling creatures from one dark, humid hideaway to another. Microbes snatch a ride on these hairs or are accidentally consumed by the cockroach only to pass into the alimentary canal where they may multiple in number. In one study, the bacterium Pseudomonas aeruginosa was found to have increased multiple-fold over the course of 114 days in the gut of a cockroach (3).

Colored scanning electron micrograph (SEM) of Blattella germanica, the German cockroach, one of the smallest known species. This roach’s long antennae can be seen protruding from its head and its wings (blue) can be seen at lower left. The anatomy of the cockroach provides several areas for bacteria, viruses and parasitic eggs/cysts to settle into. Image: Volker Steger, Science Photo Library. Click for source.

In this regard, roaches are not so much vectors as they are reservoirs; a mosquito will squelch its proboscis in your ankle, inoculating you with malaria in their quest for blood but a cockroach indiscriminately contaminates anything lying around. Entomologists describe this process as “mechanical transmission”, indirectly transmitting disease to humans. It’s not personal, it’s just business. 

All types of passengers are welcome on this cockroach bus. Over 30 species of bacteria have been found on the cuticle and gut of roaches, including those of serious medical import such as E. coli, various species of Salmonella and Staphylcoccous, Pseudomonas aeruginosa and Klebsiella pneumoniae (4). These bacteria cause diseases such as urinary tract infections, dysentery, diarrhea, pneumonia, cholera, polio, septicemia and wound infections (5). One study that trapped cockroaches in order to measure their bacterial load found that number was as high as 14 million microbes found on the exterior of the bodies, and 7 million in their fecal droppings (5).

Viable eggs and dormant cysts of parasites also hitch a ride; the culprits include the ova of Ascaris lumbricoides (giant roundworm), Anchylostoma deodunale (hookworm), Trichuris trichura (whipworm), Enterobius vermicularis (pinworm) and Strongyloides stercoralis (threadworm), and the cysts of Entomoeba hystolitica, Balantidium coli, C. parvum, C. cayetenensis and Isospora belli (4). Even the virus that causes polio, poliomyelitis, has been found within the guts of cockroaches (6).

There are several documented cases of small outbreaks that pinpoint to cockroaches playing an indirect but prominent role in disease transmission. In one county in Northern Ireland in the late 1970s, fifteen food-handlers in various establishments fell ill to dysentery caused by the Shigella bacterium over the course of eight weeks (2). These restaurants had serious infestations, particularly in the kitchen and dining areas, and the stomach contents of trapped roaches showed viable Shigella dysenteriae serotype 7 bacteria, incriminating the arthropods in the spread of the disease.

Cockroaches were also suspected to be the cause of a hepatitis A outbreak in a Los Angeles housing project in the late 1950s. From 1956 to 1959, the Carmelitos Housing Project represented 39% of all cases of hepatitis A in Los Angeles County with numbers of the infected steadily increasing through the years (7). It was only until a full-scale cockroach control program employing a newly developed insecticide, the industrial silica aerogel Dri-Die 67, was the outbreak halted. Two years following the program, incidences of hepatitis A from the Housing Project dropped to 0.0% and cockroaches traversing between the sewage system and the Project were pinpointed as the source of the epidemic.

A colored scanning electron micrograph close-up of Periplaneta americana, the American cockroach, which can be found around the world. Image: Stephen Gschmeissner. Click for source.

Typhoid patients in Italy were found to have cockroaches harboring S. typhi in their homes in a study conducted in 1943 (2). Similarly, the same organism was found in cockroaches infesting a Belgian hospital’s children’s ward undergoing an epidemic of gastroenteritis in 1950 (2). Most recently, outbreaks of Klebsiella pneumoniae in neonatal units have been tied to cockroach infestations in hospitals in Ethiopia and South Africa (8)(9). These studies indicate that cockroaches may play an unappreciated role in the epidemiology of infections in both the home and hospital.

Though it’s difficult to say what part roaches play in small disease outbreaks, they are capable of harboring antibiotic-resistant bacteria. A 2012 study in Ethiopia looked at cockroaches trapped in a neonatal intensive care unit and found widespread multi-drug resistance among individual species of bacteria residing in the roaches. Reading the lists of antibiotics these bacteria were found to be resistant to is like a “who’s who” of the antibiotic world – ampicillin, augmentin, tetracycline, chloramphenicol, amoxicillin, doxycycline, and ciprofloxacin (8). An earlier study in South Korea found that cockroaches trapped in homes located 3 miles from a hospital harbored bacteria that were resistant to anywhere from 6 to 12 commonly used antibiotics (3). These medications are the mainstay for treating bacterial infections and the discovery that cockroaches in hospitals harbor bacteria no longer susceptible to them is discomfiting to say the least.

Bugs are such an inescapable component of our day-to-day living, whether we care to acknowledge them or not. They live their own buggy lives, spinning webs, squirming through our compost or draining picoliters of our blood. We pay little attention to them until they inconvenience us and spoil our clean, bleached perception of the world.

Cockroaches are especially gifted at this. They are the boldest creepy-crawlies, not only daring to openly traverse our homes and personal spaces but thriving in those environments. They need us for the waste and shelter we provide, and for that we despise them. And, sadly, the public opinion of them isn’t wrong. They really are gross – they serve as an efficient means for microbes of all kinds to traverse between sites of human waste and food preparation and consumption. Their traipsing through family dwellings, food establishments and hospitals compromises public health and may also contribute to the ongoing antibiotic-resistance in bacteria worldwide.

Check out the Resources below to see how you can prevent buggies and bacteria from getting a free ride into your kitchen. In the meantime, happy hunting!

Resources

The most recent cockroach-related outbreaks of disease have happened in developing countries that may lack adequate municipal sanitation and regular garbage disposal. Hospitals and multi-family dwellings that rely on old buildings may also suffer cockroach infestations due to shoddy construction or inevitable decay (3)(10). The WHO has a very helpful, fact-filled PDF here on how to protect your home from these little invaders.

Really wanna get in deep with Blattella germanica, the German cockroach? For only $326, this book could be yours. What a deal!  If you’re just into skimming, then you can check it out on Google here.

Cockroaches can dirty up human spaces but at least they have little friends that can keep their own bodies clean – mites!

From the ignominious Daily Mail, a collection of scanning electron micrograph images of the buggies that live in your home with you. More images can be found here but they’re sadly unlabeled.

References
(1) Rozendaal JA. October 1997. “Cockroaches.” Vector control: Methods for use by individuals and communities. World Health Organization. PDF of chapter is accessible here. Click here for access to the entire resource.
(2) Burgess NR & Chetwyn KN. (1981) Association of cockroaches with an outbreak of dysentery. Trans R Soc Trop Med Hyg. 75(2): 332-3
(3) Hsiu-Hua P et al. (2005) Isolation of bacteria with antibiotic resistance from household cockroaches (Periplaneta americana and Blattella germanica) Acta Tropica 93: 259–265  T
(4) Tatfeng YM et al. (2005) Mechanical transmission of pathogenic organisms: the role of cockroaches. J Vect Borne Dis. 42: 129–134
(5) Chaichanawongsaroj et al. (2004) Isolation of gram-negative bacteria from cockroaches trapped from urban environment. Southeast Asian J Trop Med Public Health. 35(3): 681-4
(6) Healing TD. (1993) Arthropod Pests as Disease Vectors. Proceedings of the First International Conference on Urban Pests. Accessible here.
(7) Tarshis IB. (1962) The cockroach–a new suspect in the spread of infectious hepatitis. Am J Trop Med Hyg 11: 705-11
(8) Tilahun et al. (2012) High load of multi-drug resistant nosocomial neonatal pathogens carried by cockroaches in a neonatal intensive care unit at Tikur Anbessa specialized hospital, Addis Ababa, Ethiopia. Antimicrobial Resistance and Infection Control. 1: 12
(9) Cotton MF et al. (2000) Invasive disease due to extended spectrum beta-lactamase-producing Klebsiella pneumoniae in a neonatal unit: the possible role of cockroaches. J Hosp Infect. 44(1): 13-7
(10) Fakoorziba MR et al. (2010) Cockroaches (Periplaneta americana and Blattella germanica) as potential vectors of the pathogenic bacteria found in nosocomial infections. Ann Trop Med Parasitol. 104(6): 521-8

ResearchBlogging.org
Pai, H., Chen, W., & Peng, C. (2005). Isolation of bacteria with antibiotic resistance from household cockroaches (Periplaneta americana and Blattella germanica) Acta Tropica, 93 (3), 259-265 DOI: 10.1016/j.actatropica.2004.11.006

An Update on Baylisascariasis: Benign Infection in an Elderly Woman

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A timely letter was published in the Emerging Infectious Diseases journal shortly after my article on Baylisascaris procyonis was posted two weeks ago. It describes a quite unusual case of the infection in a recently deceased elderly woman that had lived in British Columbia, Canada. I wanted to write a quick note about this because it changes the dimensions of our understanding of this parasitic infection, challenging the notion of this disease as typically only afflicting infants and toddlers. Additionally, this letter nicely demonstrates how essential autopsies are to the ongoing pursuit of medical knowledge.

The patient was a 73-year-old woman who had suffered from Alzheimer-induced dementia for nearly a decade. She had spent most of her life living in a rural region of British Columbia and, towards the end of her life, as a resident in a nursing home. An autopsy indicated that the cause of her recent death was cardiopulmonary arrest due a large pulmonary embolus or, in layman’s terms, a blood clot.

"Baylisascaris procyonis infection in the frontal cerebral lobe white matter. A) Larval nematode seen in multiple transverse sections, surrounded by mild chronic inflammation and reactive changes. B) Morphologic features of the larvae included maximum diameter of 65 μm; thin, striated cuticle (Cu); single paired lateral alae (Al); and paired excretory columns (EC) that were smaller in diameter than the central intestine (In)." Image & description: Hung T et al. Click for source.

Aside from the expected Alzheimer-associated pathology found in the brain, there was also a number of lesions in the white matter of the left frontal lobe. Each lesion contained a single larva that was identified as B. procyonis, the raccoon roundworm that is rarely found in the human brain. These lesions were surrounded by inflammatory cells and what the authors describe as “mild chronic reactive changes”. I take this to mean that there was some fibrosis encapsulating the larva, which is a typical reaction of the body to most parasites and fomites. You can see this in the images published with the letter and reproduced to the left – there are dozens and dozens of little cells with black nucleic surrounding five larva and their density decreases as it radiates outward from the locus of the parasites. A tornado of cells. The brain tissue just looks busy and annoyed, doesn’t it?

The authors note that, yes, this woman had dementia which might have masked any of the clinical implications from baylisascariasis. However, there isn’t any behavioral or pathological evidence to exclude the fact that this was anything but a benign or mild infection.

Just what am I getting to? This: baylisascariasis might be more common in the population as a benign or sub-clinical infection then us parasitologists had previously thought. I briefly alluded to this in my article by mentioning  research of children in Chicago with B. procyonis antibodies but didn’t evince any symptoms of infection. There might be a lot more of us walking around with baby raccoon roundworms in our noggins and we might never know until we drop dead of old age and our skulls are cracked open all in the name of science.

There is no definitive way to know just when was this woman was infected. Did she have this infection for decades, having inoculated herself with the eggs around her home in rural British Columbia, or was this a recently acquired infection in the years before her death? Or, did she get the infection as a result of the behavioral manifestations of Alzheimer’s disease, as the authors suggest: “More likely, the combination of confusion and poor hygiene and ambulatory state in the patient may have predisposed her to acquiring B. procyonis roundworms through ingestion of contaminated soil.” Who knows! It’s a parasitological mystery! The best kind, no?

This letter is an exciting and important development for our understanding of this disease on three grounds. First, the case involves the oldest patient on record infected with Baylisascaris procyonis. Second, this marks only the second case from Canada, which may carry epidemiological implications regarding the spread of the parasite and its dynamics with the raccoon population in the country. Data on the parasite’s prevalence in the human population remains super sparse, so the Canadians will just have to keep this case in their back pocket and save it for when new insight into the parasite’s prevalence becomes available. Third, and most importantly, this woman seems to have had a totally asymptomatic infection of the parasite. She did not die from the infection and seems to have exhibited no untoward symptoms that one would anticipate considering giant larva babies were lodged in her brain. Her death cannot be attributed to the larva’s presence, just to old age and bad luck.

Autopsies are an incredibly vital and under-appreciated resource in public health and medicine. Without the results of this Canadian’s autopsy, we might never know that baylisascariasis can occur in humans as a benign or sub-clinical infection. A few months back, the supremely excellent news agency Pro Publica conducted an investigation into the state of autopsies in America,  “Post Mortem: Death Investigation in America”. Their articles and research make for a fascinating read and document the decline in forensic facilities, their access to necessary resources to perform autopsies, the numbers of properly trained coroners and forensic pathologists and, critically, an overall decline in the numbers of autopsies performed nationwide. There are a number of reasons why this is the case and I highly recommend a visit to their site where you can brush up on your real-life CSI knowledge. Just be sure to strap yourself in for an alarming few hours of gripping, horror-story reading.

This short research letter has yielded a tiny but important spot of data that tells us more about our immunological response to this fascinating parasite and the scope of its possible disease manifestations. If more autopsies were conducted in the States, we might know a lot more about the parasites and protozoa that hitchhike in our bodies and brains. Information that I know we’re all desperately craving for, right?

References

Hung T, Neafie RC, & Mackenzie IR (2012). Baylisascaris procyonis infection in elderly person, British Columbia, Canada. Emerging infectious diseases, 18 (2), 341-2 PMID: 22305101

This post was chosen as an Editor's Selection for ResearchBlogging.org

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