Thoughts on the New Bird Flu H7N9 & It’s Animal Connection

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Much of the United States is mesmerized by the belligerent squawks from North Korea’s Kim Jong-un and the volatile tension straddling the Korean peninsula, but I’m more concerned about what is happening in China right now and the troubling trickle of news on a new bird flu strain H7N9.

At least 16 people have been infected, patients who were widely distributed through the geographic enormity that is China, and already six have died. But what makes this small cluster of flu cases unusual is its timing – we usually see flu outbreaks emerging in the fall and winter months and we are just now breaking into the month of April – and that this type of flu strain is not known to infect humans.

H7N9 seems to be following a well established pattern of other emerging viruses: originating in east Asia, the infection appears to have a tentative association with wet markets and butchering, and is of zoonotic or animal origin. We’ve seen this situation previously with Nipah virus in Malaysia infected pigs and slaughterhouse employees and with SARS and its birth in the wet markets of Guangdong Province in China.

Laurie Garret masterfully crafts an unnerving story, of unknown unknowns regarding these human flu cases and the potential linkage between the thousands of pigs and fowl carcasses that clogged Chinese waterways in March.

Here’s how it would happen. Children playing along an urban river bank would spot hundreds of grotesque, bloated pig carcasses bobbing downstream. Hundreds of miles away, angry citizens would protest the rising stench from piles of dead ducks and swans, their rotting bodies collecting by the thousands along river banks. And three unrelated individuals would stagger into three different hospitals, gasping for air. Two would quickly die of severe pneumonia and the third would lay in critical condition in an intensive care unit for many days. Government officials would announce that a previously unknown virus had sickened three people, at least, and killed two of them. And while the world was left to wonder how the pigs, ducks, swans, and people might be connected, the World Health Organization would release deliberately terse statements, offering little insight.

By the end of March, at least 20,000 pig carcasses and tens of thousands of ducks and swans had washed upon riverbanks that stretch from the Lake Qinghai area all the way to the East China Sea — a distance roughly equivalent to the span between Miami and Boston. Nobody knows how many more thousands of birds and pigs have died, but gone uncounted as farmers buried or burned the carcasses to avoid reprimands from authorities.

We are very early into this developing scenario and this spate of cases could fizzle into just a blip in the news cycle and on the infectious disease radar. You should read Maryn McKenna’s reasoned and calm analysis here and to devour a slew of delicious infectious disease geek resources at the tail end of her article.

The point I want to make here is a reminder of how closely intertwined the lives of humans are with the lives of the animals we breed and eat. Not many of us raise pigs in the backyard or hear the cock’s crow in the morning and it’s easy to forget that for thousands of years we have lived in close proximity to our poultry and livestock.

But this is still the case in developing nations and particularly those with industries reliant on raising and butchering animals for the global market as well as people supporting a family with their hens and chicks. It is these people and places that are at most risk of emerging zoonotic infections like H7N9 and they require careful surveillance and monitoring of the health and well-being of both people and animals. Remember: catching a novel disease from an animal is the rule not the exception.

Resources

The most important link I can give you: “The New Bird Flu, And How To Read The News About It” from Maryn McKenna.

A timeline of events from Laurie Garret’s article “Is This a Pandemic?” in the short news cycle of H7N9. Her article can be accessed here.

Shanghai will be temporarily closing its live poultry markets on Saturday due to fears of a spreading H7N9 .

Man’s Best Friend, the Turkana Tribe & a Gruesome Parasite

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Dogs are dirty, dirty animals. I know because I’ve had several, which currently includes a mud-loving, cockroach-catching, drooly mess of a boxer who enjoys nothing more than sleeping her way over every soft surface in my house. The fact that dogs also transmit diseases, and an incredible variety of them at that, does not help matters! Parasites, viruses, bacterial and fungal infections! To their owners! To me, maybe you, maybe your friends! Your relationship with your pet is, in short, a lot richer than you could ever imagine. In light of this, I have a real doozy of a story about the relationship between pet dogs and a miserable little parasite set in the barren desert of northwest Kenya.

First, the parasite. Echinococcus granulosus is the causative agent of hydatid disease, a real nasty piece of work that usually plagues dogs and the ruminants they herd or hunt. Hydatid disease typically follows a dog-sheep-dog pattern, cycling through its intermediate host, the sheep, with the ultimate destination in its direct host, the dog. Dogs eat infected viscera, become infected with thousands of tiny tapeworm, shed the tapeworm eggs in their feces, sheep consume the eggs and the band plays on.

The life cycle of E. granulosus. Image: CDC. Click for source.

E. granulosus is ugly business for intermediate hosts and those poor souls who have inadvertently consumed the eggs. Following ingestion of the eggs, the larva bursts free from its shell, penetrates the intestinal wall and speeds it way to the liver, lungs, spleen and a few other choice organs. The disease manifests slowly, with bubble-like cysts sprouting from these organs. It’s quite horrific. At this point, this infection is termed hydatid disease. One of the most striking experiences of my parasitological studies was seeing an image of a dissected echinococcosis-infected rat with its entire body cavity filled with spherical pink cysts. It looked like an overflowing bubble bath. In my opinion, hydatid disease is the ne plus ultra of gruesome parasitic diseases.

In humans, hydatid disease directly results from accidental consumption of the parasite eggs. The disease appears as multiple solid, tumor-like cysts sprouting on the interior and exterior of the organs. The cysts can range in size from 2 to 20 cm, are filled with fluid and can contain many smaller, daughter cysts (1). As the fluid-filled cyst is under pressure, problems can develop if the cyst happens to rupture as a result of trauma (2); if this untimely event occurs, the body will go into anaphylactic shock. Symptoms depend on what region of the body is infected: in the liver, jaundice, abdominal pain and biliary duct obstruction can occur; in the lungs, coughing and chest pain. Cysts can metastasize to other regions of the body as well.

The disease in endemic in agricultural and herding regions throughout the world, in particular Eurasia, the Mediterranean, North and East Africa, and Australia (2). The disease can be found in wild animals, ruminant livestock and domesticated dogs. The parasite is a global economic pest, significantly reducing meat and milk production as well as causing fertility loss in livestock. It is also one of the major zoonotic parasitic diseases afflicting humans in such regions as the Middle East, Arabic North Africa and Eastern Europe (3). The only place in the world that has the highest incidence and prevalence of hydatid disease is the Turkana district, due to the unique role that dogs play in the day-to-day life of their human owners.

A map of the Horn of Africa, showing the location of the Turkana district highlighted in pink. Image: Unknown. Click for source.

The Turkana are nomadic pastoralists living on a 60,000 km2 parcel of land in northwest Kenya, in an arid region bound by Uganda, South Sudan and Ethiopia (4). For centuries, they’ve spent their lives herding goats, cattle and now, due to a serious drought, desert-hardy camels. It’s an environmentally hostile place – a remote, scorchingly hot desert. Communities lack educational and medical facilities, and limited access to what little safe water exists. A Turkana survives on less than a dollar a day, a situation regrettably common in this region (5). Droughts regularly assault the region. Safe to say, the place is not on many lists of possible vacation spots.

What makes this tribe so unique is their exceptionally intimate relationship with the yellow pariah dogs that live in their small communities. This relationship far exceeds the traditional pet ownership bond that much of the industrialized world indulges in with their furry creatures. The Turkana dogs live and sleep within an enclosed homestead, known as manyattas, that is composed of several huts. Dogs often lick clean cooking-ware and serving-ware and are encouraged to consume remaining leftovers. They have been reported as occasionally defecating in the huts that they spend all day in to escape the desert heat (6). They serve as nurse-maids (nurse-dogs?) to children who have yet to be toilet-trained and lick clean infants after they vomit (7). They consume the menses of the women, in a process that was only briefly alluded to in the literature I researched (8). Thankfully.

A Turkana woman in her hut preparing food and surrounded by scavenging yellow pariah dogs. Image: CN Macpherson et al. Dogs, zoonoses, & public health. Click to access the online book.

The dogs’ feces are prized and used medicinally, cosmetically and spiritually (7). They’re often used to dress wounds and women will smear them on their chest to alleviate the weight and chafing of the heavy beaded necklaces that they wear multiply stacked on their neck. Not quite Neutrogena or Aveeno moisturizing lotion but this is desert-living on a budget, people! Dog feces also have protective spiritual qualities and can ward off evil spirits (the living and dead, I presume)(9).

In a region bereft of water, employing dogs to clean infants and inanimate objects as an alternative to using scarce water starts looking cleverly reasonable. It’s not the most hygienic standard of living according to our Purell-absolutely-everything Western style of living but the Turkana seem to make do aside from this little parasite dilemma.

Anywhere else in the world, humans are an accidental host to echinococcosis. In the Turkana district, the Turkana play an extraordinarily active biological role due to their tribal customs (10). It’s not only that dogs lick children, cooking objects and themselves, thereby inoculating pretty much everything with infective feces. The Turkana also feed the dogs the infected entrails and hydatid cysts of slaughtered livestock (8). The dogs don’t just stay indoors sleeping, crapping and licking away in the huts  – they also lay in what few waterholes that exist in order to cool off, contaminating the Turkana’s meager water sources. Dogs also scavenge the remains of potentially infected wildlife and dead Turkana, reinfecting themselves with the parasite.

‘Dead Turkana’, you say? Oh yes, the Turkana don’t indulge in expensive burial rituals: only respected elderly men and married mothers are given a proper burial while the rest of the crowd are shallowly covered in the desert, giving wild animals and dogs ample access to consume infected human remains (10). These burial patterns ensure that hydatid disease continues within the Turkana community as well as promoting a wild animal reservoir for the parasite. So there’s that little anthropological factoid that factors into this hydatid story as well.

Left. A Turkana woman infected with hydatid disease. Right. A physician cradling the surgically removed hydatid cysts. Image: Unknown. Click for source.

So cue in the Lion King’s “Circle of Life” song here. The contributions of the Turkana to the cycle of echinococcosis is so epidemiologically exquisite, it’s damn near perfect. It’s an ideal situation for this parasite, being continuously shuttled between its direct host, the dog, and a rather supportive intermediate human host. The Turkana’s tribal customs and enduring bond with dogs ensures that hydatid disease remains in the community; research indicates that echinococcosis eggs have been found everywhere – from the topsoil inside and surrounding huts, inside water and cooking containers, and contaminating well water (11). As such, the Turkana have a whopping 7 to 10% echinococcosis prevalence rate and as many as 65% of canines can be infected (5). Rates of infection are higher in the more northern, arid regions due to the considerable reliance upon livestock husbandry and a greater dependence upon dogs to clean items owing to the greater scarcity of water (4)(1).

The best method for treating echinococcosis is surgical management, in which cysts are excised intact or are individually treated using the PAIR technique. PAIR consists of carefully poking a hole in a cyst, aspirating the fluid from the cyst, infusing chemotherapy drugs in the cyst and then re-aspirating the drugs (Percutaneous Aspiration, Infusion, Reaspiration). This method allows for the cyst to be killed in situ and is much safer for the patient. Many medical groups have traveled to Kenya in the ‘70s to treat the Turkana and by 2004 over a thousand people have been been treated with either surgery or PAIR and an additional 2500 others with chemotherapy (5). These treatments have resulted in a reduction of prevalence of hydatid disease in the tribe from 7% to 2.5%.

Groups that have attempted to educate the tribe on the parasite and change their behaviors see little success (12). Campaigns to control hydatid disease is hindered by the nomadic nature of the Turkana, their extreme poverty and low literacy rate, as well as the considerable expense of canine chemotherapy. The tribe is unwilling to change their attitudes to the dogs and to their vital role in the community (7). So far, the most profitable strategy, in terms of financial cost and public health, of dealing with hydatid disease in the Turkana is treating individuals with surgery and PAIR.

As I was doing my research, I kept on thinking, “Well, what can you really do with this community?” They’re an ancient nomadic people who have been doing their own thang for centuries. And, you know, it’s been working out pretty well for them, aside from this whole ‘bubbling cyst in my belly’ snafu. Sure, some people might suffer some ill effects from infection but that number is tiny, a slight 2 to 7% of the population. For the most part, the disease can be asymptomatic and the case-fatality rate is superlow at 2% (2). So why mess with a good thing? On one hand, I think we should be reluctant to introduce Western modes of thought and culture into the unique cultural lifestyle of the Turkana. On the other, hydatid disease is a serious economic dilemma for the tribe, makes a select few of the population very ill and, well, is just gross!

So: what to do? I’m tempted to say leave them to their canine-loving ways. The Turkana attribute this “big-belly disease” is a curse from their neighbor enemies, the Toposa in southern Sudan (8). It’s a curse alright but the only people they have to blame are themselves. Here’s to giving hugs, not kisses, to your dogs!

RESOURCES

To see more pictures of the Turkana, their home and way of life, check out this Picasa album by Dr. Melanie Renfrew.

I briefly alluded to a nasty drought affecting the Turkana. Please read this article and how it is radically changing their ancient way of life here.

To read a case of a Somali woman with multiple hydatid cysts in her hip (her hip!), go here. Beware: lots of medical jargon and a gruesome picture of the excised cysts.

A story of a LA infectious-disease practitioner and the travails of her Palestinian patient infected for over 60 years with the parasite.

REFERENCES
(1) T. Romig et al. (2011) Echinococcosis in sub-Saharan Africa: emerging complexity. Vet Parsitol. 181(1): 43–47
(2) D Despommier, RW Gwadz, PJ Hotez and CA Knirsch. Parasitic Diseases. 5th ed. New York: Apple Trees Production, LLC. 2006
(3) Seyed Mahmoud Sadjjadi. (2006) Present situation of echinococcosis in the Middle East and Arabic North Africa. Paristol Int. 55 Suppl: S197 – S202
(4) RM Cooney, KP Flanagan & E Zehyle. (2004) Review of surgical management of cystic hydatid disease in a resource limited setting: Turkana, Kenya. Euro J of Gastroenterology & Hepatology. 16(11): 1233–1236
(5) J Magambo, E Njoroge, E Zeyhle. (2006) Epidemiology and control of echinococcosis in sub-Saharan Africa. Parasitol Int. 55 Suppl: S193 – S195
(6) TM Wachira, CNL Macpherson & JM Gathuma. (1991) Release and survival of Echinococcus eggs in different environments in Turkana, and their possible impact on the incidence of hydatidosis in man and livestock. J of Helminthology. 65(1): 55-61
(7) G. Oncnoke. (1991) Echinococcosis in Turkana District, Kenya. Proceedings of the 6th International Symposium on Veterinary Epidemiology & Economics, Ottawa, Canada, Public health session. Pg 634
(8) AA Majok & CW Schwabe Development among Africa’s migratory pastoralists. Greenwood Publishing Group, 1996. Online book.
(9) MC Inhorn & PJ Brown. An anthropology of infectious disease: international health perspectives. Psychology Press, 1997. Online book.
(10) CN Macpherson (1983) An active intermediate host role for man in the life cycle of Echinococcus granulosus in Turkana, Kenya.  Am J Trop Med Hyg. 32(2): 397
(11) I Buishi et al. (2006) Canine echinococcosis in Turkana (north–western Kenya): a coproantigen survey in the previous hydatid-control area and an analysis of risk factors. Ann Trop Med Parasitol. 100(7) 601–610
(12) DL Watson-Jones & CN Macpherson (1988) Hydatid disease in the Turkana district of Kenya, VI. Man:dog contact and its role in the transmission and control of hydatidosis amongst the Turkana. Ann Trop Med Parasitol. 82(4): 343-56.
This post was chosen as an Editor's Selection for ResearchBlogging.org
Romig, T., Omer, R., Zeyhle, E., Hüttner, M., Dinkel, A., Siefert, L., Elmahdi, I., Magambo, J., Ocaido, M., Menezes, C., Ahmed, M., Mbae, C., Grobusch, M., & Kern, P. (2011). Echinococcosis in sub-Saharan Africa: Emerging complexity Veterinary Parasitology, 181 (1), 43-47 DOI: 10.1016/j.vetpar.2011.04.022

Consider the Carpaccio: Looking at Toxoplasmosis

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A parasite that infects the human brain, subtly changing its personality and social behavior, and capable of passing from mother to infect an infant in utero? That is the essence of a body horror, but this little rascal isn’t fiction. And it gets better: this parasite is considered to be one of the most successful parasites in the world due to its widespread, global distribution as well as its capacity to infect nearly every type of body tissue in all warm-blooded vertebrates (a). Schedule a phone conference with Spielberg and Cruise ASAP, guys, we’ve got the next sci-fi-action blockbuster on our hands (brains?). We’re looking at the ubiquitous protozoa Toxoplasma gondii and research on its capacity to modulate human personality and behavior.

T. gondii is an obligate intracellular parasite that has a vast host distribution, capable of infecting all species of mammals. Domestic cats and other felines are, however, the definitive host for the parasite’s reproductive stage. As such, all other animals serve as intermediate hosts of this polyxenous parasite. Humans are usually infected through consumption of infected raw or undercooked meats that happen to be studded with tissue cysts, typically lamb or pork (a). Turns out that T. gondii infection, known as “toxoplasmosis”, is the most common food-borne parasitic infection that requires hospitalization, and the third most common food-borne illness overall (b). Indeed, a study in 2002 conducted in the United Kingdom examined commercial meat sold in grocery stores and found that 38% of samples were infected with T. gondii cysts (h).

Examples of Toxoplasma gondii transmission. Image: Nature Education. Click for source.

Humans can also acquire infection through contaminated water and contact with cat feces that contain oocysts. Depending upon one’s diet and exposure to cats, researchers estimate that up to 80% of the population may be infected with T. gondii (k). Unwelcome news for lovers of carpaccio and cats.

Acute toxoplasmosis includes symptoms very similar to a cold – fever, headache, sore throat and coughing – along with a few psychopathological features including depression, anxiety, apathy and paraesthesia (“pins and needles” sensation) (c). The parasites (in the form of tachyzoites, one stage of its life cycle) infect macrophages and are distributed throughout the body. Over time, parasite-containing cysts form as a response to the body’s acquired immunity and are commonly found in the brain, lymph nodes, lungs and liver (a). In 60% of cases, infection is asymptomatic and many people are unaware that they’re even infected (g). The parasite does its worst damage among immunocompromised patients, either as a primary infection or as a recrudescent infection, and is a dangerous complication for those who are HIV-positive. Congenital transmission in which a woman becomes infected during pregnancy is also of public health concern. A newborn exposed in utero may be born with profound neurological and ocular sequelae, such as microcephaly, deafness, retina damage and mental retardation (g). Spontaneous abortion or stillbirth may also be another heart-wrenching outcome of primary toxoplasmosis.

T. gondii oocysts in a fecal floatation. Image: CDC. Click for source

A great literature review by Pappas et al. examined worldwide seroprevalence levels to craft a global epidemiological picture of the disease. Click here to check out the map. Prevalence of the disease was found to be highest in Europe and South America and may be attributed to a greater consumption of undercooked meats (b). Most infectious diseases are geographically limited to specific locales due to their climatic requirements, access to intermediate hosts and other factors. The most interesting aspect of toxoplasmosis is that these little buggers can be found everywhere in pretty much every population group of humans studied! Toxoplasma is a remarkably adaptive and successful parasite, and not only because of its ubiquitousness – it also keeps its hosts alive (for the most part) instead of scrambling our brains by provoking an inflammatory immune response.

An intriguing hypothesis is that infection can bring about personality and behavior changes (k). T. gondii is neurotrophic and exhibits a particular preference for the glial cells that provide support to the brain’s neurons. That toxoplasmosis may modulate human behavior is fascinating in itself as it’s already been proven with rodents; rats infected with the parasite show behaviors associated with decreased anxiety and neophobia, as well as increased levels of aggressiveness (d). Such marked changes have been interpreted as the parasite increasing the rodent’s risk of cat predation, adapting to its intermediate rodent host by enhancing the likelihood of transmission to its definite feline host (d). The mechanism is unclear but many speculate that the parasite’s location in such a privileged spot in the brain may affect neuro-immunomodulation and neurotransmission (f). Sneaky stuff.

So consider this: Toxoplasma may also affect its human host’s behavior so as to enhance the parasite’s transition to its definite host in the cat. In other words, the parasite may be manipulating how we think and act to maximize the possibility … of our brain being eaten by our feline friends.

Of course no such thing happens. But indeed, there are a few studies that have found correlations between toxoplasmosis and changes in personality profiles. One such study conducted in 2000 by Flegr et al. used Cattel’s 16 Factor Questionnaire, a self-reported personality profile survey, to look at differences in personality traits amongst acute and latent toxoplasmosis patients. Both stages of the disease were correlated with increases in warmheartedness, outgoingness, easygoingness and high will-power in women, while the same factors were associated with decreases in men (d). Infected women are more likely to respect social rules, be amicable, attentive and loyal to others than women who are uninfected; infected men are more introspective, suspicious and have low self-esteem (g). Both women and men score higher for levels of anxiety than those uninfected (d)(g). Women seem to luck out with toxoplasmosis, whereas men turn into something like a jealous ex-boyfriend stalking you on Facebook.

Light micrograph of a cyst containing T. gondii parasites (stained red) in brain tissue. Thousands of resting parasites can be seen enveloped by the thin parasite cyst wall. Image: Science Photo Library. Click for source.

I read these results and am hesitate to fully endorse them. Don’t get me wrong, it’s a neat idea. Brain zombies? I’m totally there! But maybe this is the molecular biologist in me, reluctant to believe self-reporting psychological surveys. These ideas of behavior and personality modulation are also pretty controversial. And, of course, there’s the issue of correlation versus causation. Does toxoplasmosis cause a change in one’s personality or does a type of personality (say, a Brazilian cat-lover who is fond of undercooked pork) predispose one to infection with toxoplasmosis?

The researchers claim that the fact that identical personality changes can be seen in both the acute and latent cases serve as an indication of the persistence of the parasite’s effect. In another study by Flegr that looked at infected women over the course of fourteen years, he claimed that the high anti-Toxoplasma antibody titre seen in these patients reflects the long-term duration of the infection and can thusly be attributed to long-term personality shifts (d). However, IgG antibody levels typically level off in chronic infections due to a reduction in antigenic stimulation as the parasite settles down into its new human home (i). Does the parasite permanently change a person’s personality upon acute infection or does it continually modulate it over time? There’s a lot of questions raised in the paper but, as a thought experiment, it’s an interesting read.

In a similar vein is an article written by Kevin Lafferty that uses Flegr’s results. In “Can the common brain parasite, Toxoplasma gondii, influence human culture?” Lafferty speculates that the personality profiles resulting from toxoplasmosis, with increased feminine qualities in women and more masculine ones in men, may explain “greater differentiation of sex roles” in countries with rigid gender norms (e). The relationship between toxoplasmosis and the common personality profiles of a population may explain some aspects of the “personality” of a culture, in particular gender roles and expectations (e). You can find it here. More thought experiment stuff, really.

So. Brains. Toxo. What to make of it? There’s a wealth of research and reviews out in Pubmed-land that look at behavioral and mental disorders and the prevalence of toxoplasmosis infection. Schizophrenia and epilepsy are the two main neurological disorders that seem to continually be coincident with toxoplasmosis (g). Of course, everything will boil down to the boxing match between correlation vs. causation, as well as the incontrovertible fact that infection, mental disease, personality and the reason why people like cats (no, seriously, why?) result from a multitudinous array of factors – genetics, history, culture and culinary taste – that probably have nothing to do with this parasite. But maybe that steak should be more on the medium rare side, hmm? It’s food for (neuromodulated) thought!

Resources

T. gondii is one of those crazy protozoan parasites with complicated life cycles. I greatly simplified the details and you should go to the CDC site to get more info about the biology and such.

If you’re curious about that Cattel 16 Factor Questionaire, you can take a look at it here.

References

(a) Despommier, D, Gwadz RW, Hotez PJ and Knirsch CA. Parasitic Diseases. 5th ed. New York: Apple Trees Production, LLC. 2006
(b) Pappas G, Roussos N & Falagas ME. (2009) Toxoplasmosis snapshots: Global status of Toxoplasma gondii seroprevalence and implications for pregnancy and congenital toxoplasmosis. Int J for Parasitology. 39:1385–1394
(c) Flegr J, Zitková S, Kodym P, Frynta D. (1996) Induction of changes in human behaviour by the parasitic protozoan Toxoplasma gondii.  Parasitology. 113 (Pt 1):49-54
(d) Flegr J, Kodym P, Tolarová V. (2000) Correlation of duration of latent Toxoplasma gondii infection with personality changes in women. Biol Psychol. 53(1):57-68
(e) Lafferty KD (2006) Can the common brain parasite, Toxoplasma gondii, influence human culture? Proc Biol Sci. 273(1602): 2749-55
(f) Fekadu A, Shibre T, Cleare AJ.  (2010) Toxoplasmosis as a cause for behaviour disorders–overview of evidence and mechanisms.  Folia Parasitol (Praha). 57(2): 105-13
(g) da Silva RC, Langoni H. (2009) Toxoplasma gondii: host-parasite interaction and behavior manipulation. Parasitol Res. 105(4):893-8 Epub
(h) Aspinall TV, Marlee D, Hyde JE, Sims PFG. (2002) Prevalence of Toxoplasma gondii in commercial meat products as monitored by polymerase chain reaction—food for thought? Int J Epidemiol. 32:1193–1199
(i)Remington JS and R McLeod. Toxoplasmosis. Infectious Diseases in Medicine and Surgery (3rd Edition). J Bartlett, S. Gorbach, N Blacklow (Eds). Lippincott Williams & Wilkins: Philadelphia, 2003
(j) Daryani A,  Sharif M, Hosseini SH, Karimi A and Gholami S. (2010) Serological survey of Toxoplasma gondii in schizophrenia patients referred to Psychiatric Hospital, Sari City, Iran. Tropical Biomedicine. 27(3): 476–482

This post was chosen as an Editor's Selection for ResearchBlogging.org
Flegr J, Kodym P, & Tolarová V (2000). Correlation of duration of latent Toxoplasma gondii infection with personality changes in women. Biological psychology, 53 (1), 57-68 PMID: 10876065