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 definite host, the dog. Dogs eat infected viscera, become infected with thousands of tiny tapeworms, 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 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 km^2 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 thankfully only briefly alluded to in the literature I researched (8).
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 (1)(4).
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” to 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.55Suppl: 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.
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
