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

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.

A Turkana woman. Her heavy beaded necklaces, braided mohawk, lip piercing and large leaf-shaped earring are traditional attire for the women of the tribe. Image: from the Cudahy-Massee Expedition. Click for source.

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.

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

Buzz Kill: Blood-Borne Disease Transmission at the Hajj

With Hanukkah and Christmas just recently past and Chinese New Year fast approaching, it seems a suitable time to consider the topic of religious celebrations and infectious diseases, no? ‘Tis the spirit and all! I’ll be looking at one of most intriguing religious events in the world, the Islamic pilgrimage to Mecca known as the Hajj, and the special epidemiological event that accompanies it.

The Hajj is a powerfully sacred and social event for Muslims. The importance of the pilgrimage to the Saudi Arabian desert city and the communal celebration of the prophet Muhammed cannot be understated – it’s a profoundly holy journey and religious duty that every Muslim is urged to complete at least once in their lifetime. It is also unique from an epidemiological standpoint: two to three million people from 70 countries meeting in one tiny place is the siren call for respiratory, water-borne and blood-borne microbial diseases.

A Muslim praying at the Hajj with a backdop of thousands of pilgrims. Image: Hassan Ammar. Click for source.

So what does the Hajj consist of exactly? Depending on the lunar calendar, the Hajj may occur any time of the year; last year, the week-long event fell between November 4th to the 9th. The pilgrimage involves a series of performative rites that must be completed in the city of Mecca and its environs; these rites serve as a reenactment of the key historical events underpinning the birth of Islam. On the first day of the Hajj, pilgrims will walk counter-clockwise seven times around a rectangular building named the Kaaba located at the very center of Mecca. The Kaaba serves as an orientation point for Muslim prayer rituals and is considered the physical and spiritual nucleus of the Islamic religion. Pilgrims, also known as Hajjees will then run back and forth between the hills of Al-Safa and Al-Marwah a total of seven times and will end their day by drinking water from the holy Zamzam well.

A map showing the Hajj route and procession taken by pilgrims. Image: Creative Commons.

The second day is spent in vigil, praying to Allah and reciting the Quran at the granite hill of Mount Arafat, located just southeast of Mecca. The following day, pilgrims will gather in the thousands to perform a ritual enactment of the Stoning of the Devil by throwing pebbles at the three pillars of Jamarat in the small town of Mina. They then leave this area to shave their heads, perform a ritual animal sacrifice and go on to celebrate the religious holiday of Eid al-Adha. Their spiritual marathon is finally complete.

During this pilgrimage, Hajjees live in a spiritual state of purity called Ihram. Prior to entering this condition, pilgrims will ritually cleanse themselves, trim their nails and remove any unwanted body hair. From then on, men are dressed simply in two sheets of unstitched white cotton and a pair of plain sandals. Women wear the hijab, with their face and hands exposed. In this sanctified state, Hajjees are forbidden from shaving, trimming their nails, wearing scented toiletries, arguing or swearing along with a few other unbecoming behaviors.

The experience can be difficult for the heat-susceptible, agoraphobic, the frail or very young; Mecca during the Hajj is often stifling hot, humid and beyond overcrowded. Performing the rites  with millions of other people over a wide geographical area can be physically strenuous and quite exhausting. There have been several recorded cases of fatal stampedes and crowd crushes during the jam-packed Stoning of the Devil, sunstroke and heat exhaustion are not uncommon, cholera outbreaks have historically plagued pilgrims, and pneumonia, meningitis and food poisoning have repeatedly occurred. Really, it goes without saying that if millions of international travelers converge in one city for a physically active, overcrowded affair, one should consider oneself lucky not to catch a respiratory or diarrheal bug.

You certainly wouldn’t expect to come down with a blood-borne transmitted virus and nasty chronic disease.

Regrettably, that scenario may not be that unlikely for male pilgrims on the verge of exiting Ihram; contracting HIV or any of the unsavory gang of hepatitis viruses such as hepatitis B, C or D (HBV, HCV or HDV) is quite possible due to the unseemly practice of communal shaving.

A pilgrim bleeding while being shaved at the end of Ihram. Note the bare hands. Image: Unknown. Click for source.

Following the Stoning of the Devil and the completion of their religious rites, Hajjees migrate to Mina where hundreds of barbers await with razor blades to shave the scalps of male pilgrims and where women will trim a finger-length lock of hair. This last ritual seals the deal, so to speak, allowing pilgrims to compete their observance of the Hajj. Saudi officials require all barbers to be licensed though makeshift barbers still abound, waiting on roads for eager pilgrims with razors in hand (1). Pilgrims may also buddy up to shave each other’s scalps. These unlicensed barbers and pilgrims can often be found reusing unsterilized blades to communally head-shave Hajjees, a fabulous technique for transmitting blood-borne diseases (BBDs).

Indeed, physicians associated with the Saudi Arabian Field Epidemiology Training Program describe the practice of communal head-shaving at the Hajj as an ‘optimum focal setting for the spread of serious BBDs’ (2). There’s a considerable amount of hair-raising unhygienic behaviors going on – not only are unsterilized razors reused on multiple individuals, barbers often do not wear gloves, incur many abrasions on their hands and dispose of the razors improperly.

Only a few studies have looked at the demographics and practices of these barbers but they have yielded some insightful data. A study in 1999 examined 158 barbers recruited from makeshift shaving sites near Jamarat. Eight nationalities were represented but the majority stemmed from three impoverished countries – 72 from Myanmar, 27 from Egypt and 22 from Bangladesh. Most interestingly, two-thirds of the barbers worked seasonally. They were not licensed professionals, but rather opportunistic seasonal workers that had worked at the Hajj for a median of two to five years (2).

The barbers reported each shave as lasting roughly two to ten minutes (3); these rapid-fire, assembly line-like operations can increase the likelihood of accidental nicks and grazes. Twenty-one percent of barbers report using a blade more than once (3). When razors are finally disposed of 83% will discard them on a ground densely covered in shorn hair instead of in the rubbish bins provided by Saudi authorities (3). This is of crucial consequence considering the numbers of pilgrims who are barefoot or wearing sandals. The head-shaving event also occurs in a very short time-frame overall, within a few hours in a circumscribed geographical area, compounding the likelihood of a BBD swap meet.

The eye-opening video below shows some of these seasonal barbers at work.

Around 90% of male pilgrims will have their scalps closely shaved (4). And pilgrims do indeed get nicks and abrasions: two separate studies found roughly 60% of Hajjees incurred scalp cuts (5)(6). There aren’t any studies examining the incidence or rate of BBD transmission among pilgrims during the Hajj so we’re unable to know how frightful of a problem this is. But consider this: many pilgrims come from regions of the world with high endemicity of BBDs such as Pakistan, Nigeria, Egypt and Turkey (2)(3)(5). And there are barbers working at the Hajj who have tested positive for BBDs – a study conducted in 1999 found that 10% tested positive for HCV and there was a positive correlation between barbers infected with HCV and the length of time they had worked at the Hajj (5). Though the epidemiological data is thin on what could actually is going on here, we can still state with some certainty that razor recycling shouldn’t be going on.

Hepatitis viruses are patient predators. They’ll stake out on bloody scalpels, syringes and surfaces for four days (HCV) or up to a week (HBV) until an open wound allows them to slink into a new body (7). It is for this very reason that Hepatitis B was one of the most commonly acquired infections in hospitals among medical personnel before the advent of the hepatitis A/B vaccine. When razor are used frantically and repeatedly to shave pilgrim’s heads, accidents will naturally happen. Skin catches on the blade. A microscopic cut, a slight nick and a drop of blood beads. Maybe in the hubbub, in the physical and spiritual heat of the moment, a barber grazes his bare hands and fingers on that pilgrim’s blood droplet. Or accidentally smears his own fresh blood, precipitated by a slip of the blade on an earlier scalp. The blood blends, indistinguishable from the other. Was that barber or pilgrim infected; did a virus slip between the two? In any case, another eager, awaiting Hajjee sits down for a shave and the razor is used again. This happens over and over and over, until the razor blade is finally deemed blunt and useless.

A public health poster in a Saudi Arabaian hospital warning pilgrims of the dangers posed by shaving during the Hajj. Image: Uknonwn. Click for source.

It’s a perverse tragedy that pilgrims exiting a state of profound spiritual and physical holiness may find their very blood contaminated by a barber with unhygienic practices. Pilgrims can become infected with a fatal illness that is clinically asymptomatic in its early stages only to fly back home to their communities oblivious of their condition. Catching the flu or pneumonia at the Hajj is one thing but bringing home a deadly viral illness is quite another.

Clearly the provision of safe razor blades, screening and supervision of barbers and widespread education on this matter are desperately needed. In a study from 1998, 74% of Hajjees and 20% of barbers were unaware that diseases could be transmitted by used razor blades (3). Many pilgrims expressed more concern about the spread of visible skin diseases than anything else. The invisible nature of BBDs only helps to further conceal the potential for a BBD micro-epidemic at the Hajj.

Consideration of the provision of housing, sanitation and overall public health of these religious visitors is of enormous importance for Saudi Arabian officials planning for the Hajj, and they do a phenomenal super-human job of keeping millions of people safe and cared for by providing free health care, organizing the festivities and what not. Seven hospitals have been established to provide free medical services and can supply over 2000 beds for those requiring hospitalization (6). The Ministry of Health establishes infection control policies using current knowledge of ongoing global outbreaks, infectious disease epidemiology and established preventative medicine techniques (1)(5). By all accounts, they did a great job during the H1N1 flu pandemic in 2009 by requiring pilgrims to have flu shots, restricting visas for pilgrims from affected countries, setting up thermal sensors at airports to detect the feverish and deploying thousands of physicians throughout the pilgrim circuit (9). They also require all entering pilgrims to display certificates of vaccination for hepatitis A/B, meningococcal meningitis and yellow fever.

A pilgrim recieving a shave in a sanctioned barbershop during the Hajj. Image: Unknown. Click for sourece.

But keeping an eye on rogue unlicensed barbers can be difficult for officials considering the high crowd density and activity. Whatever may be the case, the seriousness of the matter can’t be ignored. A vigorous public health campaign as well as a serious crackdown on these barbers is needed in order to halt this hairy business. It’s been noted before that an epidemic of the flu, meningitis or cholera could easily bloom into a pandemic at the Hajj. Even so, the prospect of a multinational epidemic of BBDs spread by irresponsible hygiene practices is appalling. A hair-raising thought, indeed.

Recommended Reads

The hepatitis family, particularly the members B, C and D, is some real nasty shit. I didn’t go into any detail about their molecular biology but if you’re interested, please go here.

Go here to see the vaccinations required by the Saudi Ministry of Health for all visiting pilgrims.

For a list of every single conceivable disease you could catch during the pilgrimage, check out this baby.

An extremely helpful guide to how to handle oneself at the Hajj.

References

(1) ZA Memish. (2002) Infection control in Saudi Arabia: Meeting the challenge. Am J Infect Control. 30(1): 57-65
(2) The  Saudi Arabian Field Epidemiology Training Program (2000) Blood-Borne Diseases Among Barbers During Hajj, 1419 H (1999). Saudi Epidemiology Bulletin: 7(1). Accessed online on Dec 10, 2011. Link.
(3) Saudi Arabian Field Epidemiology Training Program (1998) Head-shaving practices of barbers and pilgrims to Makkah, 1998 Saudi Epidemiology Bulletin. 5(3): 18-19
(4) SM Rafiq, H Rashid, E Haworth & R Booy. (2009) Hazards of hepatitis at the Hajj. Travel Med Infect Dis. 7(4): 239-46
(5) Rashid H & Shafi S. (2006) Blood borne hepatitis at Hajj. J of Hep Mon. 6(2): 87-88
(6) Alrabeh AM, El-Bushra HE, Al-Sayed MO, et al. (1998) Behavioral risk factors for disease during Hajj: the second survey. Saudi Epidemiol Bull. 5(3). Accessed online on Dec 10, 2011. Link.
(7) CDC; Division of Viral Hepatitis. (2009) Hepatitis B FAQs for the Public. Accessed online on January 4, 2012. Link.
(8) Omar Sacirbey, 2009, Will flu epidemic slow the Hajj? Chron.com (Online). Accessed online on Dec 10, 2011. Link.

Memish ZA (2002). Infection control in Saudi Arabia: meeting the challenge. American journal of infection control, 30 (1), 57-65 PMID: 11852419