Cystic echinococcosis in Turkana, Kenya: 30 years of imaging in an endemic region

Abstract

Cystic echinococcosis (CE), a widespread, complex zoonosis, causes chronic disease associated with high morbidity. The pastoral Turkana people of Kenya have one of the highest prevalence rates of CE in the world. Between 1983 and 2015, a CE control program in the Turkana region used ultrasound (US) screening surveys and surgical outreach visits to evaluate CE prevalence and treat those with the disease. As the gold standard modality for diagnosing CE, US reveals a great deal of information about the disease in affected populations. The aim of this study is to discuss the characteristics of untreated CE in the Turkana people as revealed by US data collected during the CE control program and evaluate disease presentation, factors influencing the risk of transmission, and the timeline of disease progression. Data were obtained from written patient notes from US screenings and images; cysts were classified using the World Health Organization (WHO) standardized US classification of CE. Findings include greater prevalence of cysts, later stages of cysts, and multiple cysts in older age groups, with no multiple cysts occurring in patients under six years of age, which are consistent with the assertion that rates of exposure, transmission, and infection increase with age in endemic regions. Findings also raise questions regarding the timeline of disease progression, and factors potentially influencing disease transmission within this and other endemic populations. A comprehensive survey focusing on cultural and community observations (e.g., changing behaviors, hygienic practices, etc.) may provide more detailed information regarding factors that facilitate transmission.

Introduction

Cystic echinococcosis (CE) is a complex disease with a global distribution. Infection is acquired by humans ingesting the eggs of Echinococcus granulosus sensu lato (i.e. the species in general) leading to the development of cysts of varying composition (Thompson and McManus, 2001, Symeonidis et al., 2013). The most common location of cyst formation is in the liver, followed by the lungs; but cysts can occur in any organ or body tissue (Thompson and McManus, 2001, Kern, 2003, Symeonidis et al., 2013). In the majority of endemic areas, 60–75% of patients are asymptomatic (Belard et al., 2016), but CE can become complicated by cyst rupture, secondary parasitic or bacterial infections, or growth of the space-occupying cystic lesions which interferes with organ function (Pawłowski et al., 2001).

The advent of portable ultrasound (US) screening has allowed for more effective mass surveillance and evaluation of CE prevalence among human populations. Once the equipment has been purchased, cost per examination is inexpensive. CT and MRI were not available in this resource-limited region, and provide little if any clinical information that US cannot reveal (Macpherson et al., 1987, WHO-IWGE, 2003). In community-based US screening programs, US is attractive to patients due to its immediate results, and its being painless, non-invasive, and well-known to the local people with whom permanent records can be shared (Macpherson et al., 1987). This facilitated the rapid screening of all individuals present in the vicinity, providing representative age/gender prevalence data of US-accessible cases of CE.

In pastoral populations where livestock serve many purposes including cementing friendships and marriage and are rarely slaughtered for food, surveillance for infected offal is virtually impossible. For these reasons, surveillance for CE and evaluation of control program outcomes are more frequently conducted in human rather than livestock populations, an approach implemented in a number of regions, including parts of Argentina, Uruguay, Peru, and China (Larrieu and Frider, 2001, Macpherson et al., 2003, Larrieu et al., 2004, Craig and Larrieu, 2006, Larrieu et al., 2011). In these programs, US functions not only as a screening tool, but also as a non-invasive method of evaluating the typical clinical presentation of CE, including cyst sizes, locations, and stages (Cohen et al., 1998, Wang et al., 2001, Macpherson et al., 2003, Wang et al., 2003).

The Turkana people of northwest Kenya are transhumant pastoralists who seasonally migrate with their livestock depending on local climatic conditions (Macpherson et al., 1986, Eckert and Hertzberg, 1994. US screening for CE among this population began in the early 1980s (Macpherson et al., 1987). A mass community-based US and serological study, enrolling approximately one third of the population was conducted to assess the baseline prevalence of CE in the pilot control area, a 9000 km² region in north-western Turkana (Macpherson et al., 1983, Macpherson et al., 1984, Macpherson et al., 1985, Macpherson et al., 1987).

US and serological surveys conducted on resident Turkana from July to September 1985, screened 3553 of an estimated 8000–12,000 population, and revealed a combined CE prevalence of approximately 6.6% (extrapolated 6.5–9.4%), with an average cyst size of 80 mm in diameter (Macpherson et al., 1987). Analysis of US-detected cases only revealed a prevalence of 5.6%, with infection being approximately twice as common in women (6.9%) as men (3.5%) (Macpherson et al., 1989). These findings indicated that northwestern Turkana had one of the highest prevalence rates of CE in the world (Macpherson et al., 1986). Further analyses revealed that the most commonly infected organ in Turkana patients was the liver, and the majority of hepatic cysts were single and unilocular (Macpherson, 1983). Most cysts were between 100 and 200 mm in diameter (Macpherson, 1983). Cysts were described based on their numbers and compositions (single vs. multiple, unilocular vs. multilocular, etc.), but, as the WHO classification had not yet been developed, cysts were not classified by stage at that time and therefore the relationships between cyst stage as per the WHO classification and their associations with other cyst and patient characteristics, such as cyst size or age of patients, were not explored.

CE can be caused by different species of Echinococcus, whose organ predilection and impact on the clinical manifestations may differ (Alvarez Rojas et al., 2014). In Turkana, published data showed that, among 80 parasite samples from 26 subjects, approximately 85% of the samples were identified as E. granulosus sensu stricto (strains G1–G3) and 15% were identified as the E. canadensis G6/7 strain (Mutwiri et al., 2013).

The aim of this study is to explore the clinical presentation and characteristics of CE—including the stages, sizes, and locations of cysts—in the Turkana population, and deliberate on their implications regarding disease natural history, transmission factors, and timeline of disease progression. Determining patterns in clinical presentation specific to a population or region can highlight the need for additional investigations and identify targets for control efforts. Uncovering distinct patterns also facilitates comparison between populations with the same disease, improving understanding of the variations in disease presentation among different populations and the epidemiological factors contributing to these differences.