Risk Factors for Human Cystic Echinococcosis in Latvia

Introduction

E chinococcus granulosus (sensu lato [s.l.]) are tapeworms with lifecycles involving definitive hosts (dogs and other carnivores) and intermediate hosts (e.g., sheep, pigs, and moose). Humans may become accidental hosts by ingesting E. granulosus eggs, and develop a disease, cystic echinococcosis (CE). CE, characterized by fluid-filled cysts, is a chronic life-threatening disease (reviewed by Possenti et al. 2016, Kern et al. 2017). E. granulosus was recently ranked as the second most relevant zoonotic foodborne parasite in Eastern Europe (Bouwknegt et al. 2016). At the global level, E. granulosus also ranked second among zoonotic foodborne parasites, and it causes a high disease burden (Budke et al. 2006, Torgerson and MacPherson 2011, FAO/WHO 2014, Kern et al. 2017, Tamarozzi et al. 2018).

Human infections with E. granulosus are linked to behavior enabling direct contact to and ingestion of the eggs of the parasite, which are present in the feces of infected definitive hosts (MacPherson 2005). Previous studies have revealed that the risk factors for human E. granulosus infection include presence of dogs, easy access of dogs to offal of infected livestock, insufficient anthelmintic treatment of dogs, raising livestock, and unregulated home slaughtering of livestock (Campos-Bueno et al. 2000, Eckert et al. 2000, Shaikenov et al. 2003, Romig et al. 2006, Bružinskaitė et al. 2009, Rojo-Vazquez et al. 2011, WHO 2011, Brundu et al. 2014, Marcinkutė et al. 2015).

Since the 1990s, a rise in the number of registered human CE cases has been observed in two Baltic countries, Latvia and Lithuania (Marcinkutė et al. 2015). The data available indicate that in the Baltic countries, CE is often diagnosed at a rather late stage, whereas little is known about risk factors for CE (Marcinkutė et al. 2015).

The aim of this study was to compare the frequency of selected potential risk factors in individuals diagnosed with CE and matched control individuals in Latvia.

Materials and Methods

Results

The age of the cases at the time of answering the questions ranged from 24 to 84 years (mean, 57.3 years, and median, 57 years). The majority (69.6%) of the cases were women.

We focused on questions about plausible risk factors for infection with E. granulosus (s.l.) (Table 1). The number and proportion of cases and controls who selected specific answers for the selected risk factor questions are shown in Table 1. Living in rural dwelling, owning dogs kept or roaming outdoors, owning dogs fed with viscera of livestock, having close contact with dogs or cats, owning livestock, home slaughtering, and having hunters in the family were significantly more common among cases than among controls. The proportions reporting owning dogs dewormed irregularly or never, picking mushrooms, picking forest berries, and having a kitchen garden were not significantly different.

Furthermore, because having close contact with dogs or cats was among the factors that were more common among cases than among controls, we analyzed cat-related questions of the questionnaire. Owning cats kept or roaming outdoors was significantly more common among cases than in controls (36/46 vs. 27/46, 78.2% vs. 58.7%, p value 0.04783).

Discussion

This study identified several factors as more common in cases, individuals with diagnosed CE, than in matched controls, which adds to the limited information available on relevant risk factors for CE in northeastern Europe (Marcinkutė et al. 2015). The results will help in targeting preventive measures and planning further studies.

Because dogs can play a role in the transmission of helminthic zoonotic agents, including E. granulosus (Deplazes et al. 2011; Otero-Abad et al. 2013), we had a special focus on questions about dogs (Table 1). Owning dogs kept or roaming outdoors was significantly more common among cases than among controls (Table 1). Dogs allowed to roam free may have possibilities of finding and ingesting raw offal of infected animals, and their feces may not become collected from the environment. The environmental contamination might also explain why owning cats allowed to roam outdoors appeared associated with being a case, despite domestic cats are not considered epidemiologically relevant hosts for E. granulosus (Bonelli et al. 2018). It can be speculated, for example, that cats with canine fecal contamination on their fur could transmit the eggs of the parasite closer to humans.

A result worth emphasizing was that owning dogs fed with viscera of livestock was more common among cases than among controls. This feeding practice is deliberately helping the lifecycle of the zoonotic parasite.

Living in rural dwelling, owning livestock, and home slaughtering were more common among cases than among controls (Table 1). As humans cannot acquire the infection directly from the intermediate hosts, these risk factors are indirect, likely linked to dogs. Local lifecycle of the parasite is supported if dogs are fed or allowed to eat raw offal of infected animals, especially as it is an apparently common practice to deworm dogs irregularly or never (Table 1), and if the feces of the dogs are allowed to contaminate the environment, feed, or water of livestock. Indeed, an on-farm transmission pattern related to home slaughtering tradition may have a major role in the epidemiology of E. granulosus in the rural environment in this region (Marcinkutė et al. 2015). Previous studies on E. granulosus in livestock in Latvia showed relatively low prevalence estimates in cattle (0.001–0.11%), sheep (0.005–0.2%), and pigs (0.002–0.2%) (Marcinkutė et al. 2015), whereas studies in the neighboring country Lithuania reported that 13.2% (81/612; 95% CI 10.7–16.2) of pigs that originated from family farms were infected with E. granulosus, and that 3.8% of dogs in the villages were infected with E. granulosus (Bružinskaitė et al. 2009). The lifecycle of E. granulosus (pig strain) appears well established in Lithuania (Marcinkutė et al. 2015), whereas it remains understudied in Latvia.

Cases had hunters in their family more commonly than controls did. Hunters and their households might be a subpopulation at higher risk for CE that has received little attention. In the northernmost Baltic country Estonia, as part of a larger study on zoonotic parasitic infections, 1 (0.7%, 95% CI 0.0–3.4) of 144 hunters tested seropositive for Echinococcus spp. using a commercial ELISA (Lassen et al. 2016). In particular, hunters might be more exposed to Echinococcus canadensis (Oksanen and Lavikainen 2015, Romig et al. 2015). In Latvia and Estonia, E. canadensis has been found in 2.6% and 4% of investigated wolves (Canis lupus), respectively (Bagrade et al. 2009, Moks et al. 2009), and a relevant intermediate host species is moose (Alces alces), which is hunted for human consumption. Although exposure to eggs present in the feces of infected wolves could be a possible infection route to humans, picking mushrooms and forest berries that indicate exposure to the forest environment were not significantly more common among cases than among controls. The role of dogs may be important in the spillover from the sylvatic cycle of E. canadensis (Hämäläinen et al. 2015). Dogs could acquire the infection by eating raw viscera of infected, hunted moose, and the feces of infected dogs, if not collected and appropriately disposed of, may contaminate the environment shared with humans.

The strengths of this study include its setting in a country where Echinococcus spp. are of importance, but where major data gaps about the locally relevant risk factors for the human disease they can cause have hampered planning preventive measures. The main limitations of this study were the retrospective study design and the limited number of cases and controls. Moreover, it is important to stress that the diagnoses were based on combination of serology and diagnostic imaging, but further medical details were not considered and the diagnoses were not confirmed by the authors of this study. In particular, the parasite species/strain-level diagnoses were not reached. To avoid including asymptomatic CE in the control group, we only included persons who had undergone abdominal ultrasound examination without pathological findings. The reasons for performing the ultrasound were not evaluated, and this control group may not represent the general public well. The controls were matched to mirror the gender distribution, geographical distribution, and exposure time (age) of the cases; this study could not investigate these aspects as potential risk factors. Given that the time period between infection with E. granulosus and the diagnosis of CE can be long, it remains unknown when the diagnosed infections were acquired, and identifying risk factors retrospectively is also challenging.

The results of this study can inform planning of preventive measures, whereas parasite species/strain-level diagnoses would help in targeting them more specifically. Current E. granulosus (s.l.) control efforts predominantly focus on the control of dog populations, regular administration of praziquantel to dogs, improved control of slaughter, and health education (Eckert and Deplazes 2004). The results of this study offer support to focusing on these aspects in the preventive measures also in Latvia.

Conclusions

In this study, we identified several factors as more common among cases, individuals with diagnosed CE, than among matched controls. The recognition of risk factors has a critical importance on the improved prevention and control of CE in humans. The results of this study suggest that preventive measures in Latvia should focus on the role of dogs. Species/strain-level diagnoses of the human infections are needed to enable more specific studies and more targeted preventive measures.