The Ethiopian SORT IT Course Cysts and parasites in an abattoir in Northwest Ethiopia; an urgent call for action on “one health”

Introduction: Zoonotic parasitic infections such as echinococcosis affect cattle, sheep and goats by lowering quality of meat and hides as well as decreasing milk production. The burden of such diseases among humans is usually underestimated as they are difficult to diagnose. We used abattoir data to estimate the prevalence of zoonotic parasitic infections in animals. Methodology: Data from 2005-2018 was used from the registry of an abattoir in Northwest Ethiopia. Frequencies, proportions and trends over time were analyzed. Meat inspection was conducted by visualization, palpation and incision. Results: A total of 58,787 animals were slaughtered in the abattoir during the study period. These included 51,956 (88 %) cattle, 5,890 (10%) sheep and 941 (2%) goats. The detected parasites included Echinococcus in 12,334/58,787 (21%) and Fasciola in 10,551/58,787 (18%) animals. Echinococcus infection was highest among goats (267/941, 28%), followed by cattle (11,591/51,956, 22%) and sheep (476/5,890, 8%). Fasciolosis was detected in 9,877/51,956 (19%) cattle and 178/941 (19%) goats. The number of animals slaughtered strongly decreased over time from 8,405 in 2006 to 1,605 in 2018. However, the proportion of parasitic infections remained high with some fluctuations over the study period. Conclusions: Echinococcosis and fasciolosis were very common with one out of five animals slaughtered infected. This is of public health concern and needs urgent multi-sectorial efforts from stakeholders at the national and regional level for control of these diseases. One health program approaches may warrant the control of transmission to humans.


Introduction
Zoonotic parasitic infections are an important public health problem which require a one health approach strategy for control [1][2][3][4]. Transmission to humans occurs by ingesting parasites in contaminated food, water or soil and through direct contact with dogs, cattle or other domestic animals. In Ethiopia, the common practice of backyard slaughtering, high numbers of free-roaming dogs, lack of abattoirs proportional with the population and improper waste disposal of infected organs may all contribute to high levels of transmission [3]. Studies showed offal is easily accessible to scavenging dogs, cats and other wild carnivores [5].
Zoonotic parasites can cause huge economic losses through decreased productivity of animals affected, and through condemnation of infected organs such as livers, kidneys and meat. They may also decrease milk production, animal fertility and hide quality [6]. Diagnosis of zoonotic parasites in animals is usually done by post-mortem visual inspection, incision and palpation of the organs. This is systematically done for all animals slaughtered in abattoirs [3]. Commonly detected parasites include Echinococcus, Fasciola, and Taenia, of which Echinococcus is one of the nationally prioritized zoonotic diseases in disease control programs [7,8].
Based on abattoir reports, the prevalence of echinococcosis in animals in hyperendemic areas 54S ranges from 20%-95% [3]. In Ethiopia, there are small abattoir-based studies on a limited number of cattle, sheep and goats that show a prevalence range of echinococcosis from 6% in Central Oromia, Adama [9] to 53% in Hawasa [10]. Prevalence in North Gondar Zone was 21% [11].
In humans, infections with zoonotic parasites are characterized by an indolent manifestation, making them hard to diagnose even though they may be deadly. For example, diagnosis of Echinococcus in humans is often accidental, based on ultrasound examinations done for other clinical indications [3]. Therefore, prevalence data are likely a gross underestimation of the real burden of disease in humans. Abattoir-based animal studies may give indications about the risk of transmission to humans. The trend in prevalence can help determine whether the risk of transmission is increasing.
In this study we investigated the trend and prevalence of echinococcosis and other zoonotic parasitic diseases among animals in an abattoir in North Gondar zone in Ethiopia during the period 2005 to 2018.

Study design
A cross-sectional study using retrospective abattoir data from September 2005 to September 2018 was conducted.

General setting
Ethiopia is in the horn of Africa and has the second largest human population with the biggest livestock population on the continent. About 80% of Ethiopians have a mixed agricultural practice (both growing crops and raising livestock), while they also often have dogs to protect their farms. According to the Ethiopian Federal Ministry of Agriculture data, there are a total of 293 abattoirs in Ethiopia, with most slaughtered animals originating from the surrounding rural areas.
In recent years, a national program dedicated to one health has been established, prioritizing five zoonotic diseases. However, this program is not supported by the government and other organisations, and no solid publications have come out so far.

Specific setting
ELFORA abattoir is found in Gondar city, North Gondar zone which is located 727 km Northwest of Addis Ababa in Amhara Regional State. Studies showed that North Gondar is one of the endemic areas of echinococcosis with a prevalence of 21% [11]. The area has an altitude of 550 to 4,620 meters above sea level. The district comprises a livestock population of 1,936,514 cattle, 524,083 sheep and 682,264 goats [12]. The abattoir was established 40 years ago. It is the only abattoir in the North Gondar zone, providing services for Gondar city and its catchment areas. Cattle, sheep and goats are the three species of animals slaughtered in the abattoir.

Routine procedures
Routine abattoir meat inspections are conducted by veterinarians or trained inspectors. All meat inspection team members, including the butchers, take food safety, hygiene and food handling training regularly.
In slaughtered animals, the presence of any abnormalities as well as diseases like Echinococcus and other zoonotic parasites such as Fasciola, lungworm, and Taenia are checked. The examination includes the visceral organs (liver, lung, heart, spleen and kidney), carcasses, lymph nodes, heads, and tongues and is conducted by visualization, palpation and incision of each slaughtered animal. Any organ abnormalities or defects that are unsafe for human consumption will either be treated by chilling, condemned or buried. All parts of the animal should be kept together and Presence of cysts commonly measure 5 -10 cm and contain fluid. Some may reach up to 50 cm in diameter. They can be found in the lung, liver, kidney, heart, muscles, brain and even bones Presence of white or grey tissue, irregularly rounded and frequently honeycombed, or a gritty sound upon incision of the tissue with a knife 55S correlated for inspection before they are removed from the abattoir floor. All findings are routinely registered within the case registry [7] (Table 1).

Study animals
All cattle (bovine), sheep (ovine) and goats (caprine) slaughtered and registered at the abattoir during the study period were included.

Data collection and analysis
The routine meat inspection abattoir case registry was used as a source of data. Variables collected were the type of animal, sex, year, the presence and type of parasitic infections and other signs of parasitic infection. Data were double entered directly into Microsoft Excel version 10. Annual numbers of slaughtered animals and the number of animals with echinococcosis and other zoonotic parasitic infection were computed to show the occurrence, proportion and trend over the last 14 years. Stata version 15 was used to show the trend over time graphically among three species of slaughtered animals.

Ethical approval
Permission to conduct the study was obtained from Gondar ELFORA abattoir, Gondar, Ethiopia. Institutional ethics approval was received from the Ethiopian Public Health Institute (EPHI) in Addis Ababa, Ethiopia. The study was also approved by the Ethics Advisory Group of the International Union against Tuberculosis and Lung Disease, Paris, France.

Results
A total of 58,787 animals were slaughtered in the abbatoir from 2005-2018. Of these, 52,935 (90%) were male. Three species of animals were slaughtered in the abattoir; 51,956 (88%) cattle, 5,890 (10%) sheep and 941 (2%) goats. Data on goats was available only for four years (2005-2009). There was a decreasing pattern in the total number of animals slaughtered at the abattoir over the study period (Figure 1 and 2). However, the proportion affected by parasites remained persistently high (Figure 2 and 3).
Infection with other zoonotic parasites such as lungworm, Taenia and Tenicullos was uncommon. However, liver cirrhosis and calcifications in different tissues were commonly found and were increasing in the last four years (Figure 3).

Discussion
This is the first study reporting on zoonotic parasitic infections over a longer time frame in Ethiopia. The findings are alarming with one out of five slaughtered animals affected by echinococcosis or fasciolosis. Other evidence of parasitic infections such as liver cirrhosis and tissue calcifications were also common. Especially goats (28% and 34%) and cattle (22% and 38%) were highly affected by Echinococcus and Fasciola. Although a decline in prevalence was observed in 2014-2015, no clear reason for it could be identified. Furthermore, the decline was not sustained.
These findings are in line with findings from other smaller studies conducted in Ethiopia, which showed a prevalence of echinococcosis between 20-52% [11,[13][14][15]. A study conducted among cattle in North Gondar zone show a fasciolosis infection rate of 23% [16].
The persistently high prevalence of zoonotic parasitic infection over a long period indicates high levels of transmission in this region. Reasons for this are likely to be related to the common practice of backyard slaughtering and gaps in proper disposal mechanisms. There are no regulations enforced on disposal of animal leftovers, especially outside of the abattoirs. The high prevalence of parasitic infections among animals has significant implications for the risk of transmission to humans, especially in Ethiopia, where the majority of the population lives near both cattle and dogs.
With increasing urbanization, an increasing number of hotels and restaurants, high expansion of universities and boarding schools, we expected an increase in meat consumption and number of animals slaughtered every year at the abbatoir. However, our data surprisingly showed a declining trend in yearly slaughtered animals. This finding may indicate that consumers are conducting more backyard slaughtering rather than using the abattoir. A reason for this may be that the high rate of parasitic infections leads to increasing rejection rates of organs and meat at the abattoir and therefore, consumers might opt out from using the abattoir for fear of losing their product. Unhygienic slaughtering practices, improper disposal of infected organs and their subsequent consumption by dogs and cats are all likely to contribute to a vicious cycle of re-infection.
These findings call upon an urgent need for implementation of disease control against parasitic infections in the area. A strategic and sustainable one health approach program should be employed with multiple level interventions. We advise the following strategies: 1) all stakeholders need to be aware of the magnitude of the situation and integrate efforts for its control. 2) resources should be mobilized for a deworming campaign among cattle, sheep and goats as well as other domestic animals including dogs and cats.
3) use of slaughterhouses should be encouraged. Pastoralists should be compensated for their animals in case infected meat and organs are discarded. 4) backyard slaughtering should be discouraged, and waste disposal mechanisms should be improved. 5) raw infected organs should not be fed to dogs and cats to interrupt the transmission.6) health education on the risk of raw meat and milk consumption needs to be strengthened.
Our study was subject to a few limitations. Data taken from the routine abattoir meat inspection registry was limited, and therefore transmission hotspots and risk factors of infection could not be determined. Adding variables such as the specific address and characteristics of each animal to the registry can help answer these questions. Since parasitic infections were diagnosed by visual inspection and palpation only, findings may be subject to the skill of the meat inspectors and parasites that require other diagnostics may have been missed.

Conclusion
Zoonotic parasitic infections are very common in Northwest Ethiopia. High prevalence of echinococcosis, fasciolosis and other signs of parasitic infection persisted over a long period. These findings indicate a high risk of transmission to humans. A one health approach for disease control interventions should be employed urgently.