A Nationwide Seroepidemiologic Study on Q Fever Antibodies in Sheep of Portugal

Introduction

Qfever is an almost global zoonotic disease caused by Coxiella burnetii, which is able to infect several animal species and of which cattle, sheep and goats are the primary animal reservoirs (Van den Brom et al. 2015, Khor et al. 2018). Q fever in humans can produce acute disease that usually leads to pneumonia, hepatitis, and self-limited illness (Guatteo et al. 2011). Chronicity is associated to endocarditis in immuno-compromised individuals or abortions and stillbirths in pregnant women (Angelakis and Raoult 2010, Dabaja et al. 2018). Human infection occurs by C. burnetii-contaminated aerosols of animal origin that are inhaled (Guatteo et al. 2011). Although rare, oral transmission by consumption of contaminated dairy products is also possible as is also sexual and vertical transmission (Kruszewska and Tylewska-Wierzbanowska 1997, Milazzo et al. 2001). Though almost neglected in the past, recent outbreaks have alerted the public and the scientific community (van der Hoek et al. 2010). In The Netherlands, a large outbreak affecting 2357 human cases that lasted several years was notified in 2009 and linked to abortion waves on dairy goat flocks (van der Hoek et al. 2010). In fact, Q fever in small ruminants (sheep and goats) is associated with vast shedding of bacteria in placentas, feces, milk, and birth fluids, and usually manifest as abortions, which greatly increases the risk of disease spread (O'Neill et al. 2014, Filioussis et al. 2017).

In the Iberic Peninsula, very few regional studies on Q fever in ruminants have been made (Anastácio et al. 2013, Cumbassá et al. 2015), and no serologic survey in the full continental territory Portugal has ever been done. Hence, an epidemiologic survey was set up to estimate the seroprevalence of Q fever antibodies in sheep of all regions of Portugal.

Materials and Methods

Results and Discussion

The presence of anti-C. burnetii antibodies was found in 122 sheep, which represents a 11.4% (95% CI 9.6–13.5) seroprevalence of IgG anti-C. burnetii in sheep of Portugal. Of these 122 positive sheep, 53 (43.4%, 95% CI 34.5–52.7) were considered low positive and 69 (56.6%, 95% CI 47.3–65.5) considered strong positive. Regarding the distributions according to regions, anti-C. burnetii were found in 18 of 161 sheep of the North of Portugal (11.2%, 95% CI 6.8–17.1), of which 7 (38.9%; 95% CI 17.3–64.3) were low positive and 11 (61.1%, 95% CI 35.7–82.7) were strong positive; in 44 of 246 sheep of the Center of Portugal (17.9%, 95% CI 13.3–23.3), 13 (29.5%, 95% CI 16.8–45.2) were low positive and 31 (70.5%, 95% CI 54.8–83.2) were strong positive; in none of the 21 sheep from Lisboa and Vale do Tejo (0%, 95% CI 0.0–0.0); in 59 of the 616 sheep of Alentejo (9.6%, 95% CI 7.4–11.9), 32 (54.2%, 95% CI 40.8–67.3) were low positive and 27 (45.8%, 95% CI 32.7–59.2) were strong positive; and only 1 of the 24 sheep of Algarve (4.2%, 95% CI 0.1–21.1) was considered low positive (100%, 95% CI 2.5–100) (Table 1; Fig. 1). The seroprevalence found in Portugal, even considering individual regions, appears to be within the low ranges when comparing with the seroprevalence observed among sheep in the neighboring country of Spain, reported to be from 9.8% in the Basque country (northern country) to ∼30% in the islands of Canarias, considered a highly endemic region (García-Pérez et al. 2009, Rodriguez et al. 2010, Ruiz-Fons et al. 2010, Fernández-Aguilar et al. 2016, Bolaños-Rivero et al. 2017). In fact seroprevalence in sheep is estimated to be around 15–20% in many countries of the world (Guatteo et al. 2011), which confirms that sheep of Portugal showed relatively low Q fever seroprevalence.

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FIG. 1.

Percentages of anti-Coxiella burnetii seropositive sheep in the five NUTS II regions of continental Portugal.

When comparing anti-C. burnetii presence in sheep according to NUTS II distribution, a higher seroprevalence in the Center region can be observed when comparing to the other regions of Portugal. Unlike the regions south of the Center region (Alentejo, Lisboa, and Vale do Tejo and Algarve) that have vast flat plains and low density extensive husbandry systems, the North region has a highly irregular mountainous terrain (favoring intensive husbandry) and the Center has a mixture of hills and mountains that transition to plains to the south (Tibério and Dinis 2014). This terrain profile shifts from mountainous to plains in the Center region and favors semi-extensive husbandry systems, where sheep are housed during the night and are allowed movement during the day (Fraga et al. 2014, Tibério and Dinis 2014). The semi-extensive husbandry that allows use of common pasture by sheep during the day can favor infection by spore-like forms that are deposited in the soil and have a long survival time, helping explain the increased anti-C. burnetii seroprevalence in this region. Also from a climatic standpoint the country presents a relatively large set of mesoclimates, spanning from dryer in the Southern regions, to more humid and windy in the North and Center regions (Santos et al. 2012). This windy climate in the Center region may also favor C. burnetii airborne dispersion and transmission in the outdoor environment and help explain the increased seroprevalence in this region, when compared to the remaining regions of Portugal.

To this moment only one sheep seroprevalence study has been performed in Portugal, collecting blood from 2011 (Anastácio et al. 2013). In that study, the global individual seroprevalence was 8.6% and animals belonged to the Center region of Portugal, which is lower than the seroprevalence detected in this study for that region and may indicate an increasing circulation of C. burnetii. However, caution must be taken in this comparison since different enzyme immunoassays were used along with different sampling designs.

In conclusion, this is the first nationwide seroepidemiologic study that surveyed Q fever in sheep in Portugal also profiling the distribution of seropositive animals according to regions. Although seroprevalence seems low, the agent appears to be distributed across the country and hence alerts for the possibility of zoonotic transmission have to be made. Moreover, sheep traditional farming is widely present in Portugal and is part of the cultural and gastronomical background of the country. This close proximity to small ruminants may contribute to the zoonotic transfer to humans. Although preliminary results from this study show relatively low Q fever seroprevalence in Portugal, there is the need to provide a clearer understanding of C. burnetii epidemiology in Portugal. Implementing monitoring programs on sentinel herds may help prevent or mitigate the effects of potential epidemics.