You are on page 1of 3

Small Ruminant Research 134 (2016) 62–64

Contents lists available at ScienceDirect

Small Ruminant Research


journal homepage: www.elsevier.com/locate/smallrumres

Short communication

Presence of Coxiella burnetii (Q fever) in goats on the Canary Islands:


Current status
María Teresa Tejedor-Junco, Margarita González, Juan Alberto Corbera, Carlos Gutiérrez ∗
Research Institute of Biomedical and Health Sciences, University of Las Palmas de Gran Canaria, 35413, Arucas, Las Palmas, Canary Islands, Spain

a r t i c l e i n f o a b s t r a c t

Article history: The Canary Islands have been considered as Q fever endemic territory for humans and livestock, but those
Received 15 August 2015 studies were carried out 20 years ago. In order to evaluate the current status of the disease in livestock,
Received in revised form 9 December 2015 a cross-sectional survey was performed evaluating 22 milking goat farms and 550 goats throughout all
Accepted 20 December 2015
the 7 Canary Islands. A questionnaire to collect epidemiological data was also included. Blood sera were
Available online 28 December 2015
analyzed using a commercial Q fever antibody ELISA test kit. The overall animal seroprevalence was
42%, with significant differences among the islands, their climate zones, and local particularities. These
Keywords:
findings would confirm the endemic character of the disease 20 years later and would indicate the need
Q fever
Coxiella burnetii
to implement an urgent control plan as well as surveillance measures by the Official Veterinary Services.
Goats © 2015 Elsevier B.V. All rights reserved.
Seroprevalence
Zoonosis
Canary Island

1. Introduction as sentinel animals given their higher seroprevalence and, on the


other hand, their higher census and economic importance for the
Q fever is widely distributed throughout the world with the Canary Archipelago. Results would serve as baseline for possible
exception of New Zealand (OIE, 2010). The etiological agent, Cox- control programs as well as for public health risk assessments.
iella burnetii, is a Gram-negative obligate intracellular bacterium,
adapted to thrive within the phagolysosome of the phagocyte.
Although Q fever is present in virtually all “animal kingdom”, 2. Materials and methods
including arthropods, the disease affects mostly humans, cattle,
2.1. Animals
sheep and goats (OIE, 2010).
The Canary Islands, a fragmented subtropical territory of the From February to June 2014, a cross-sectional survey was carried out to eval-
Spanish kingdom, are considered an endemic region of Q fever uate the status of Q fever in goats in all the 7 Canary Islands. Based on the insular
(Pascual Velasco et al., 1992). Some studies on human population census (Table 1) and geographic locations the islands were divided into group A
(lower than 20,000 goats), group B (20,001–50,000 goats) and group C (higher than
revealed an overall seroprevalence of 21.5% (Bolaños et al., 2003a),
50,000 goats). Twenty-two farms (according to two-stage cluster sampling method
and new clinical cases are reported annually on the islands (Bolaños -Thursfield, 2007-) were randomly selected, corresponding 2, 3 and 4 for the insular
et al., 2003b; Espejo et al., 2014). Concerning livestock, some sero- groups A, B and C, respectively. Although the overall prevalence could be affected
prevalence surveys were carried out in the Canary goat population, using this sampling frame, the impact by island and the comparison between islands
about 20 years ago, showing an overall seroprevalence of 33% would justify the frame used. A total of 550 animals considering at least a level of
confidence of 95%, desired absolute precision of 5% and an expected prevalence of
(Velasco, 2010). More recent studies evaluating domestic rumi- 50% (Thursfield, 2007). The number of animals to be sampled per farm was 25 (for a
nants on Gran Canaria reported seroprevalences of 60.4%, 31.7% and minimal expected prevalence of 12% according to previous prevalence in ruminants
12.2% for goat, sheep and cattle respectively (Rodríguez et al., 2010), -Rodríguez et al. (2010) and taking into consideration the smallest insular census
and 19% for dromedary camels (Mentaberre et al., 2013). After these (6416, El Hierro island) and all were lactating females (for a better management
they were sampled in the milking room). A questionnaire to collect epidemiological
findings, our group decided to estimate the current status of this
data was taken from each farmer, and variables were: location of the farm, herd
disease in all the Canary Islands, assessing goats from each island size (<50–100 animals/101–400/>401) history of abortions (frequent/not frequent),
vaccination against C. burnetii, manure removal frequency (weekly/monthly/lower
frequency/never) urbanization grade (no urbanized/urbanized), and milk processing
(artisanal cheese factory/industrial cheese factory). The urbanization grade was cat-
∗ Corresponding author. Fax: +34 928451142. egorized as “no urbanized” and “urbanized” depending on the absence or presence
E-mail address: carlos.gutierrez@ulpgc.es (C. Gutiérrez). of people living in the surroundings (about 500 m).

http://dx.doi.org/10.1016/j.smallrumres.2015.12.034
0921-4488/© 2015 Elsevier B.V. All rights reserved.
M.T. Tejedor-Junco et al. / Small Ruminant Research 134 (2016) 62–64 63

Table 1
Summarized information by island including sample size and seroprevalences.

Island Goat censusa Sampled goats Sampled farms C. burnetii + (%) C. burnetii − (%)

La Palma 22,730 75 3 49 (65%) 26 (35%)


El Hierro 6,416 50 2 34 (68%) 16 (32%)
La Gomera 7,105 50 2 28 (56%) 22 (44%)
Tenerife 50,085 100 4 20 (20%) 80 (80%)
Gran Canaria 82,806 100 4 21 (21%) 79 (79%)
Lanzarote 22,520 75 3 35 (47%) 40 (53%)
Fuerteventura 119,509 100 4 47 (47%) 53 (53%)

Total 311,171 550 22 234 (42%) 316 (58%)


a
Source: Regional Canary Islands Government, Statistic Office, http://www.gobcan.es/agricultura/otros/estadistica/).

2.2. Serological evaluation The Netherlands after the outbreaks of human clinical Q fever
occurred recently (21.4%) (Schimmer et al., 2011). In this latter case,
Blood samples were taken from jugular vein and transported under refriger-
goats were the associated reservoirs for the human infection. In our
ation until their arrival at laboratory. Serum was obtained after centrifugation at
2000 × g and stored at −20 ◦ C until use. Sera were tested to detect antibodies against study, goat seroprevalence would be increased when compared
C. burnetii using a commercial Q fever antibody ELISA Test Kit (Idexx, Liebefeld-Bern, with data reported 20 years ago (33%), although improved diag-
Switzerland), following the manufacturer’s recommendations. nostic methods currently available could have detected a higher
number of cases. In fact, CFT (complement fixation test) and IFA
2.3. Statistical analyses
(indirect-immunofluorescence assay) which were used in those
Normality test and inferential analyses were done at 95% of confidence using IBM studies have currently a limited use. Nonetheless, these results
SPSS Statistics for Macintosh, Version 22.0. Chi-square (2) or Fisher exact tests were would suppose a high risk for humans and animal population. Fur-
used to compare two proportions. Odds ratio measure of association was employed ther studies including also other ruminant species would be needed
for disease comparisons. in order to estimate the real threat for humans in the region.
Concerning the associated risk factors to present specific anti-
3. Results bodies, goats belonging to intensive or semi-intensive managed
farms showed a higher seroprevalence, probably due to a closer
Of the 550 examined goats, 234 (42%) showed specific anti- contact of the animals. The absence of vaccination programs against
bodies against C. burnetii, while 316 (58%) presented doubtful or C. burnetii in all the Islands could also explain this finding. From
negative results. Data ordered by island are shown in Table 1. the reproductive viewpoint, abortions are widely associated to
Statistically significant differences were found comparing the C. burnetii infection in goats; however, there were no significant
different islands (2 = 86.76, P < 0.0001), and accordingly, individ- differences on seroprevalence between herds with high or low
ual data were then compared to mean values of the Archipelago abortion rates. In goats, as in sheep, asymptomatic disease can be
(Table 2). As summarized in Table 2, goats located in some islands more common than reproductive disorders (Menzies, 2011). Thus,
like La Palma (OR = 2.58), El Hierro (OR = 2.64), Fuerteventura vaccination of the animals would be an important control measure
(OR = 2.20) or Lanzarote (OR = 1.65) showed higher risk of being in for Q fever, but currently vaccination is not a routine practice on
contact with the bacterium; in contrast, negative OR observed in the Canaries. Inactivated phase I vaccine has been recommended
Gran Canaria or Tenerife would indicate a protective factor to have by international organisms in at-risk areas (OIE, 2010), which must
contact with C. burnetii, at least compared to mean values of the be considered by the Regional Official Veterinary Services in order
Canaries. to fight against the disease
From the reproductive viewpoint, we did not find significant As regards to manure removal frequency, it has been demon-
differences between those herds declaring high or low frequency strated that goat manure contaminated with C. burnetii can be a
of abortions. At this respect, none of the farmers interviewed used source of infection for human beings; in fact, proximity of con-
vaccines to prevent Q fever in their herds. Regarding the manure taminated land parcels have predicted human cases better than
removal frequency, responses were: weekly (10), monthly (7), proximity of Q-fever positive farms (Hermans et al., 2014). This
lower frequency (4), never (1). Statistical analysis did not reveal aspect should be considered when implementing a control plan on
significant differences between positive and negative herds. Con- the Canaries. Concerning milk processing, about 50% of the sampled
cerning milk processing, 14 of the 22 sampled farms had artisanal farms commercialized artisanal cheese without previous pasteur-
cheese factories, 3 of which included pasteurization as a previ- ization of the milk. Thus, islands like La Palma and La Gomera are
ous hygienization process of the milk, while 8 farmers derived the particularly worrying because all the sampled farms produced and
milk to an industrial milk factory. Non-statistical differences were commercialized unpasteurized cheese. The hypothesis that inges-
found in Q fever prevalence between all sampled farms. As regards tion of C. burnetii would infect individuals is controversial. The
to the urbanization grade, 10 farms were located in rural areas bacterium is the most heat resistant organisms of public health
without human population in the surroundings, while 19 were sur- significance. Although C. burnetii seems not be viable in dairy prod-
rounded by some human settlements; showing an increased risk ucts (Eldin et al., 2013), stringency of milk pasteurization has been
in the rural areas compared with the urbanized farms (2 = 8.05; established as a safety measure (Cerf and Condron, 2006).
p = 0.005; OR = 1.63; CI 95% = 1.16–2.29). As a conclusion from our results, goat seroprevalence of C. bur-
netii on the Canary Islands can be considered as high, reinforcing
4. Discussion the hypothesis that the disease is endemic on the Archipelago.
Moreover, the disease would be an important re-emerging disease
The overall goat seroprevalence in Canaries was 42%, which on the Archipelago. An urgent control plan as well as surveillance
should be considered as high compared to other Spanish regions measures must be exercised by the Official Veterinary Services for
(8.7% in the Northern Spain) (Ruiz-Fons et al., 2010) or European containment of the disease and to avoid the risk for humans and
territories like Switzerland (11%) (Magouras et al., 2015), or even animals to be infected.
64 M.T. Tejedor-Junco et al. / Small Ruminant Research 134 (2016) 62–64

Table 2
Values of individual Chi-squared test of each island.

Island 2 P value OR CI 95%

La Palma 17.46 <0.0001 2.58 1.64–4.07


El Hierro 10.05 0.002 2.64 1.42–4.91
La Gomera 1.92 0.165 – –
Tenerife 33.68 <0.0001 0.22 0.13–0.38
Gran Canaria 28.19 <0.0001 0.24 0.15–0.43
Lanzarote 7.33 0.007 1.65 1.15–2.37
Fuertventura 11.99 0.001 2.20 1.41–3.58
*
OR: Odds ratio; CI: Confidence interval. 2 represents the mean of each island compared to the 6 other islands.

Conflict of interest Magouras, I., Hunninghaus, J., Scherrer, S., Wittenbrink, M.M., Hamburger, A., Stärk,
K.D., Schüpbach-Regula, G., 2015. Coxiella burnetii infections in small
ruminants and humans in Switzerland. Transbound. Emerg. Dis. (in press).
The authors declare no conflict of interest. Mentaberre, G., Gutiérrez, C., Rodríguez, N.F., Joseph, S., González-Barrio, D.,
Cabezón, O., de la Fuente, J., Gortazar, C., Boadella, M.A., 2013. A transversal
Acknowledgements study on antibodies against selected pathogens in dromedary camels in the
Canary Islands, Spain. Vet. Microbiol. 167, 468–473.
Menzies, P.I., 2011. Control of important causes of infectious abortion in sheep and
The authors wish to thank veterinarians in charge of the goat goats. Vet. Clin. North Am. Food Anim. Pract. 27, 81–93.
health associations on each island as well as the farmers and herd OIE, Office International des Epizooties, Q, fever, Manual of Diagnostic Tests and
Vaccines for Terrestrial Animals, (Chapter 2.1.12., 2010, www.oie.int).
keepers to allow us the access. Pascual Velasco, F., Rodríguez Pérez, J.C., Otero Ferrio, I., Borobio Enciso, M.V., 1992.
Seroprevalence of Q fever among the adult population of Lanzarote (Canary
References Islands). An. Med. Interna 9, 428–432.
Rodríguez, N.F., Carranza, C., Bolaños, M., Pérez-Arellano, J.L., Gutierrez, C., 2010.
Seroprevalence of Coxiella burnetii in domestic ruminants in Gran Canaria
Bolaños, M., Santana, O.E., Angel-Moreno, A., Pérez-Arellano, J.L., Limiñana, J.M.,
Island, Spain. Transbound. Emerg. Dis. 57, 66–67.
Serra-Majem, L., Martín-Sánchez, A.M., 2003a. Seroprevalence of infection by
Ruiz-Fons, F., Astobiza, I., Barandika, J.F., Hurtado, A., Atxaerandio, R., Juste, R.A.,
Coxiella burnetii in Canary Islands (Spain). Eur. J. Epidemiol. 18, 259–262.
García-Pérez, A.L., 2010. Seroepidemiological study of Q fever in domestic
Bolaños, M., Santana, O.E., Pérez-Arellano, J.L., Angel-Moreno, A., Moreno, G.,
ruminants in semi-extensive grazing systems. BMC Vet. Res. 6, 3, http://dx.doi.
Burgazzoli, J.L., Martín-Sánchez, A.M., 2003b. Q fever in Gran Canaria: 40 new
org/10.1186/1746-6148-6-3.
cases. Enferm. Infecc. Microbiol. Clin. 21, 20–23.
Schimmer, B., Luttikholt, S., Hautvast, J.L., Graat, E.A., Vellema, P., Duynhoven, Y.T.,
Cerf, O., Condron, R., 2006. Coxiella burnetii and milk pasteurization: an early
2011. Seroprevalence and risk factors of Q fever in goats on commercial dairy
application of the precautionary principle? Epidemiol. Infect. 134, 946–951.
goat farms in the Netherlands, 2009–2010. BMC Vet. Res. 7, 81, http://dx.doi.
Eldin, C., Angelakis, E., Renvoisé, A., Raoult, D., 2013. Coxiella burnetii DNA, but not
org/10.1186/1746-6148-7-81.
viable bacteria, in dairy products in France. Am. J. Trop. Med. Hyg. 88, 765–769.
Thursfield, M., 2007. In: Blackwell, M. (Ed.), Veterinary Epidemiology. 3rd ed.
Espejo, E., Gil-Díaz, A., Oteo, J.A., Castillo-Rueda, R., García-Alvarez, L.,
Blackwell Science, Oxford, pp. 228–246.
Santana-Báez, S., Bella, F., 2014. Clinical presentation of acute Q fever in Spain:
Velasco, F.P., 2010. Coxiella burnetii infections in domestic ruminants in Canary
seasonal and geographical differences. Int. J. Infec. Dis. 26, 162–164.
Islands (Spain). Transbound. Emerg. Dis. 57, 464.
Hermans, T., Jeurissen, L., Hackert, V., Hoebe, C., 2014. Land-applied goat manure
as a source of human Q-fever in the Netherlands, 2006–2010. PLoS One 9 (5),
e96607, http://dx.doi.org/10.1371/journal.pone.0096607.

You might also like