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Survey on Blood-Sucking Lice (Phthiraptera: Anoplura) of Ruminants and Pigs with Molecular Detection of Anaplasma and Rickettsia Spp

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Survey on Blood-Sucking Lice (Phthiraptera: Anoplura) of Ruminants and Pigs with Molecular Detection of Anaplasma and Rickettsia Spp Veterinary Parasitology 174 (2010) 355–358 Contents lists available at ScienceDirect Veterinary Parasitology journal homepage: www.elsevier.com/locate/vetpar Short communication Survey on blood-sucking lice (Phthiraptera: Anoplura) of ruminants and pigs with molecular detection of Anaplasma and Rickettsia spp S. Hornok a,∗, R. Hofmann-Lehmann b, I.G. Fernández de Mera c, M.L. Meli b, V. Elek d, I. Hajtós d, A. Répási d, E. Gönczi b, B. Tánczos a, R. Farkas a, H. Lutz b, J. de la Fuente c,e a Department of Parasitology and Zoology, Faculty of Veterinary Science, Szent István University, István u. 2., 1078 Budapest, Hungary b Clinical Laboratory, Vetsuisse Faculty, University of Zurich, 8057 Zurich, Switzerland c Instituto de Investigación en Recursos Cinegéticos IREC (CSIC, UCLM, JCCM), Ronda de Toledo, 13005 Ciudad Real, Spain d County Veterinary Station, Borsod-Abaúj-Zemplén, Vologda u. 1., 3525 Miskolc, Hungary e Department of Veterinary Pathobiology, Center for Veterinary Health Sciences, Oklahoma State University, Stillwater, OK 74078, USA article info abstract Article history: Lice may serve as biological or mechanical vectors for various infectious agents. To inves- Received 18 June 2010 tigate louse infestation of ruminants and pigs, and pathogens potentially transmitted by Received in revised form 25 August 2010 them, anopluran lice (n = 1182) were collected in Hungary, and evaluated for the presence Accepted 1 September 2010 of anaplasma, rickettsia and haemotropic mycoplasma DNA. On cattle the following species were found: Linognathus vituli (57%), Haematopinus eurysternus (38%) and Solenopotes capil- Keywords: latus (5%). L. vituli had a lower mean individual count/host when compared to H. eurysternus. Anoplura On calves only L. vituli was observed, with a higher louse burden than on full-grown cattle. H. Linognathus Haematopinus eurysternus and S. capillatus were more likely to occur simultaneously with another species Anaplasma on the same host, than L. vituli. Goats infested with Linognathus stenopsis had the over- Rickettsia all highest prevalence (68%), while pigs harbouring Haematopinus suis showed the lowest Vector (<1%). Anaplasma DNA was detected in 50% of pools analysed. In L. vituli Anaplasma ovis (or a closely related novel Anaplasma marginale genotype) was identified. Anaplasma-positivity of H. suis suggests that pigs may extend the reservoir and/or host spectrum of relevant species. Anaplasma-infected L. stenopsis pools show for the first time that caprine anaplas- mosis is endemic in Hungary. Rickettsia spp. were demonstrated from Linognathus spp. and H. eurysternus. No haemotropic mycoplasmas were detected in any samples. In conclusion, this is the first molecularly confirmed report of bovine and ovine Anaplasma spp. in L. vituli, L. stenopsis and H. suis. The present results suggest that phthirapterosis of domestic animals deserves more attention, and lice should be evaluated among the broad range of potential vectors of arthropod-borne pathogens. © 2010 Elsevier B.V. All rights reserved. 1. Introduction ological changes in their hosts, i.e. weight loss, hide damage and mild to severe anaemia – the latter especially in cat- The blood-sucking lice (Phthiraptera: Anoplura) are tle (Nelson et al., 1970; Gibney et al., 1985; Otter et al., permanent, host-specific ectoparasites of mammals. Their 2003). Secondly, as vectors, they can transmit louse-borne veterinary significance may be twofold. First, they can be pathogens (viruses, bacteria, fungi and protozoa) to sus- responsible for economical losses by inducing pathophysi- ceptible hosts. In this respect, their biological vector role usually means persistent development of disease agents in their gut cells, with or without consequent passing in their ∗ faeces. In either case, they do not inoculate the pathogen Corresponding author. Tel.: +36 1 478 4187; fax: +36 1 478 4193. E-mail address: [email protected] (S. Hornok). during a next blood-sucking, but it is rubbed into the host’s 0304-4017/$ – see front matter © 2010 Elsevier B.V. All rights reserved. doi:10.1016/j.vetpar.2010.09.003 356 S. Hornok et al. / Veterinary Parasitology 174 (2010) 355–358 skin inadvertently (Durden and Lloyd, 2009). Alternatively, 2.3. Molecular investigations if lice are short-term mechanical vectors, it becomes possi- ble that within hours of their former feeding they inoculate The DNA contents of each sample were preliminar- disease agents attached to their mouthparts (Shope, 1940; ily assessed by an 18S rRNA gene TaqMan real-time PCR Crystal, 1958). A prerequisite for both types of transmis- (Applied Biosystems, Rotkreuz, Switzerland) as described sion is that lice transfer between hosts, which is an integral previously (Boretti et al., 2009). In order to eval- aspect of their behaviour (Durden and Lloyd, 2009). uate the presence of bacterial agents (Rickettsiales: Reports on pediculosis of domestic animals are scarce, Anaplastamaceae and Rickettsiaceae; Mycoplasmatales: and prevalence data from several parts of Europe are lack- Mycoplasmataceae) conventional PCR was performed for ing or outdated. Correspondingly, in veterinary medicine the detection of Anaplasma spp. (screening for the 16S rRNA the epidemiological significance and vector potential of gene, positives evaluated for the msp4 gene) and real-time anopluran lice also appears to be underestimated or insuf- PCR assays were run for the demonstration and quantifi- ficiently evaluated. In part, this may be due to the regular cation of Rickettsia (23S and gltA genes) and haemotropic and widespread use of broad spectrum endectocides that Mycoplasma spp. (16S gene) as published (Brown et al., are given to kill parasites other than lice. However, it must 2001; de la Fuente et al., 2005; Boretti et al., 2009; Willi be kept in mind that in areas with lower standards of live- et al., 2009). Negative control reactions were included stock management lice and their vector role should not be using the same procedures and water instead of DNA to neglected or discounted: on the contrary, they may rep- monitor contamination of the PCR. Amplified fragments resent emerging problems (Otter et al., 2003; Bisdorff et of anaplasma DNA were resin purified (Wizard, Promega) al., 2006). Therefore this study was undertaken to eluci- and cloned into the pGEM-T vector (Promega) for sequenc- date the occurrence of sucking lice of ruminants and pigs ing both strands by double-stranded dye-termination cycle in Hungary, and to contribute to the general knowledge on sequencing (Secugen SL, Madrid, Spain). At least two inde- the potential vector role of relevant species. pendent clones were sequenced for each PCR. 2.4. Statistical analysis 2. Materials and methods Sample prevalence data were analysed by using Fisher’s 2.1. Sample collection exact test. Louse burdens were compared with Student’s t-test. Differences were regarded significant when P < 0.05. Adults and nymphs of blood-sucking lice have been removed from domestic animals kept indoors during the 3. Results and discussion winter time. Sampling was performed from cattle on four farms, from goats on three farms, and from pigs in one Altogether 1182 sucking lice were collected (Table 1). farm, during March of 2009 in central and north-eastern All species occurring on relevant hosts in the temperate Hungary. A total of 173 cattle, 50 goats and 350 pigs zone were found (Durden and Lloyd, 2009). However, this were included in the study. All animals were immobilized is the first report of Solenopotes capillatus from Hungary and their whole body surface scrutinized for the pres- (Piotrowski, 1970). Comparing the anopluran species of ence of lice. During sampling the predilection sites for cattle, S. capillatus was the rarest (Table 1), with highly macroscopically distinguishable lice on cattle (Haematopi- overdispersed intensities of infestation (three cows with nus and Linognathus sp.) and goats (Linognathus sp.) were only one specimen, and one with 37). Linognathus vit- noted. The age of cattle was also recorded. Specimens uli individuals were significantly more abundant than collected from the same animal were stored in one vial. Haematopinus eurysternus and S. capillatus (P < 0.001). Cat- Species identification was completed under stereomicro- tle infested with L. vituli also predominated (P < 0.001). The scope according to Zlotorzycka et al. (1974) and Kim et al. order of importance for the three bovine blood-sucking (1986). Lice belonging to one species and removed from the louse species – based on abundance data and prevalence same host individual were stored together in 70% ethanol (extensity of infestation, Table 1) – is opposed to what was until evaluation. reported for Germany, where S. capillatus was the most fre- quently encountered species, followed by H. eurysternus, 2.2. Pooling and DNA extraction and L. vituli as the rarest (Matthes et al., 1991). L. vituli was represented by a significantly lower mean A maximum of ten lice per animal belonging to the same individual count per host (Table 1), than H. eurysternus species were pooled together. All individuals in the pool (P = 0.027), unlike in another study from Canada (Colwell were washed sequentially in detergent-containing water, et al., 2001). Regarding co-infestations of cattle, H. eurys- in tapwater and in distilled water. Air-dried lice were sub- ternus and S. capillatus were significantly more prone to be sequently minced with pointed scissors at the bottom of in concurrence with another species (37.5 and 50%, respec- Eppendorf-tubes, in 100 ␮l of phosphate-buffered saline tively) than L. vituli (6.4%; P = 0.019). On calves only L. vituli (PBS). DNA was extracted using the QIAamp DNA blood was found. No significant difference was observed between mini kit (QIAGEN, Hilden, Germany) following the manu- the mean age of L. vituli, H. eurysternus and S. capillatus- facturer’s instructions and including an overnight digestion infested animals (data not shown). However, the mean ◦ step (incubation at 56 C for at least 8 h) with tissue lysis louse count of L. vituli was significantly higher (P = 0.001) buffer and Proteinase-K (QIAGEN, Hilden, Germany).
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