Date Published: June 16, 2008
Publisher: BioMed Central
Author(s): Milla Solismaa, Sauli Laaksonen, Minna Nylund, Elisa Pitkänen, Riitta Airakorpi, Antti Oksanen.
In autumn 2006, Finnish meat inspection data revealed lesions in tendons, muscles and ligaments of bovine hind legs leading to partial condemnation of carcasses. In gross pathological examination at Finnish Food Safety Authority Evira, Oulu (now Fish and Wildlife Health) Research Unit, Onchocerca sp. (Filarioidea; Onchocercidae) nematodes were detected in lesions. Due to this, a pilot study was made in order to find out what filarioid nematodes do occur in cattle, horses and sheep in Finland.
Ventral skin biopsies from 209 dairy cattle and 42 horses, as well as blood samples from 209 cattle, 146 horses and 193 sheep, were collected from different parts of Finland and examined for microfilariae. Visceral organs and other tissues from 33 cattle with parasitic lesions were studied histopathologically.
Onchocerca sp. microfilariae (mf), 240 μm long, range 225–260 μm, 5.4 μm thick, were found in 37% of the skin biopsies of cattle. All blood samples from cattle, horses and sheep and skin biopsies from horses were negative for mf. Ventral skin microfilaria prevalence in cattle was higher in southern Finland than in the North (p = 0.001). Animal age and sampling time was not associated with mf prevalence. The infection was evenly distributed among young and older animals. Macroscopic lesions on tissues included greenish-grey discolouration and often oedema. In most of the lesions, small pale nodules were seen on the fasciae. Histopathologic examination of the samples revealed mild to intense infiltration with eosinophilic granulocytes and multifocal nodular lymphoplasmacytic aggregations were seen. In some samples, there were granulomatotic lesions with central necrotic tissue and cell detritus, surrounded by eosinophilic granulocytes, lympho-, plasma- and histiocytes and some multinucleated giant cells. Around living nematodes no or only weak inflammatory changes were observed.
Onchocerca sp. infection in cattle was found to be common in Finland, but the amount of pathological changes leading to condemnation of infected parts is low compared to the mf prevalence. Pronounced pathological changes are distinct but rare and mild changes are difficult to distinguish. No other filarioid nematodes were observed from the animals and it appears that horses and sheep may be free from filarioid nematodes in Finland.
Filarioid nematodes are known to occur among domestic animals almost all over the world. The economically most important and also most abundant filarioid nematodes in cattle are Setaria digitata, S. labiatopapillosa, S. marshalli, Onchocerca gibsoni, O. gutturosa, O. armillata, O. lienalis, O. ochengi, Parafilaria bovicola and Stephanofilaria spp. Generally, species of Onchocerca are medium-sized filarioids which usually inhabit subcutaneous tissues, ligaments and aponeuroses of large mammals whereas species of Setaria are found in the abdominal cavities of artiodactyls. The filariids (Parafilaria and Stephanofilaria) are small to medium-sized subcutaneous parasites of certain mammals. All filarioid nematodes produce larvae (microfilariae, mf) into the skin (Onchocerca spp., Parafilaria spp. and Stephanofilaria spp.) or blood circulation (Setaria spp.) of the host where they are available to the haematophagous insects which operate as intermediate hosts and active vectors for the parasites .
Material from cattle, sheep and horses was collected between 28 February and 24 September, 2007. Blood and skin samples from the animals were collected from slaughterhouses at Kuopio (Atria) (28.2.-14.6.07, 150 cattle skin samples of 17734 slaughtered), Kemi (Veljekset Rönkä Oy) (17.4.-22.5.07, 59 cattle skin samples of 673 slaughtered, 15.5.-24.9. 07, 193 sheep blood samples of 1104 slaughtered and 13 horse blood and skin samples) and Hautjärvi (Hannu Vainio Oy) (29 horse skin samples). In addition, blood samples from horses (133) were collected at different horse clinics by practising veterinarians in Oulu (17), Hyvinkää (21), Ypäjä (18), Lahti (19), Laukaa (20), Ylivieska (18) and Tampere (20). Blood samples from horses were mostly from half-breed trotters or mounts (riding-horses) visiting clinics for some undefined reason. Cattle and horse samples originated from all over Finland and sheep from the provinces of Lapland and Oulu. In slaughterhouses, samples were taken from all slaughtered horses during collecting period and cattle and sheep samples were collected randomly when labour was available. All the animals included in this study were over one year old and had been grazing outdoors in the previous summer and thus had been exposed to the potential vectors of filarioid nematodes. Blood samples were taken from all of the animals. Skin biopsies were taken from 209 cattle and from 42 horses. Tissue samples from 33 cattle (not included in the blood and skin monitoring) with lesions considered parasitic (subcutaneous and subfascial oedema and granulomas with greenish or yellowish coloration indicating eosinophilic infiltration, fibrotic or granulomatous fibrin depositions on visceral organs, especially on liver) were collected by the meat inspecting veterinarian during routine meat inspection from Kuopio slaughterhouse from 8 November, 2006, to 23 May, 2007. Tissues were delivered fresh to Evira, where they were dissected under stereo microscope for adult parasites, fixed in 10% neutral buffered formalin and routinely processed; embedded in paraffin, cut in 4 μm sections and stained with haematoxylin and eosin, and examined histopathologically. Samples included muscles and fasciae, tendons or ligaments of legs, flank or brisket from 24, liver samples from ten, lung samples from four and a spleen sample from one animal.
All blood samples examined were negative (cattle 209, horses 147, sheep 193). Also skin biopsies from the 42 horses examined were found negative for mf. Of the 209 cattle skin biopsies from umbilical area, 78 (37%) were positive for Onchocerca sp. mf (Table 1) and of the 60 samples collected from ears, 5% were positive.
Because of the meat inspection data, the finding of Onchocerca sp. microfilariae from skin samples of cattle was expected although the high prevalence (37%) was a surprise. However, in Europe Onchocerca spp. infections in cattle are quite abundant; for example in Germany the mf prevalence in one study was 40.4%  and in North Wales 28.5% .
Onchocerca sp. infection in cattle is fairly common in Finland, but the amount of pathological changes leading to condemnation of infected parts is low compared to the mf prevalence. Pronounced pathological changes are distinct but mild changes are difficult to distinguish. In the future it would be important to follow the development of the situation by improving the monitoring of changes in meat inspection. Also its pathological significance should be determined. Future challenges are also in recognizing the Onchocerca species infecting cattle, its vectors and possible prevention. According to this study, horses and sheep may be free from filarioid nematodes in Finland.
The authors declare that they have no competing interests.
MS participated in the collection of the samples, did all analyzes for identification of microfilariae from skin biopsies and blood and drafted the manuscript, SL participated in the design and coordination of the study, helped in the collection of the samples and helped to draft the manuscript, MN did all the pathological examinations and wrote parts of the chapters “Material and Methods” and “Results”, EP and RA partly coordinated the study and delivered numerous samples for examination, AO helped to draft the manuscript. All authors read and approved the final and revised manuscript.