High lungworm burden in enclosed wild boar from Eastern Austria

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Research Article

High lungworm burden in enclosed wild boar from Eastern Austria

Corresponding author: Mag.med.vet.Bettina Lechner, Institute of Parasitology, Department of Pathobiology,Vetmeduni Vienna Veterinärplatz 1 A-1210, Vienna, AUSTRIA. Tel: +43 1 25077 2201; Fax: +43 1 25077 2290;

Email: bettina.lechner91@gmail.com Received: 12-18-2015

Abstract

Objective

We aimed to investigate the endoparasite status, especially the lungworm burden, of wild boar in an enclosed hunting ground in Eastern Austria.

Animals and samples

In total, 49 lungs and 47 corresponding faecal samples of animals of different age groups (shoats, young pigs and adults) were examined.

Methods

Lungs were dissected and adult metastrongylids were counted and determined to species level (n=25/animal). Faecal sam-

ples were prepared by sedimentation/flotation and examined qualitatively and also quantitatively (by McMaster counting).

Results

Adult lungworms were present in 94% of the animals. Eggs of Metastrongylus spp. (89%), Ascaris suum (8%), Globocepha- lus urosubulatus (96%), Trichuris suis (51%), as well as oocysts of coccidia (100%) were detected. Five different species of Metastrongylus (M. apri, M. salmi, M. pudendotectus, M. confusus and M. asymmetricus) were found in the lungs. Oocysts of E. debliecki, E. scabra, E. perminuta, E. porci, E. polita and Cystoisospora suis could be differentiated. E. debliecki was the most common (100 %), E. porci (28 %) the rarest species. In most cases, parasite excretion tended to decline with increasing age. In contrast to domestic pigs, C. suis could be found in all age groups.

Conclusions

The high intensities and infection rates indicate a considerable infection pressure which may lead to health problems in en- closed wild boar. Proper habitat conservation and hunting practices are necessary to keep a stable and healthy population in such enclosed environments.

Keywords: game animals; nematodes; Metastrongylus; Eimeria; Cystoisospora; Globocephalus; Trichuris, Ascaris

Introduction

Besides roe and red deer, wild boar is one of the most im- portant hoofed game species in Central Europe. Due to the difficult hunt and the excessive food supply the populations are constantly increasing. Growing populations in restricted habitats however pose an increasing risk of parasitic infec-

tions. Especially in game enclosures it must be assumed that the transmission risk for various pathogens increases inor- dinately [1, 2].

Coccidial infections are frequently asymptomatic, but Cystoisospora suis and rarely Eimeria spp. can also cause catarrhal, rarely necrotic enteritis with non-haemorrhagic diarrhoea in young piglets, leading to weight loss and poor performance [3-6].

Little is known about the prevalences in wild boar and the effects on their health. For Austria, so far five species of Eime- ria have been described from domestic and wild suids. The latter harboured mostly Eimeria debliecki and Eimeria polita, as well as C. suis [7].

The large roundworm Ascaris suum can be found in the small intestines of domestic and wild suids and can cause reduced growth when present in large numbers [8]. Similarly, the whip- worm Trichuris suis frequently resides in the large intestines of wild and domestic pigs and can cause enteritis with diarrhoea in intensive infections, as well as hypalbuminaemia and re- duced growth [9]. The porcine hookworm Globocephalus uro- subulatus on the other hand infects primarily wild boar [10].

The porcine lungworms of the genus Metastrongylus are rarely found in domestic pigs since they require earthworms as inter- mediate hosts so only pigs with outdoor access to earthworm habitats can become infected while wild boars frequently har- bour these parasites. Especially in young animals the parasite is rather pathogenic, inducing lung damage with dyspnoea, weight loss and even death [11, 12]. Due their pathogenici- ty they are still considered to be the most important airway pathogens in extensive pig management [13, 14]. In Europe, so far five different species have been described, Metastrongylus apri (syn. M. elongatus), M. salmi, M. pudendotectus, M. confusus and M. asymmetricus [12, 15-19].

To evaluate the parasite burden of wild boar from an enclosure in Eastern Austria, we investigated lungs and faecal samples of animals from different age categories for infections with parasites, especially lungworms.

Material and Methods

Samples

Samples were provided by hunters and originated from a large enclosure in Eastern Austria. As soon as possible after killing, lungs and faecal samples were kept refrigerated in a cooling chamber at a temperature of 4-8 °C until examination 3-5 days later. The hunters also evaluated age, weight and body condi- tion of the animals. In total 49 animals, 10 male and 23 female shoats (<1 year), two male and six female young animals (1-2 years), four sows and four tuskers were examined. Lungs were available from all of them, faecal samples from all but two shoats (n=47). Lungs were inspected for gross pathological changes, the upper and lower airways were cut open, the lung- worms removed and fixed in 70% ethanol.

Lungworm differentiation

Specimens from each positive lung were counted. A maximum of 25 females per each lung were differentiated according to different keys [12, 18, 20]. The species were differentiated according to their characteristic endings shown in Figure 1.

Figure 1. Metastrongylus species in wild boar: Posterior ends of females of M. apri (A); M. pudendotectus (B), M. asymmetricus (C), and

M. confusus (D).

Coproscopy

Using a combined sedimentation/flotation technique, faecal sample were examined for parasite stages (helminth eggs and coccidian oocysts) using saturated sugar solution. Positive samples were examined by a modified McMaster technique [21]. Coccidia oocysts were microscopically differentiated ac- cording to their size and morphology [22].

Statistical evaluation

To compare the parasite distribution in different age groups data were analysed by nonparametric tests (Kruskal-Wallis and Mann-Whitney U test) in SPSS v. 20 (SPSS Inc., Chicago, USA). Correlations between body mass and parasite burden/ excretion and between different species of Metastrongylus were tested calculating Pearson’s rank correlation coefficient.

Results

Body condition of the animals

The body condition was documented for 48 animals, and 38

of these were in very good or good physical condition. Nine shoats were poorly nourished and a male adult animal was emaciated. For nine of the ten animals with a poor condition faecal samples could be examined. No correlation with the bur- den of adult lungworms or with the excretion of oocysts/nem- atode eggs could be established (details not shown).

Lung pathology

During gross examination purulent areas, enlarged lymph nodes, pulmonary oedema and haemorrhage, emphysema and adult lungworms could be seen in different parts of the lung. Haemorrhage was the most common finding, which could at least partly be attributed to gunshot injuries and was not eval- uated further. Emphysema was the second most common al- teration, found in 90% of the shoats in different parts of the lung. Young pigs showed mainly signs of purulent pneumonia and enlarged lymph nodes (Fig. 1). Earlier works stated that pathological changes induced by porcine lungworms are irre- versible [11], indicating the health importance of metastron- gylid infections in wild boar.

Metastrongylid infections

In total, 46 animals (94%) harboured adult lungworms. Shoats showed a mean worm burden of 195.5 specimen (SD=251.5, median 109, maximum number of worms: 1020) which was higher than in the other two groups (Table 1).

Overall, five different species of Metastrongylus could be differ- entiated, M. apri, M. salmi, M. pudendotectus, M. confusus and M. asymmetricus (Fig. 2). M. apri and M. salmi had prevalences of 75-100% and 63-100%, respectively, depending on the age of the animals, whereas M. asymmetricus was the rarest with 13- 42% (Fig. 3). Differences in species composition between the age groups of the animals were, however, not significant. A sig- nificant positive correlation between infections with M. salmi and M. pudendotectus (p = 0.000; Pearson’s Rho = 0.493) and an almost significant positive correlation between infections with M. confusus and M. apri (p = 0.000; Rho = 0.564) could be observed.

Metastrongylids are of the most important extraintestinal nematode pathogens of wild boar and organic pigs in terms of animal health, due to the wide distribution of the intermediate earthworm host. A high overall prevalence precluded statisti- cally significant differences between age groups, hinting at a continuous reinfection cycle within the enclosure. So far, cor- relations between infection intensity and body condition could not be stablished, however, a tendency of lower body weight in animals with high infections was observed. Other studies could show a correlation between poor body condition and lungworm infection [27].

Table 1. Prevalences and infection intensities for adult Metastrongylus spp. and excretion rates for coccidia oocysts and eggs of Metastrongy- lus, Trichuris and Globocephalus and (only in shoats) Ascaris in different age groups. SD: standard deviation

Age group Parasites Prevalence (%) Excretion rates (eggs/oocysts per gram of faeces)

Minimum Maximum Median Mean SD
Shoats Metastrongylus adults 96.8 0 1020 109 195,5 251.6
(<1 year) Coccidia oocysts 100 450 88,850 11,650 19,579 20,073.8
N=33 (lungs) Metastrongylus eggs 90.3 50 400 0 52 103.9
N = 31 (faecal samples) Trichuris eggs 51.5 50 100 0 11 28.8
Globocephalus eggs 93.5 50 3000 450 544 649.7
Ascaris eggs 12.9 50 4950 0 265 955.0
Young pigs Metastrongylus adults 100 1 44 63 22,1 17.2
(1-2 years) Coccidia oocysts 100 4,500 151,150 27,025 50,244 12,667.0
N = 8 Metastrongylus eggs 87.5 50 100 0 20 35,0
Trichuris eggs 62.5 50 50 0 10 21.1
Globocephalus eggs 100 50 1150 125 305 395.4
Adults Metastrongylus adults 87.5 0 307 51,5 87,9 107.0
(>2 years) Coccidia oocysts 100 1,650 37,550 11,850 14,769 57,487.6
N = 8 Metastrongylus eggs 87.5 50 100 0 33 51.6
Trichuris eggs 37.5 50 50 0 17 25.8
Globocephalus eggs 100 100 1650 575 608 590.3
TOTAL Metastrongylus adults 95.8 0 1020 0 1020 149.6
N= 49 (lungs) Coccidia oocysts 100 450 151,150 14,050 23,980 28,979.5
N = 47 (faecal samples) Metastrongylus eggs 89.4 0 400 0 49 88.8
Trichuris eggs 51.1 0 100 0 13 26.5
Globocephalus eggs 95.7 0 3000 400 550 600.3
Ascaris eggs 8.0 0 4950 0 174 781.6

This may be due to an influence of age, but irrespective of the risk factors, high worm burdens indicate high infection pres- sure and in the long run this may lead to serious health prob- lems in the observed herd since in enclosures parasite stages may accumulate (in the environment or in intermediate hosts, depending on the life cycle).

Figure. 2. Lung alterations according to age groups.

Coproscopy

Coccidia oocysts could be found in all examined samples (Table 1). Five species of Eimeria (E. debliecki, E. perminuta, E. polita, E. scabra and E. porci) were found in a prevalence of 25-100%, while Cystoisospora suis was found in 97.9% of the samples, mostly in shoats (Table 2).

the same time, E. scabra excretion rates were also negatively correlated with body weight (p = 0.007; Rho = -0.446), which could be an effect of age distribution, although correlations between parasite excretion and age could not be established, probably due to low numbers of animals in some age groups.

In contrast to earlier studies [7, 23] in the present study

E. perminuta and not E. suis was detected.

Figure 3. Prevalences of adult Metastrongylus species in different age groups.

Interestingly, all age groups shed considerable amounts of C. suis oocysts, which is in contrast to observations in domestic pigs where infection is mostly seen in suckling piglets [24].

Table 2. Coccidia (Eimeria spp., Cystoisospora suis) according to species and age group.

Number of samples E. debliecki E. perminuta E. polita E. scabra E. porci C. suis
Shoats 31 31 30 17 31 8 30
Young pigs 8 8 8 4 8 2 8
Adults 8 8 8 4 6 3 8
TOTAL 47 47 46 25 45 13 46

Excretion intensities varied between 450 and 151,150 oocysts per gram of faeces (Table 1). E. scabra was found significantly more often in shoats than in the older pigs (p = 0.007) while no correlation could be found for the other coccidia species. At

Besides eggs of Metastrongylus, eggs of Globocephalus, Trichu- ris and Ascaris could be detected by flotation. Age-related dif- ferences were seen only for Trichuris eggs which were found mainly in young pigs (62.5%) and Ascaris eggs which were

found only in shoats (Table 1). The highest excretion rates were seen for Ascaris with 4,950 eggs per gram of faeces (epg) and for Globocephalus with 3,000 epg, both in shoats. Metas- trongylus and Trichuris eggs were excreted with a maximum of 400 and 100 epg (Table 1). Quantitative excretion of metas- trongylid eggs was positively correlated with the excretion of hookworm eggs (p = 0.000; Rho = 0.679).

Ondrejková et al. [25] investigated the effect of endoparasites on the oral vaccination against classical swine fever in wild boars and found that parasitic infections influence the efficacy of oral vaccination against swine fever and support the ability of the virus to reproduce and cause disease, and to infect the surrounding the wild boar populations [25]. It must therefore be assumed that parasitic infections render wild boar more prone to other infections.

Conclusion

The rate of lungworm infections of the examined animals was very high in all age groups, as were the infection rates for coc- cidian. The worm burden and oocyst excretion rates especially in shoats indicated a high infection pressure in young animals which was partially reduced in older boars, probably due to frequent reinfection in combination with induction of immuni- ty [19]. High excretion rates for hookworm, ascarid and whip- worm eggs in younger animals also indicate a development of immunity; however, this appears to be slow and incomplete ex- cept for A. suum, which was excreted only by shoats. The lung alterations, especially emphysema and purulent pneumonia, indicated that animals were more or less severely affected by lungworms (and possibly secondary bacterial infections) in all age groups. Under these circumstances both the high extensi- ty and the high parasite burden indicate that animal health is most likely compromised by parasitic infection since animals constantly remain in the same contaminated environment. Contrary to this, Popiolek et al. observed a higher prevalence of Metastrongylus in a wild population than in farmed wild boar [26], so management of farmed wild boar may influence the parasite burden. In the longer term, it is expected that animals with reduced pulmonary function will suffer from reduced food intake, poor growth or even weight loss, as indicated by the approximately 20% of the hunted animals which were in poor body condition, with the consequence of a weakened im- mune system.

Means of improving animal health in a game enclosure are restricted to controlled hunting to reduce population density, while improved hygiene of feeding areas might be more diffi- cult to implement. Navarro et al. [28] showed that it is import- ant to restrict supplemental feeding because of the high den- sity of wild boar in feeding grounds. They also observed that wild boars defecate before entering feeders which lead to an accumulation of parasite stages, and Nagy et al. [29] reported

an increased density of earthworms infected with metastron- gylids in the feeding area of wild boar, so that an accumulation of parasite stages at such sites (where their final hosts aggre- gate) must be assumed.

The ultimate aim of all measures must be to achieve a balance between game animals and their enclosed habitat to maintain a functional ecological cycle.

Acknowledgements and Conflict of Interest

The authors declare that they have no conflict of interest.

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