MARKO LEGLER, SONJA WOLKEN, CHRISTIAN EPE, PETRA THOMAS, NORBERT KUMMERFELD: Cestodes and intestinal trematodes of Common Swifts in the area of Hanover (Germany) and the use of Praziquantel for treatment

Abstract

The investigation of sixty Common Swifts (Apus apus, Apodiformes) in the area of Hanover, Lower Saxony, Germany from 2006 to 2008 revealed cestodes and trematodes as common intestinal parasites. The prevalence of cestodes in Swifts was 84,6 % in adults and 91,5 % in juveniles. The extent of intestinal trematodes was 15,4 % in adult and 38,3 % in juvenile birds. The parasitological investigations identified two cestode species: Neoliga depressa and Neoliga occidentalis and two digenean species: Platynosomum sp. and Plagiorchis sp. The present study revealed Praziquantel (10 mg/ kg body weight PO Once; Droncit^®) as a potent antiparasitic medication for the treatment of a parasitosis with tapeworms and intestinal flukes in Common Swifts.

MARKO LEGLER¹, SONJA WOLKEN², CHRISTIAN EPE², PETRA THOMAS², NORBERT KUMMERFELD¹:

Cestodes and intestinal trematodes of Common Swifts (Apus apus) in the area of Hanover (Germany) and the use of Praziquantel for treatment

¹Clinic for Exotic Pets, Reptiles and Birds and ²Institute for Parasitology University of Veterinary Medicine, Hanover
Keywords
Common Swifts − Apus apus − Cestodes − Trematodes − Praziquantel − Droncit^®

Introduction

The Common Swift (Apus apus; Fig. 1) is the most frequently encountered species of the order Apodiformes in Europe and West, Central and East Asia and winters in sub-Saharan Africa. In much of the extensive Palaearctic breeding range the Swifts are found primarily in areas of human habitations and the nesting sites are in all suitable cavities in buildings, for example in window sills or under the roof (Polaschek 1988; Chantler and Driessens 1995; Bauer et al. 2006). As a consequence, from June to August juvenile Swifts in all ages are frequent patients in the practice of avian veterinarians. Adequate hand-feeding diet and techniques and also housing conditions are necessary for a successful rehabilitation (Polaschek 1987; Matthes not dated; for review, see Haupt 2001 and 2009). Some juvenile hand-reared Swifts in a bad condition showed a better growth rate after being treated with anthelmintics. This treatment also decreases the incidence of vitamin B deficiency in Swifts during the hand-rearing period (Haupt, personal communication, 2008). There could be a relation between these findings and the parasitic load. Praziquantel is a broad-spectrum anthelmintic effective against trematodes, adult cestodes and also with some activity against larval cestodes. Administration of Praziquantel (typically a single oral dose) causes paralysis of susceptible worms or damage to their tegument, making them more vulnerable to host enzymes or antibody dependent immune effector mechanisms (Harnett 1988).

To date there is little knowledge about parasites of the digestive system of Common Swifts, especially in young birds (Sprehn 1932, Galkin 1983).

Material and methods

In total sixty Common Swifts (13 adults and 47 juveniles) from the area of Hanover, Lower Saxony, Germany, were examined for gastrointestinal helminths during the breeding seasons (May to August) from 2006 to 2008. A necropsy was performed from 41 birds, which were euthanized in the Clinic for Exotic Pets, Reptiles and Birds of the University of Veterinary Medicine Hanover after an incurable injury (mainly eye and head traumata, shoulder and wing injuries). A rehabilitation and release to the wild of these birds was not possible (Kummerfeld 2003, Haupt 2009). The gastrointestinal tract was removed and macroscopic and microscopic (mucosal samples) investigations of the intestinal lumen and mucosal samples were done. The parasites were counted and fixed and stored in 70 % ethanol.

A treatment with Praziquantel (10 mg/kg body weight PO once; Droncit^®) was performed on 19 Swifts (aged between two weeks and adult Swifts). Parasitological testing of faecal samples both before and for three hours after the Praziquantel treatment were made. The parasites in the faecal samples were counted, fixed and stored in 70 % ethanol.

The fixed parasites were stained with carmine (Staining protocol, Institute for Parasitology of the University of Veterinary Medicine Hanover) and examined by microscope, based on morphological criteria (for review, see Galkin 1983, Georgiev and Murai, 1993).

Some samples of the intestine with parasites were immediately fixed in formalin and standardised stained with hematoxylin-eosin.

Differences between the results of the difference groups were tested for significance with Student's t-test, program SPSS for statistical analysis, SPSS Inc. Significance was assumed at P ≤ 0,05.

Results

The parasitological examination revealed cestodes in 11 out of 13 (84,6 %) adult Swifts and intestinal trematodes in 2 out of 13 (15,4 %) adults. Up to 33 (mean 19,27; median 21) tapeworms and up to 3 trematodes could be detected. All examined birds were in a good body condition.

In 43 out of 47 (91,5 %) juvenile Swifts cestodes and in 18 out of 47 (38,3 %) intestinal trematodes were found. Up to 32 cestodes (mean 15,2, median 15) and up to 10 (mean 5,5; median 6) intestinal trematodes could be detected in the juvenile Swifts. Twenty-nine birds were in good (Fig. 2) and 18 Swifts were in a poor body condition. There was no significant difference (P > 0,05) in the parasitic load between juvenile Swifts in good or poor body condition.

No side effects could be observed after the use of Praziquantel in different ages from 2 weeks to adult Swifts, and different dietary conditions of Common Swifts. There was no significant difference (P > 0,05) between the counted number of excreted parasites from treated birds (Fig. 3) and the number of parasites, that were found in the intestine of dissected Swifts (Fig. 8).

In faecal samples of untreated nestlings of Swifts only ova from trematodes (Fig. 4) and in untreated adult Swifts gravid proglottids from cestodes and ova from cestodes (Fig. 5) and trematodes were observed.

The parasitological investigation identified two cestode species Neoliga depressa (scolex in Fig. 6A) and Neoliga occidentalis (Dilepidoidea; subfamily Neoliginae, scolex in Fig. 6B) and two digenean species Platynosomum sp. (Dicrocoeliidae) and Plagiorchis sp. (Plagiorchiidae, Fig. 7) based on morphological criteria (Galkin 1983; Georgiev and Murai 1993; Spassky 2002).

The histopathology of the small intestine resulted inflammations on the insertion site of cestode scolex with the rostellum in the intestinal mucosa (Fig. 8)

Discussion

In the area of Hanover, Lower Saxonia, Germany, cestodes and intestinal trematodes were found in 43 (91,5 %) and in 18 out of 47 (38,3 %) juvenile Common Swifts, respectively. Also in adult Swifts a high prevalence of cestodes 11 out of 13 (84,6 %) and intestinal trematodes in 2 out of 13 (15,4 %) could be found. The same results detected by Galkin (1983) at the Kurish Spit (Russia) in adult birds (n=7). For comparison the invasion extension for cestodes in Barn Swallow (Hirundo rustica) is in juveniles only 15,98 ± 7,81 % (n=77) and in adults 35,06 ± 8,07 (n=130; Salamatin et al., 2006). For Barn Swallows (Hirundo rustica) 40 % (32 of 81) of the broods in villages throughout the area of Ulm (Germany) proved to be infected with trematodes (Janssen and Bock, 1989).

The Dilepidoidea of Apodidae and Hirundinidae form a separate subfamily Neoliginae, which is subdivided into two tribes: tribe Neoligini, the obligatory parasites of Apodiformes, and the tribe Angularellini, obligatory parasites of swallows (Passeriformes). A survey of different known apodidae cestodes and trematodes is given in Galkin (1983), Georgiev and Murai (1993) and Spassky (2002). The detected different cestodes and trematodes from the area of Hanover are also described in these surveys from other areas of distribution of Common Swifts. As opposed to cestode infections nematodes seem to be rare in Swifts based on the obligate insectivore (aerial plankton) nutrition (Lack and Owen 1955; Gross 1998). But Swifts could be sensitive to parasitosis caused by nematodes. Haupt (2001) described an infection with Capillaria sp. and Syngamus sp. after a feeding with earthworms, a natural paratenic host for these species.

The life cycle of the parasites of Swifts is unknown in detail. But, trematodes of the genus Plagiorchis develop in a life cycle that involves freshwater snails as the first and arthropods as the second intermediate host and vertebrates as the final host, described for swallows (Janssen and Bock, 1990). Like swallows, Swifts often hunt in the vicinity of water, preying on flying insects that may contain metacercarial cysts acquired during their aquatic developmental phase, for example Coleoptera, Trichoptera, Culicidae, Chironomidae (Janssen and Bock, 1990). Typically, dilepidids have a two-host life cycle, invertebrate intermediate hosts (for example coprophagous beetles or ants) and a vertebrate definitive host (Valkounova, 1987, Mohammed et al., 1988). Swifts prey consists of a wide variety of insects and arachnid life, with the main components of plant lice, hymenopterous insects, beetles and dipterous insects, which are described as intermediate hosts (Blotzheim and Bauer, 1980; Valkounova, 1987, Mohammed et al., 1988; Janssen and Bock, 1990; Chantler and Driessens, 2000).

In our study there were two principal reasons why young Common Swifts may end up in human hands. During the summer month temperatures can get extremely high right underneath the roof on the breeding sites. The young try to cool themselves at near the entrance of the nest and so may fall out. These birds are in most of the cases well fed in a very good body condition (Fig. 2; Haupt 2001). On the other hand in periods of cold weather with shortage of insects or after the loss of parents the food for the growth of young birds is rare. During this period the young Swifts may be left for astonishingly long periods up to several days. In this circumstances the young become torpid but can survive in this state until food is eventually brought to them (Chantler and Driessens 2000; Haupt 2009). In this time the birds often lose weight dramatically and finally they get incautious and fall out of the nest. Those foundlings are often emaciated and can only be saved by expert assistance (Haupt 2001). Especially in young birds in poor body condition emaciation secondary to the parasite load could be a problem and the growth rate after being treated with anthelmintics seems to be better (Haupt, personal communication 2008). The clinical diagnosis of a cestode infection, especially in living young Swifts with faecal samples was in this investigation difficult, because in most of the cases the infection with tapeworms is in the prepatent period. The present study revealed Praziquantel (10 mg/ kg body weight PO Once; Droncit^®) in a simple regime as a potent antiparasitic medication against tapeworms and intestinal flukes without undesirable side effects in Swifts, as with other bird species (Kummerfeld, 2007). The important effect of Praziquantel seems to be the paralysis of the parasites (Harnett, 1988).

In our opinion in birds with a good body condition, a normal growth rate and well-shaped droppings an anthelminthic therapy seems to be not necessary and can destroy the development of immunity. There is in the literature ample evidence that, with time, animals develop substantial resistance to reinfections, for example an impressive immunity against ingested oncosheres (Lightowlers et al., 1992; Emery et al., 1996). The high prevalence and intensity of cestodes in all ages in this study demonstrated the high infection pressure for Common Swifts in the area of Hanover, Germany, after a release into the wild. In these cases an immunity and so a natural regulation of the parasitic load could be important.

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Figures:

Fig. 1 Fledgling of a Common Swift in a good condition (feather and body) after three weeks of hand-rearing with crickets as an adequate hand-feeding diet (© M. Legler)

Fig. 3 Excreted cestodes in the faeces of a young swift, aged 4 weeks, a half hour after the use of Praziquantel (© M. Legler)

Fig. 8 Cestodes in the intestine of a Common Swift (A) and histopathology of the small intestine with a visible inflammation on the insertion point of scolex with his rostellum in the intestinal mucosa (H & E; 100x; B; © M. Legler)

Author’s address

Dr. med. vet. Marko Legler

Clinic for Exotic Pets, Reptiles and Birds

University of Veterinary Medicine, Hanover, Germany

Bünteweg 9

30559 Hannover