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Serratospiculosis in captive peregrine falcons (Falco peregrinus) in Switzerland.

Abstract: Infection with Serratospiculum species was identified in a captive peregrine falcon (Falco peregrinus) in Switzerland. Pathologic and parasitologic examination results revealed generalized severe granulomatous airsacculitis, with intralesional adults, larvae, and eggs of Serratospiculum species. Subsequently, an individual coprological analysis of the remaining 15 falcons (peregrine falcons and gyrfalcons [Falco rusticolus]) from the same owner was performed. Eggs of Serratospiculum species (4 birds) and Capillaria species (11 birds), and oocysts of Caryospora species (1 bird) were detected. Treatment with ivermection (2 mg/kg SC) was effective, as none of the falcons excreted Serratospiculum species eggs 10 days after one dose. To our knowledge, this is the first report of infection with Serratospiculum species in captive falcons in Europe.

Key words: Serratospiculum species, airsacculitis, ivermectin, Europe, birds of prey, avian, peregrine falcon. Falco peregrinus, gyrfalcon. Falco rusticolus

Clinical Report

In January 2016, an 8-year-old female peregrine falcon (Falco peregrinus) (falcon 1) from a private falconry located in the Canton of Vaud, in the southwest of Switzerland, was found dead in its enclosure. Two days later, the carcass was brought to the Institute of Animal Pathology, Vetsuisse Faculty, University of Bern, for postmortem examination. This falcon belonged to a group of healthy peregrine falcons (n = 8) and gyrfalcons (Falco rusticolus) (n = 7) with ages between 1 and 17 years. The falcons were used both for hunting and breeding and were kept either individually or in pairs in separate enclosures. Younger birds were kept on perches (Table 1). All falcons were fed on a regular basis with day-old-chicks, quail, and rats and occasionally hunted prey, namely ravens and gulls. The falcons were dewormed yearly with a single subcutaneous injection of ivermectin (2 mg/ kg), except for two 1-year-old falcons (falcons 7 and 12) that had never been dewormed at the time of death of falcon 1. The last deworming had taken place in the beginning of 2015 (1 year prior). A full necropsy of falcon 1 was performed.

At necropsy, falcon 1 was moderately emaciated and presented a mild infection with bird lice (Mallophaga species). A total of 20-30 nematodes, approximately 20-30 cm in length, were found in the coelomic cavity and in the thoracic and abdominal air sacs, which were diffusely opaque and thickened. Within the air sac walls and in the coelomic serosa, multifocal granulomas 1-2 mm in diameter were present (Fig 1). The pericardium, liver, and kidneys were multifocally covered with a moderate to high amount of chalky white material (visceral and renal gout). Tissue samples of the air sacs and organs were immediately fixed in 4% neutral buffered formalin, embedded in paraffin, cut at 4 pm, and stained with hematoxylin and eosin for further histologic evaluation. Adult parasites found in the air sacs and coelom plus intestinal contents and fecal samples were collected and sent to the Institute of Parasitology, Vetsuisse Faculty, University of Bern, for parasite identification, coproscopy by sodium acetate-acetic acidformalin, and combined sedimentation-flotation method with Zn[Cl.sub.2]. (1) Because the macroscopic findings clearly indicated a severe parasitic infection with secondary visceral and renal gout, no bacteriologic examination was undertaken.

Histologically, within the air sacs and the air sac walls, multiple longitudinal and cross sections of adult male and female nematodes were observed. These were 300-400 [micro]m in width, had an approximately 10-pm-thick, regularly indented cuticle, and a pseudocoelom and coelomyarian musculature. A single-layered cuboidal epithelial digestive tract and a reproductive tract containing either eggs or sperm could be observed (Fig 2). Additionally, longitudinal and cross sections of nematode larvae (approximately 30-40 [micro]m in width) and many oval-shaped embryonated eggs (approximately 50 X 30 [micro]m with a 3-[micro]m-thick shell) were observed both within the air sac and the air sac wall, as well as in the serosa from the proventriculus and gizzard. The air sac walls were severely thickened due to fibrosis, neovascularization, and infiltrations by heterophilic granulocytes, macrophages, and multinucleated giant cells from the foreign body type, which formed a granulomatous inflammation surrounding the different parasitic stages (Fig 3). Within the wall of the gizzard and the proventriculus, multifocal necrotic and hemorrhagic, elongated areas, interpreted as larval migration scars, were observed (Fig 4). In the large intestine, moderate numbers of embryonated eggs were present in the ingesta. Furthermore, multifocal gout tophi were observed in the parenchyma and the serosa of the liver, heart, and kidneys, consistent with visceral and renal gout. Additionally, numerous Serratospiculum species eggs were identified by sodium acetateacetic acid-formalin and combined sedimentation-flotation analysis performed on intestinal content and fecal samples from falcon 1. These eggs measured 55 X 35 (.im, were smooth shelled, and contained a developed larva (Fig 5). Accordingly, the nematodes found in the coelom and air sacs from falcon 1 were identified as being adult forms of Serratospiculum species." Species identification could not be performed, as no complete male Serratospiculum specimens were present among the collected parasites.

After the diagnosis of serratospiculosis from falcon 1, a complete coprological screening of the remaining 15 falcons was performed to determine whether these animals were also infected with Serratospiculum species. Two peregrine falcons (falcons 2 and 4) and two gyrfalcons (falcons 10 and 11) were found to be excreting Serratospiculum eggs. Additionally, 11 falcons excreted Capillaria species eggs and one excreted Caryospora species oocysts (Table 1). Subsequently, all falcons were dewormed subcutaneously with ivermectin (2 mg/ kg). No adverse effects were detected in any of the falcons. Ten days later, a second coprological screening of all falcons was performed to evaluate deworming effectiveness. No Serratospiculum eggs could be identified, although 4 falcons (falcons 7, 8, 9, and 13) excreted Capillaria species eggs and 1 falcon (falcon 3) excreted Spirurida eggs different from Serratospiculum species eggs. Three falcons (falcons 3, 7, and 15) excreted unsporulated and unspecified coccidian oocysts.

Discussion

In this clinical report, the occurrence of a severe serratospiculosis associated with a severe, diffuse, chronic, granulomatous airsacculitis in a captive peregrine falcon from Switzerland is described. Given the high number of parasites present at necropsy in the air sacs and the severity and diffuse distribution of the lesions, we consider that in this case the serratospiculosis was the primary cause of chronic illness with a major impact on respiratory tract function, which ultimately led to the death of this bird.

Serratospiculosis is a worldwide disease caused by spirurid nematodes of the genus Serratospiculum, family Diplotrianidae, that affects the air sacs of birds. (3,4) Although these parasites can infect a broad range of avian hosts, most cases have been found in Falconiformes, particularly in members of the Falconidae family. (5,6) The genus Serratospiculum is divided into 9 species, which can be distinguished by the spicule length of the male parasites. (2) Serratospiculum seurati is the most common species affecting falcons in the Middle East, whereas Serratospiculum tendo is most commonly found in wild birds of prey in Europe. (7,11)

The life cycle of Serratospiculum species is not yet fully understood. (12) Final avian hosts become infected through the ingestion of intermediate insect hosts, such as beetles, grasshoppers, woodlice, or locusts parasitized with infective third larvae (L3). (7,13,15) After ingestion, L3 penetrate through the wall of the proventriculus and gizzard and migrate directly into the air sacs and lungs, where they undergo further molts and finally reach sexual maturity. (7) Embryonated eggs are released in the air sacs and subsequently regurgitated, swallowed, and released into the environment by means of excreted feces or regurgitated pellets. (5,11) The presence of S tendo in wild birds of prey, which feed almost exclusively on small and medium-sized birds, suggests a possible infection through avian paratenic hosts. (11,12)

Because there are relatively few reported cases of serratospiculosis, the pathogenicity of infection with Serratospiculum species remains poorly understood and its impact on the populations of birds of prey worldwide is controversially discussed. (7,11) Falcons with severe Serratospiculum species infections may show no significant clinical or pathologic changes, but they can also suffer from highly deleterious effects, leading to disease and death of the infected bird. (7,10,12,14,16) Moreover, adult Serratospiculum species can survive within the air sacs of an infected bird for several years, where they induce degeneration of the collagen and muscular layers located between the epithelial and mesothelial components, resulting in the consequent thickening of the tissue and seriously compromising air circulation. (17) Additionally, blocking of the secondary bronchi and associated parabronchi through egg deposition in the lungs and edema formation predisposes affected birds to secondary pneumonia with Pseudomonas, Klebsiella, or Aspergillus species. (7,17) The gross and histologic lesions in the falcon we describe are comparable with the ones described in falcons infested with Serratospiculum species worldwide. (17,19) The visceral and renal gout also detected in this falcon is a likely consequence of prolonged dehydration secondary to chronic illness. However, because no bacteriologic culture was performed, it is unknown whether a secondary bacterial infection contributed to death of falcon 1.

Three Serratospiculum species have been described to date in wild birds in Europe, namely Serratospiculum guttatum in Iceland and Spain, Serratospiculum chungi in Spain, and Serratospiculum tendo in the Netherlands, France, Germany, Italy, Russia, Poland, and Spain. (3,9,11,13,20-26) According to available data, S tendo infections seem to be highly prevalent among wild birds of prey in Europe. (9-11,20,22,23) in the present case, it was not possible to identify the Serratospiculum species present in falcon 1. However, considering the distribution of the serratospiculosis cases in Europe, this animal was likely infected with 5 tendo. In Europe, besides peregrine falcons, which seem to be a preferential host, (10,11,22) S tendo has been identified in saker falcons (Falco cherrug), common kestrels (Falco tinnunculus), lanner falcons (Falco biarmicus), black kites (Milvus korschun, syn. Milvus migrans), northern goshawks (Accipiter gentilis), and rooks (Corvus frugilegiw). (3,10,11,20,22-23,27) Also, S guttatum has been recently described in the air sacs of wild gyrfalcons from Iceland. (25)

The distribution and relevance of Serratospiculum species in Switzerland is widely unknown. Serratospiculum species was an incidental finding in 2 wild peregrine falcons that died of toxicosis in 2011 and 2014. (28) Another wild peregrine falcon that was submitted for necropsy at the Centre for Fish and Wildlife Health, Vetsuisse Faculty, University of Bern, in 2015, harbored undetermined nematodes from the Diplotrianidae family in the air sacs (N. M., unpublished data, 2015). These findings indicate the presence of Serratospiculum species in the Swiss wild bird populations. To our knowledge, the present report is the first described case of an infection with Serratospiculum species in captive falcons not only in Switzerland, but also in Europe.

The exact source of infection with Serratospiculum species in this captive falcon group could not be elucidated. However, 4 of the 5 falcons infected with Serratospiculum species (including falcon 1) shared their enclosure with other infected birds (Table 1). This suggests that the falcons became infected within their enclosure through the ingestion of insects carrying L3 larvae and not during hunting or with the food they were provided. This is, in turn, consistent with the presence of the parasite in the environment.

Prophylaxis against Serratospiculum species infection implies regular deworming and making all enclosures insect proof. Several antihelminthic drugs against Serratospiculum species have been described, such as febendazole, levamisole, mebendazole, moxidectin, thiabendazole, melarsomine combined with ivermectin, and ivermectin alone. (7,15,29-32) In the present case, a single subcutaneous dose of 2 mg/kg ivermectin was effective against Serratospiculum species as shown by the coprologic analysis of all remaining falcons 10 days after treatment. Also, no side effects were observed in any of the treated birds. Single ivermectin treatment at an even lower dose of 1 mg/kg SC was reported to be efficient in removing adult Serratospiculum species. (7) Additional safe deworming protocols using ivermectin that have been reported include subcutaneous administration of ivermectin at 1 mg/kg followed by a second treatment at the same dose 1 week later, and a single oral administration of moxidectin at 200 pg/ kg; oral ivermectin administration was shown to be ineffective in controlling infections with S seurati in the Middle East. (7,32) The same authors also reported that ivermectin (1 mg/kg SC) is effective against Capillaria species. However, in the present study, several falcons excreted Capillaria species eggs (4 birds), unspecified coccidian oocysts (3 birds), and Spirurida species eggs differing from Serratospiculum species eggs (I bird). This finding may be a result of excretion of parasites present in the gut of ingested prey, which are consequently excreted by the birds of prey in the feces.

In conclusion, serratospiculosis is not found exclusively among wild birds in Europe and therefore should be considered as a differential diagnosis for veterinarians assessing captive falcons presenting with respiratory signs or decreased flight performance, or both.

Acknowledgments: We thank Drs Pierre and Christine Basset, the owners of the falcons, for the background information, fecal sampling, and shipment; Dr Kristel Kegler from the Institute of Animal Pathology, Vetsuisse Faculty, University of Bern, for assistance in picture editing; Manuela Bozzo, Erika Burgi, and Evelyne Rohrer from the Institute of Animal Pathology, Vetsuisse Faculty, University of Bern, for their excellent histologic technical assistance; and Larissa Hoffmann. Liliane Krahenbuhl, Christine Salvisberg, and Gertrud Rosenberg from the Institute of Parasitology, Vetsuisse Faculty, University of Bern, for analyzing the fecal samples.

References

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Ines B. Veiga, DVM, PhD, Marion Schediwy, Med Vet, Brigitte Hentrich, Dr Med Vet, Caroline F. Frey, Dr Med Vet, Dipl EVPC, Nelson Marreros, Dr Med Vet, and Nadine Stokar-Regenscheit, Dr Med Vet, Dipl ECVP

From the Institute of Animal Pathology (Veiga, Schediwy, Stokar-Regenscheit), the Institute of Animal Parasitology (Hentrich. Frey, Marreros), and the Centre for Fish and Wildlife Health (Marreros), Vetsuisse Faculty, University of Bern, Langgassstrasse 122. 3012 Bern, Switzerland.

Caption: Figure 1. Serratospiculum species adult located in the left thoracic and abdominal air sacs of falcon 1 (arrow) after removal of most parasites. The air sac walls are diffusely thickened, irregular, grey, and opaque and show multifocal, approximately 2-mm-diameter granulomas (arrowhead).

Caption: Figure 2. Cross section of an adult male Serratospiculum species and of multiple embryonated eggs (arrow) located withi n the granulomatous airsacculitis (hematoxylin and eosin; scale bar = 200 ([micro]m).

Caption: Figure 3. Granuloma formation in the adult male falcon described in Figure 1. Multinucleated giant cells from the foreign body type (thin arrow) surrounding Serratospiculum species embryonated eggs (large arrow) and larval longitudinal sections (arrowhead) (hematoxylin and eosin, scale bar 50 = [micro]m).

Caption: Figure 4. Focal necrosis and fibrosis in the muscular layers of the gizzard wall (arrowhead) due to larval migration of Serratospiculum species in peregrine falcon 1. Infiltrations of heterophilic granulocytes and lymphocytes surround the migration tract (thin arrow) (hematoxylin and eosin, scale bar = 50 [micro]m).

Caption: Figure 5. Serratospiculum species eggs excreted by falcon 1 (scale bar = 50 [micro]m).
Table 1. Falcon characteristics and coprological screening results by
sodium acetate/acetic acid/formalin and combined sedimentation/
flotation method with ZnCl2 before and 10 days after deworming with
ivermectin (2 mg/kg SC).

                             Housing       Age
Bird no.            Sex      (facility)    (years)

Falco peregrinus
1                   Female   Enclosure 1   8
2                   Male     Enclosure 1   6
3                   Female   Enclosure 2   14
4                   Male     Enclosure 2   3
5                   Female   Enclosure 3   6
6                   Male     Enclosure 3   6
7                   Female   Perch         1
8                   Female   Perch         2
9                   Female   Perch         2
Falco rusticolus
10                  Female   Enclosure 4   3
11                  Male     Enclosure 4   5
12                  Female   Perch         1
13                  Male     Single        6
14                  Female   Single        7
15                  Female   Single        16
16                  Female   Single        17

                    Parasites (species)
Bird no.            before deworming

Falco peregrinus
1                   Serratospiculum
2                   Serratospiculum, Capillaria
3                   Capillaria
4                   Serratospiculum
5                   Capillaria
6                   Capillaria
7                   None
8                   Capillaria
9                   Capillaria
Falco rusticolus
10                  Serratospiculum, Capillaria
11                  Serratospiculum
12                  Capillaria, Caryospora
13                  Capillaria
14                  Capillaria
15                  Capillaria
16                  None

                    Parasites (species)
Bird no.            after deworming

Falco peregrinus
1                   Not performed
2                   None
3                   Spirurida, (a) coccidia (b)
4                   None
5                   None
6                   None
7                   Capillaria, coccidia (b)
8                   Capillaria
9                   Capillaria
Falco rusticolus
10                  None
11                  None
12                  None
13                  Capillaria
14                  None
15                  Coccidia (b)
16                  None

(a) Spirurida other than Serratospiculum species.

(b) Coccidia oocysts could not be further classified.
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Title Annotation:Clinical Report
Author:Veiga, Ines B.; Schediwy, Marion; Hentrich, Brigitte; Frey, Caroline F.; Marreros, Nelson; Stokar-Re
Publication:Journal of Avian Medicine and Surgery
Geographic Code:4EXSI
Date:Sep 1, 2017
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