Suspected toxicity by biological waste and air sac nematode infestation in a free-living peregrine falcon (Falco peregrinus)


Published: Dec 27, 2017
Keywords:
Biologic waste spilling Klebsiella sp peregrine falcon Serratospiculum sp.
P. N. AZMANIS (Π.Ν. ΑΖΜΑΝΗΣ)
M.-E. KRAUTWALD-JUNGHANNS
V. SCHMIDT
Abstract

This case report describes an uncommon complex of mortality in a free living peregrine falcon (Falco peregrinus). The bird was found rinsed with biologic waste and the integument was mildly inflamed. No respiratory signs were detected at first. In addition, no alterations were detected during. During orthopaedic, neurologic, ophthalmologic and radiographic examinations. Parasitological pharyngeal and faecal examination revealed Capillaria spp. and Serratospiculum spp. eggs. The therapeutic scheme included stress reduction, supportive therapy with fluids, antifungals, antibiotics, anti-inflammatory, antiparasitic agents and nutritional management. Cleaning with dishwashing gel to remove the biological waste took place, but its removal was partial. Despite the intensive care, the patient developed respiratory distress and succumbed on the fifth day of hospitalization. Pathological examination revealed adult Serratospiculum tendo parasites in the air sacs and Capillaria spp. in the large intestine. Bacteriological and mycological cultures revealed significant growth of Klebsiella pneumoniae isolated from the skin, heart, lung, liver, kidney and intestine and a mild presence of Candida albicans in the large intestine. Their probable role was judged as secondary. Mild multifocal haemorrhages with heterophilic and lymphohistiocytic infiltrates, fibrin and rod‑like bacteria were detected in the skin histopathologically, confirming the clinical integument inflammation. Cause of death was asphyxia caused by oedema, haemorrhages and blood congestion of the lung. The contribution of S. tendo in the initial spill event and case evolution is discussed. This unusual case highlights the complexity of the wildlife cases, with which avian or small animal clinicians (consulting rehabilitation centres or falconers) might be confronted. Although the application of ancillary  and advanced diagnostic tools, the in-depth knowledge of the species and the intensive monitoring are important, this might lead to an unrewarding outcome. Financial constraints in wildlife casualty cases urge the critical choice of diagnostic, therapeutic and post-mortem laboratory testing. Serratospiculum tendo should be considered in the differential diagnosis of acute respiratory distress in free-living peregrine falcons, presented in rehabilitation centres or in private practise by falconers in Greece and Europe.

Article Details
  • Section
  • Research Articles
Downloads
Download data is not yet available.
References
Ackerman N, Isaza R, Greiner E, Berry CR (1992) Pneumocoelom associated with Serratospiculum amaculata in a bald eagle. Vet Radiol Ultrasound 33:351–355.
Al-Timimi F, Nolosco P and Al-Timimi B (2009) Incidence and treatment of serratospiculosis in falcons from Saudi Arabia.
Vet Rec 165:408–410. Austin B (1998) The effects of pollution on fish health. J Appl Microbiol 85 Suppl 1:234–242.
Bain O, Mawson PM (1981) On some oviparous filarial nematodes mainly from Australian birds. Rec S Aust Mus 118:265–284.
Barbusiński K (2005) Toxicity of industrial wastewater treated by Fenton’s Reagent. Pol J Environ Sci 14:11–16.
Barker JC (1996) Lagoon design and management for livestock waste treatment and storage. Internal report. North Carolina Cooperative Extension Service, pp 11.
Bigland CH, Liu SK, Perry ML (1964) Five cases of Serratospiculum amaculata (Nematoda: Filarioidea) infection in prairie falcons (Falco mexicanus). Avian Dis 8:412–419.
Biswal S (2013) Liquid biomedical waste management: An emerging concern for physicians. Muller J Med Sci Res 4:99-106.
Bolong N, Ismail AF, Salim MR, Matsuura T (2009) A review of the effects of emerging contaminants in wastewater and options for their removal. Desalination 239:229–246.
Briggs KT, Gershwin ME, Anderson DW (1997) Consequences of petrochemical ingestion and stress on the immune system of seabirds. ICES J Marin Sci 54:718–725.
Bryndza HE (1991) Surfactant efficacy in removal of petrochemicals from feathers. In: (eds: White J, Frink L) The effects of oil on wildlife: research, rehabilitation and general concerns. IWR C, California, pp. 78–94.
Burge WD, Marsh PB (1978) Infectious disease hazards of landspreading sewage wastes. J Environ Qual 7:1–9.
Burkholder JM, Mallin M, Howard BG,, Larsen LM, Mclver MR, Christopher G, Deamer-Melia N, Briley DS, Springer J, Touchette BW, Hannon EK (1997) Impacts to a coastal river and estuary from rupture of a large swine waste holding lagoon. J Environ Qual 6:1451–-1466.
Chipasa KB (2003) Accumulation and fate of selected heavy metals in a biological wastewater treatment system. Waste Manag 23:135–43.
Clarke A (1977) Contamination of peregrine falcons (Falco peregrinus) with fulmar stomach oil. J Zool 181:11–20.
Clark WS, Gorney E (1987) Oil contamination of raptors migrating along the red sea. Environ Pollut 46:307–313.
Cooper JE (2002) Birds of prey: health and disease, 3rd ed. Wiley & Sons. London.
Dohms JE, Metz A (1991) Stress--mechanisms of immunosuppression. Vet Immunol Immunopathol 30:89–109.
Eckenfelder WW Jr, O’Connor D (1961) Biological waste treatment. Pergamon Press, London.
Fallacara DM, Halbrook RS, French JB (2011) Toxic effects of dietary methylmercury on immune function and hematology in American kestrels (Falco sparverius). Environ Toxicol Chem 30:1320–1327.
Ferguson-Lees J, Christie DA (2001) R aptors of the world. Christopher Helm, London.
Frink L, Miller EA (1995) Principles of oiled bird rehabilitation. In: (ed.: Frink L) Wildlife and Oil Spills: response, research, and contingency planning. Tristate Bird Rescue & Research, Inc., Newark, pp 61–68.
Fry DM (1995) Reproductive effects in birds exposed to pesticides and industrial chemicals. Environ Health Pers 19:165–171.
Fry DM, Lowenstine LJ (1985) Pathology of common murres and cassin’s auklets exposed to oil. Arch Environ Contam Toxicol 14:725–737.
Green CH, Gartrell BD, Charleston WAG (2006) Serratospiculosis in a New Zealand Falcon (Falco novaeseelandiae). New Zeal Vet J 54:198–201.
Handrinos G, Akriotis T (1997) The birds of Greece. Christopher Helm. London.
Hassen A, Belguith K, Naceur J, Cherif A, Cherif M, Boudabous A (2001) Microbial characterization during composting of municipal solid waste. Bioresour Technol 80:217–225.
Heidenreich M (2013) Birds of prey: disease and management, 2nd ed. Neumann-Neudamm AG Verlag, Melsungen.
Hoek W van der, Anh VT, Cam PD, Vicheth C, Dalsgaard A (2005) Skin diseases in people using urban wastewater in Phnom Penh. Urban Agri Mag 3:30–31.
Kalpakis S, Mazaris AD, Mamakis Y, Poulopoulos Y (2009) A retrospective study of mortality and morbidity factors for common buzzards (Buteo buteo) and long-legged buzzards (Buteo rufinus) in Greece: 1996–2005. Bird Conserv Int 19:15–21.
Kammerer M, Mastain O, Le Dréan-Quenech’du S, Pouliquen H, Larhantec M (2004) Liver and kidney concentrations of vanadium in oiled seabirds after the Erika wreck. Sci Total Environ 333:295–301.
Kocan AA, Gordon LR (1976) Fatal air sac infection with Serratospiculum amaculata in a prairie falcon. J Am Vet Med
Assoc 169:908.
Komnenou AT, Georgopoulou I, Savvas I, Dessiris A (2005) A retrospective study of presentation, treatment, and outcome of free-ranging raptors in Greece (1997-2000). J Zoo Wildl Med 36:222–228.
Kuhlman JR, Martin LB (2010) Captivity affects immune redistribution to skin in a wild bird. Funct Ecol 24:830–837.
Kummerfeld N, Thielking M (2013) In vitro investigation on transdermal permeation of reference substances in various
birds as a model for possible toxic effects caused by oil spills. Proceedings of 1st International Conference on Avian Herpetological and Exotic Mammal Medicine, (Wiesbaden, Germany), p. 376.
Latimer SL, Rakich PM (1994) Necropsy examination. In: (eds: Ritchie BW, Harrison GJ, Harrison LR) Avian Medicine:
Principles and Application, Wingers Publishing, Lake Worth, pp. 355-379
Latshaw JD (1991) Nutrition — mechanisms of immunosuppression. Vet Immunol Immunopathol 30: 111–120. Leighton F (1991) The toxicity of petroleum oils to birds: an overview In: (eds: White J, Frink L) The Effects of Oil on Wildlife: Research, Rehabilitation and General Concerns. IWR C, California, pp. 43–57.
Lewis D, Gattie K (2002) Pathogen risks from applying sewage sludge to land. Environ Manag Technol 3:287–293A.
Mazet JAK, Newman SH, Gilardi KVK, Tseng FS, Holcomb JB, Jessup DA, Ziccardi MH (2002) Advances in oiled bird emergency medicine and management. J Avian Med Surg 16:146–149.
Morgan KN, Tromborg CT (2007) Sources of stress in captivity. Appl Anim Behav Sci 102:262–302.
Muller MG (2009) Practical handbook of falcon husbandry and medicine, Nova Science Publishers, New York.
Murk A, Boudewijn T, Meininger P, Bosveld A, Rossaert G, Ysebaert T, Meire P, Dirksen S (1996) Effects of polyhalogenated aromatic hydrocarbons and related contaminants on common tern reproduction: integration of biological, biochemical, and chemical data. Arch Environ Contam Toxicol 31:128–140.
Pattee H, Franson C (1982) Short term effects of oil ingestion on American Kestrels (Falco sparverius). J Wildlife Dis 18:235–241.
Rossi SS, Anderson JW, Ward GS (1970) Toxicity of water-soluble fractions of four test oils for the polychaetous annelids, Neanthes arenaceodentata and Capitella capitata. Environ Pollut 10:9–18. Rushton L (2003) Health hazards and waste management. Br Med Bull 68:183–197.
Samour JH, Naldo J (2001) Serratospiculosis in captive falcons in the Middle East: a review. J Avian Med Surg 15:2–9.
Santoro M, Tripepi M, Kinsella JM, Panebianco A, Mattiucci S (2010) Helminth infestation in birds of prey (Accipitriformes
and Falconiformes) in Southern Italy. Vet J 186:119–22.
Skrjabin K (1991) Volume 1: Spirurata , Filariata. In: (ed.: Raveh M)
Key to Parasitic Nematodes. EJ Brill, Leiden, pp. 413–416.
Sonin MD (1968) Filariata of animals and man and diseases caused by them. In: (ed.: Skrjahin KI) Essentials of Nematodology.Vol 21, Union of Socialistic Soviet Republics: Akademia Nauk SSSR, Moscow, pp. 186–190.
Stamper DM, Montgomery MT (2008) Biological treatment and toxicity of low concentrations of oily wastewater (bilgewater). Can J Microbiol 693:687–693.
Steele CM, Brown RN, Botzler RG (2005) Prevalences of zoonotic bacteria among seabirds in rehabilitation centers along the Pacific Coast of California and Washington, USA. J Wildl Dis 41:735–44.
Stenkat J, Krautwald-Junghanns ME, Schmidt V (2013) Causes of morbidity and mortality in free-living birds in an urban environment in Germany. Ecohealth, 1-14.
Stephenson R (1997) Effects of oil and other surface-active organic pollutants on aquatic birds. Environ Conserv 24:121–129.
Sterner MC, Cole RA (2008) Diplotriaena, Serratospiculum, and Serratospiculoides. In: (eds.: Atkinson CT, Thomas NJ, Hunter DB) Parasitic Diseases of Wild Birds. Wiley-Blackwell, Iowa, pp. 434–439.
Tarello W (2006) Serratospiculosis in falcons from Kuwait: incidence, pathogenicity and treatment with melarsomine and ivermectin. Parasite 13:59-63.
Tišler T, Zagorc-Končan J (1997) Comparative assessment of toxicity of phenol, formaldehyde, and industrial wastewater to aquatic organisms. Water Air Soil Pollut 97:315–322.
Tseng FS (1999) Considerations in care for birds affected by oil spills. Sem Exotic Pet Med 8:21–31.
Vilanova X, Blanch AR (2005) Distribution and persistence of fecal bacterial populations in liquid and dewatered sludge from a biological treatment plant. J Gen Appl Microbiol 51:361–368.
Ward FP, Fairchild DG (1972) Air sac parasites of the genus Serratospiculum in falcons. J Wild Dis 8:165–68.
Ward RL, Ashley CS (1978) Identification of detergents as components of wastewater sludge that modify the thermal stability of reovirus. Appl Environ Microbiol 36:889–897.
Wehr EE (1938) New genera and species of the nematode superfamily Filarioidea. I. Serratospiculum amaculata, n. sp. Proceedings Helminthological Society (Washington, USA), p. 559–60.
Wernery R, Wenery U, Kinne J, Samour J (2004) A color atlas of falcon medicine. Schlütersche Verlagsgesellschaft mbH &
Co.KG, Hannover.
Zuberogoitia I, Martínez JA, Iraeta A, Azkona A, Zabala J, Jimenez B, Merino R, Gómez G (2006) Short-term effects of the prestige oil spill on the peregrine falcon (Falco peregrinus). Mar Pollut Bull 52:1176–1181.