PhD in Veterinary Sciences for Animal Health and Food Safety

Contacts

Supervisor

Curriculum vitae

Phd thesis

Project Title: European Hedgehogs: Evaluation of Human-Animal Interactions in an Urban Environment

The European hedgehog (Erinaceus europaeus) is a small insectivorous mammal that has gradually transitioned from rural to urban areas, now classified as a synanthropic species. In cities, hedgehogs benefit from increased access to food and shelter, but they also face higher risks of human-related trauma. In recent years, hedgehogs have experienced a consistent population decline across Europe, likely due to human activities. However, few studies have thoroughly investigated the underlying pathological causes of their mortality.

Additionally, hedgehogs are known carriers of zoonotic pathogens, which may contribute to the maintenance and spread of these pathogens in urban areas, potentially posing a risk to human health.

Wildlife rescue centres (WRCs) are the facilities where hedgehogs come into closest contact with humans. In these settings, animals are exposed to different environments, diets, and pharmacological treatments, which may lead to changes in their gut microbiota and the acquisition or development of antimicrobial resistance (AMR) mechanisms.

The aim of this project was to evaluate the interactions between hedgehogs and humans in urban environments by determining:
i) the dangers humans pose to hedgehogs, through an examination of their causes of mortality;
ii) the potential risks hedgehogs pose to humans, by assessing their burden of zoonotic pathogens; and
iii) the impact of close human-animal contact on hedgehog microbial populations.

To address these objectives, adult hedgehogs admitted to two WRCs in the Piedmont region were studied. The project was structured around four main objectives:

A) Identification of Main Causes of Mortality (Supervision by Prof. Quaranta and Prof. Capucchio, in collaboration with Vetsuisse University):
I conducted complete necropsies and histopathological analyses on 156 Italian hedgehogs, comparing these findings to 109 necropsy reports from Vetsuisse. The primary histopathological findings involved the lungs, with cases of lymphoplasmacytic, granulomatous, or suppurative pneumonia. In Italy, the primary causes of death were trauma and infections, while in Switzerland, infections were the leading cause, followed by trauma. These findings highlight the significant role infections play in hedgehog mortality, which contrasts with previous reports emphasizing trauma.

B) Detection of Emerging/Zoonotic Pathogens (Supervision by Prof. Capucchio and Prof. Tomassone, in collaboration with RIVM and University of Barcelona):
Selected organs from hedgehogs were analyzed via PCR for the detection of zoonotic pathogens. We detected Borrelia burgdorferi s.l., Anaplasma spp., and Rickettsia spp. in spleen and skin samples, Borrelia miyamotoi, Bartonella spp., Coxiella burnetii, and Rickettsiella spp. in the spleen, Leptospira spp. in the kidneys, and Bordetella bronchiseptica in the lungs. Using PCA analysis, we determined that hedgehogs had an equal risk of carrying zoonotic pathogens in both urban and rural areas. This suggests that urban residents may also be at risk of acquiring zoonotic pathogens from hedgehogs.

C) Gut Microbiota Composition and Changes During Hospitalization (Supervision by Prof. Bertolotti, Prof. Robino, and Dr. Colitti, in collaboration with Vetmeduni Vienna):
Anal swabs were collected from 32 hedgehogs upon admission (T0) to the WRC and after 10 days of hospitalization (T1). DNA extraction, 16S rRNA amplification, and Illumina sequencing were performed. Alpha and beta diversity analyses revealed significant differences in gut microbiota composition between the two time points. From T0 to T1, we observed an increase in Streptococcus spp., Campylobacter spp., Lactobacillus spp., and Oenococcus spp., while Aeromonas spp. decreased over time.

D) Antimicrobial Resistance Patterns in Commensal Bacteria (Supervision by Prof. Robino and Prof. Nebbia):
Escherichia coli isolates from rectal swabs were cultured and identified using MALDI-TOF analysis. SensiTitre testing was performed to determine the Minimum Inhibitory Concentrations (MICs) of bacteria collected from 40 hedgehogs at T0 and T1. A significant increase in MIC values for amikacin, chloramphenicol, cephazolin, doxycycline, enrofloxacin, and pradofloxacin was observed over the hospitalization period.

Conclusion:
Our project confirmed that human-related trauma is a primary cause of hedgehog mortality, but it also highlighted the critical role of infectious agents in their deaths. Therefore, further studies on pathogenic viruses and bacteria in hedgehogs are necessary, particularly in regard to the role of lungworms in their pathology. Additionally, we confirmed that hedgehogs are carriers of zoonotic pathogens, representing a tangible risk for the spread of these pathogens in urban environments and potential transmission to humans. Finally, we observed that hospitalization in WRCs promotes changes in gut microbiota and the acquisition or development of AMR mechanisms.

Research activities

Periods in a foreign Institution:

• Institute of Veterinary Pathology, Vetsuisse Zurich (Supervision of Prof. Anja Kipar). Duration: 06/02/2023 - 07/04/2023. Location: Zurich, Switzerland. Competences acquired: forensic and non-legal post-mortem examinations on domestic, farm, wild and zoo animals; trimming and preparation of tissue samples for histological processing; evaluation of histological slides; drafting of necroscopic reports; translation and analysis of necropsy reports of European hedgehogs and comparison with Italian results

• National Institute for Public Health and the Environment (RIVM) (Supervision of Dr. Hein Sprong). Duration: 17/10/2023 - 22/12/2023. Location: Bilthoven, The Netherlands. Competences acquired: detection of zoonotic and vector-borne pathogens in animal tissues through genomic DNA and RNA extraction, qPCR and conventional PCR analysis, amplicon purification and sequencing; tissue collection from necropsy cases.

• Universidad Autonoma de Barcelona – Sefas group (Supervision of Prof. Emmanuel Serrano Ferron). Duration: 12/02/2024 - 23/02/2024 and 15/07/2024 - 26/07/2024. Location: Barcelona, Spain. Competences acquired: spatial and statistical analysis with R software; field sampling and rodent trapping.
• Vetmeduni Vienna – FIWI group (Supervision of Dr. Friederike Pohlin). Duration: 11/03/2024 - 17/05/2024. Location: Vienna, Austria. Competences acquired: field anaesthesia and wildlife monitoring, exotic animal anaesthesia; scientific writing and statistical analysis; microbiome analysis.

Research products:

Products related to the PhD project

• Articles journals with impact factor
  • Sarchese V, Palombieri A, Prandi I, Robetto S, Bertolotti L, Capucchio MT, Orusa R, Mauthe von Degerfeld M, Quaranta G, Vacchetta M, Martella V, Di Martino B, Di Profio F. Molecular Surveillance for Bocaparvoviruses and Bufaviruses in the European Hedgehog (Erinaceus europaeus). Microorganisms. 2024 Jan 17;12(1):189. doi:10.3390/microorganisms12010189.
  • Prandi I, Dervas E, Colombino E, Bonaffini G, Zanet S, Orusa R, Robetto S, Vacchetta M, Mauthe von Degerfeld M, Quaranta G, Hetzel U, Capucchio MT. Causes of Admission, Mortality and Pathological Findings in European Hedgehogs: Reports from Two University Centers in Italy and Switzerland. Animals (Basel). 2024 Jun 22;14(13):1852. doi: 10.3390/ani14131852.
  • Di Martino B, Di Profio F, Capucchio MT, Prandi I, Robetto S, Quaranta G, La Rosa G, Suffredini E, Marsilio F, Martella V, Sarchese V. Detection and genomic characterization of a novel mammarenavirus in European hedgehogs, Italy. Emerging Infectious Diseases. Accepted
  • Di Profio F, Di Martino B, Lanave G, Robetto S, Prandi I, Capucchio MT, Mandola ML, Quaranta G, Marsilio F, Martella V, Sarchese V. European hedgehogs (Erinaceus europaeus) as hosts of chaphamaparvovirus. Veterinary Microbiology. Submitted
• Abstracts of international congress
  • Prandi I, Dervas E, Colombino E, Bertolotti L, Cardello M, Ippolito D, Perotti M, Vacchetta M, Zanet S, Mauthe Von Degerfeld M, Quaranta G, Hetzel U, Capucchio MT. Causes of mortality in wild European hedgehog (Erinaceus europaeus) populations in Italy and Switzerland. Joint Congress of Veterinary Pathology and Veterinary Clinical Pathology, Lisbon (Portugal). 31^st August – 2^nd September 2023 (Poster)
• Abstracts of national congresses
  • Prandi I, Passarino E, Bellato A, Roch-Dupland O, Bonaffini G, Ottino C, Serpieri M, Mauthe Von Degerfeld M, Quaranta G, Nebbia P, Robino P. Changes in antibiotic resistance levels of Escherichia coli strains from European hedgehogs in a wildlife rescue centre. VI Congresso Nazionale di Ecopatologia della Fauna, Caramanico Terme (Pescara, Italy). 13^th – 16^th November 2024. Accepted
  • Di Profio F, Sarchese V, Capucchio MT, Prandi I, Robetto S, Palombieri A, Quaranta G, Vacchetta M, La Rosa G, Suffredini E, Martella V, Di Martino B. Detection and genomic characterization of a novel Mammarenavirus in European hedgehogs, Italy. 8th National Congress of the Italian Society for Virology, Bologna (Italy). 7^th – 9^th July 2024
  • Prandi I, Colombino E, Perotti M, Cardello M, Ippolito D, Vacchetta M, Bertolotti L, Tomassone L, Zanet S, Mauthe Von Degerfeld M, Quaranta G, Capucchio MT. Gross and histopathological findings in European hedgehogs in Piedmont region: preliminary data. 76^th SISVET Congress, Bari (Italy). 21^st-23^rd June 2023 (Poster)
  • Prandi I, Colombino E, Perotti M, Cardello M, Vacchetta M, Bertolotti L, Tomassone L, Mauthe Von Degerfeld M, Quaranta G, Capucchio MT. Causes of admission, mortality and gross pathology in European hedgehogs in Piedmont region: preliminary data. V Congresso Nazionale di Ecopatologia della Fauna, Udine (Italy). 14^th – 17^th September 2022 (Oral presentation)
  • Prandi I, Capucchio MT, Colombino E, Perotti M, Cardello M, Bertolotti L, Mauthe Von Degerfeld M, Quaranta G, Tomassone L. Detection of vector-borne bacteria in tissue samples from European hedgehogs in the Piedmont region (Italy)”. V Congresso Nazionale di Ecopatologia della Fauna, Udine (Italy). 14^th – 17^th September 2022 (Poster)

Products not related to the PhD project

• Articles journals with impact factor
  • Prandi I, Bellato A, Nebbia P, Stella MC, Ala U, Mauthe von Degerfeld M, Quaranta G, Robino P. Antibiotic-resistant Escherichia coli in wild birds hospitalised in a wildlife rescue centre. Comp Immunol Microbiol Infect Dis. 2023 Feb; 93:101945. doi:10.1016/j.cimid.2023.101945.
• Abstracts of international congress
  • Ottino C, Bonaffini G, Serpieri M, Prandi I, Monti F, Ricci A, Mauthe Von Degerfeld M, Quaranta G. Containment of hybrid wolf through surgical infertilization in Life Wolfalps EU Project. Turkish & Italian Joint International Animal Reproduction Congress, Kemer (Turkey). 10^th – 13^th October 2024.
• Abstracts of national congresses
  • Ottino C, Scandone L, Serpieri M, Bonaffini G, Prandi I, Quaranta G, Mauthe von Degerfeld M. A non-surgical approach to prolonged constipation in an Indian python (Python molurus). 76^th SISVET Congress, Bari (Italy). 21^st-23^rd June 2023
  • Bonaffini G, Serpieri M, Ottino C, Quaranta G, Scandone L, Prandi I, Mauthe von Degerfeld M. Trattamento chirurgico di adenocarcinoma apocrino nel criceto siberiano (Phodopus sungorus): tre casi. 2023 Congresso Internazionale Scivac Rimini, Rimini (Italy). 26^th -28^th May 2023
  • Prandi I, Quaranta G, Bonaffini G, Ottino C, Serpieri M, Scandone L, Capucchio MT, Mauthe von Degerfeld M. Activity of a university clinic (C.A.N.C.) in the recovery of wildlife. V Congresso Nazionale di Ecopatologia della Fauna, Udine (Italy). 14^th – 17^th September 2022.
  • Serpieri M, Bonaffini G, Scandone L, Quaranta G, Ottino C, Prandi I, Mauthe von Degerfeld M. Containment of nutria through surgical infertilization. V Congresso Nazionale di Ecopatologia della Fauna, Udine (Italy). 14^th – 17^th September 2022.
  • Bonaffini G, Serpieri M, Scandone L, Ottino C, Prandi I, Quaranta G, Mauthe von Degerfeld M. External fixation to correct a bilateral tibiotarsal fracture in a common buzzard (Buteo buteo)”, V Congresso Nazionale di Ecopatologia della Fauna, September 14-17 2022.
  • Colombino E, Prandi I, Quaranta G, Mauthe von Degerfeld M, Capucchio MT. Main causes of death in insectivorous bats in Turin province. 75^th Convegno SISVet, Lodi (Bergamo, Italy). 15^th - 18th June 2022.
  • Bonaffini G, Scandone L, Ottino C, Colombino C, Serpieri M, Prandi I, Quaranta G, Mauthe von Degerfeld M. Rabbit ovariectomy with Airplasma technology. 75^th Convegno SISVet, Lodi (Bergamo, Italy). 15^th - 18th June 2022.
  • Serpieri M, Scandone L, Ottino C, Bonaffini G, Prandi I, Quaranta G, Mauthe von Degerfeld M. Amputazione di un arto pelvico in un Ceratophrys ornata. 2022 Congresso Internazionale Scivac Rimini, Rimini (Italy). 27^th -29^th May 2022