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Canine circovirus (CanineCV) is a recently identified virus affecting both domestic and wild carnivores, including foxes, sometimes in presence of severe clinical signs. Its circulation in wild animals can thus represent a potential threat for endangered species conservation and an infection source for dogs. Nevertheless, no data were available on its circulation in the Alps region of Northern Italy. In the present study, samples collected from 186 foxes in the period 2009–2020 from Valle d’Aosta and Veneto regions were tested using a real-time PCR assay, demonstrating a viral circulation of approximatively 2–5%, depending on the considered regions. Two complete or almost complete genome sequences were obtained, highlighting that the detected strains were part of a so defined “fox only” clade, which suggests that, despite common contact opportunities, Alps foxes are not involved in frequent transmission events to domestic dogs. Such genetic isolation could be at least partially attributed to some sort of independent evolution occurred in the foxes, leading to species barrier. Additionally, CanineCV strains in foxes from Italy were unexpectedly related to those previously identified in foxes from the United Kingdom and Scandinavian area. Combining the history of fox distribution in Europe since the last glacial maximum (LGM) with the viral history allowed us to speculate a long-standing coexistence between European canine circovirus and this host, justifying the peculiar geographic distribution and evolutionary paths of the fox infecting clade.
Giovanni Franzo; Maria Menandro; Claudia Tucciarone; Giacomo Barbierato; Lorenzo Crovato; Alessandra Mondin; Martina Libanora; Federica Obber; Riccardo Orusa; Serena Robetto; Carlo Citterio; Laura Grassi. Canine Circovirus in Foxes from Northern Italy: Where Did It All Begin? Pathogens 2021, 10, 1002 .
AMA StyleGiovanni Franzo, Maria Menandro, Claudia Tucciarone, Giacomo Barbierato, Lorenzo Crovato, Alessandra Mondin, Martina Libanora, Federica Obber, Riccardo Orusa, Serena Robetto, Carlo Citterio, Laura Grassi. Canine Circovirus in Foxes from Northern Italy: Where Did It All Begin? Pathogens. 2021; 10 (8):1002.
Chicago/Turabian StyleGiovanni Franzo; Maria Menandro; Claudia Tucciarone; Giacomo Barbierato; Lorenzo Crovato; Alessandra Mondin; Martina Libanora; Federica Obber; Riccardo Orusa; Serena Robetto; Carlo Citterio; Laura Grassi. 2021. "Canine Circovirus in Foxes from Northern Italy: Where Did It All Begin?" Pathogens 10, no. 8: 1002.
The control of infectious bronchitis (IB) is essential in intensive broiler production and is pursued through strict biosecurity and mass vaccination. Despite effective and routinely adopted, hatchery spray vaccination has been hypothesized to affect chicks’ body temperature and wellbeing. Recently, gel administration has been proposed as an alternative and proved feasible in experimental settings. In this study, IBV spray and gel vaccination methods were compared in field conditions. One hundred birds from the same hatch were enrolled in the study and vaccinated, half by spray and half by gel, with 793B and Mass vaccines. After vaccination, rectal temperature was measured and vaccine intake assessed. The two groups were housed for 35 days in separate pens and swabs and blood samples were collected at multiple time points for genotype-specific molecular analyses and serology, respectively. The temperature was significantly lower in spray-vaccinated chicks 10 min and an hour after administration. A similar trend in 793B titres was observed in both groups, while the Mass vaccine was detected later but persisted longer in gel-vaccinated chicks. No differences were observed in mean antibody titres. Compared to spray, gel administration appears equally effective and less impactful on body temperature, thus supporting its application for IBV vaccination.
Matteo Legnardi; Henrik Baranyay; Csanád Simon; János Molnár; Tiede Bijlsma; Mattia Cecchinato; András Gáspárdy; András Bersényi; Claudia Tucciarone; Giovanni Franzo; László Kőrösi. Infectious Bronchitis Hatchery Vaccination: Comparison between Traditional Spray Administration and a Newly Developed Gel Delivery System in Field Conditions. Veterinary Sciences 2021, 8, 145 .
AMA StyleMatteo Legnardi, Henrik Baranyay, Csanád Simon, János Molnár, Tiede Bijlsma, Mattia Cecchinato, András Gáspárdy, András Bersényi, Claudia Tucciarone, Giovanni Franzo, László Kőrösi. Infectious Bronchitis Hatchery Vaccination: Comparison between Traditional Spray Administration and a Newly Developed Gel Delivery System in Field Conditions. Veterinary Sciences. 2021; 8 (8):145.
Chicago/Turabian StyleMatteo Legnardi; Henrik Baranyay; Csanád Simon; János Molnár; Tiede Bijlsma; Mattia Cecchinato; András Gáspárdy; András Bersényi; Claudia Tucciarone; Giovanni Franzo; László Kőrösi. 2021. "Infectious Bronchitis Hatchery Vaccination: Comparison between Traditional Spray Administration and a Newly Developed Gel Delivery System in Field Conditions." Veterinary Sciences 8, no. 8: 145.
Feline panleukopenia is a severe disease of cats caused by feline parvovirus (FPV), and marginally canine parvovirus (CPV). Despite being less rapid than CPV, FPV evolution deserves attention, especially since outbreaks of particular severity are currently reported. This apparently different virulence needs monitoring from genetic and clinical points of view. This manuscript explored FPV molecular epidemiology at both Italian and international levels and the possible association between viral phylogeny and disease severity. Sequences from clinical cases of feline panleukopenia in Italy were obtained from 2011 to 2019, and the etiological agent was characterized, distinguishing FPV from CPV. Phylogenetic and phylodynamic analyses were conducted on Italian and international sequences. Moreover, the association between the viral sequence and clinical variables was evaluated on a group of highly characterized patients. After its origin in the 1920s, FPV showed a constant population size until a more recent expansion since 2000. Few long-distance introduction events characterized FPV spreading, however, most of its evolution occurred locally. Although without a strong statistical association, several clinical variables appeared influenced by viral phylogeny, suggesting a differential virulence potentially characterizing FPV strains. These results stress the importance of the continuous study of viral evolution and its repercussions on the disease clinical aspects.
Claudia Tucciarone; Giovanni Franzo; Matteo Legnardi; Elena Lazzaro; Andrea Zoia; Matteo Petini; Tommaso Furlanello; Marco Caldin; Mattia Cecchinato; Michele Drigo. Genetic Insights into Feline Parvovirus: Evaluation of Viral Evolutionary Patterns and Association between Phylogeny and Clinical Variables. Viruses 2021, 13, 1033 .
AMA StyleClaudia Tucciarone, Giovanni Franzo, Matteo Legnardi, Elena Lazzaro, Andrea Zoia, Matteo Petini, Tommaso Furlanello, Marco Caldin, Mattia Cecchinato, Michele Drigo. Genetic Insights into Feline Parvovirus: Evaluation of Viral Evolutionary Patterns and Association between Phylogeny and Clinical Variables. Viruses. 2021; 13 (6):1033.
Chicago/Turabian StyleClaudia Tucciarone; Giovanni Franzo; Matteo Legnardi; Elena Lazzaro; Andrea Zoia; Matteo Petini; Tommaso Furlanello; Marco Caldin; Mattia Cecchinato; Michele Drigo. 2021. "Genetic Insights into Feline Parvovirus: Evaluation of Viral Evolutionary Patterns and Association between Phylogeny and Clinical Variables." Viruses 13, no. 6: 1033.
Background Infectious bronchitis virus (IBV) is one of the most relevant viruses affecting the poultry industry, and several studies have investigated the factors involved in its biological cycle and evolution. However, very few of those studies focused on the effect of genome composition and the codon bias of different IBV proteins, despite the remarkable increase in available complete genomes. In the present study, all IBV complete genomes were downloaded (n = 383), and several statistics representative of genome composition and codon bias were calculated for each protein-coding sequence, including but not limited to, the nucleotide odds ratio, relative synonymous codon usage and effective number of codons. Additionally, viral codon usage was compared to host codon usage based on a collection of highly expressed genes in IBV target and nontarget tissues. Results The results obtained demonstrated a significant difference among structural, non-structural and accessory proteins, especially regarding dinucleotide composition, which appears under strong selective forces. In particular, some dinucleotide pairs, such as CpG, a probable target of the host innate immune response, are underrepresented in genes coding for pp1a, pp1ab, S and N. Although genome composition and dinucleotide bias appear to affect codon usage, additional selective forces may act directly on codon bias. Variability in relative synonymous codon usage and effective number of codons was found for different proteins, with structural proteins and polyproteins being more adapted to the codon bias of host target tissues. In contrast, accessory proteins had a more biased codon usage (i.e., lower number of preferred codons), which might contribute to the regulation of their expression level and timing throughout the cell cycle. Conclusions The present study confirms the existence of selective forces acting directly on the genome and not only indirectly through phenotype selection. This evidence might help understanding IBV biology and in developing attenuated strains without affecting the protein phenotype and therefore immunogenicity.
Giovanni Franzo; Claudia Maria Tucciarone; Matteo Legnardi; Mattia Cecchinato. Effect of genome composition and codon bias on infectious bronchitis virus evolution and adaptation to target tissues. BMC Genomics 2021, 22, 1 -12.
AMA StyleGiovanni Franzo, Claudia Maria Tucciarone, Matteo Legnardi, Mattia Cecchinato. Effect of genome composition and codon bias on infectious bronchitis virus evolution and adaptation to target tissues. BMC Genomics. 2021; 22 (1):1-12.
Chicago/Turabian StyleGiovanni Franzo; Claudia Maria Tucciarone; Matteo Legnardi; Mattia Cecchinato. 2021. "Effect of genome composition and codon bias on infectious bronchitis virus evolution and adaptation to target tissues." BMC Genomics 22, no. 1: 1-12.
Differently from alpha- and betaherpesviruses affecting swine, interest in the recently discovered Suid gammaherpesvirus 3, Suid gammaherpesvirus 4, and Suid gammaherpesvirus 5, also known as porcine lymphotropic herpesviruses (PLHV-1, PLHV-2, and PLHV-3), has largely focused on their role as potential zoonotic agents in cases of xenotransplantation. However, their role as primary pathogens of swine or as co-factors for other lymphotropic infections has essentially been neglected. The present study aims at filling this gap, evaluating the association between PLHVs infection and different clinical conditions and/or porcine circovirus (PCV) co-infection. One hundred seventy-six samples were obtained from different animals located in a high-density pig area of Northern Italy in the period 2017–2020. The presence of PLHVs and PCVs was tested and quantified by specific real-time PCR: PLHVs were widespread among pigs (PLHV-1, PLHV-2, and PLHV-3 prevalence was 28.97%, 10.79%, and 4.54%, respectively) and detected in all considered tissues and clinical conditions. Frequent co-infections were also observed among PLHVs and with PCVs, although a significant association was not detected with the exception of a positive interaction between PLHV-1 and PLHV-3, and a negative one between PLHV-2 and PCV-2. Significantly, no association between PLHVs, alone or in co-infection, emerged with any of the considered clinical signs, their frequency being comparable between healthy and diseased animals. Based on these pieces of evidence and despite their high prevalence, PLHVs’ relevance for the swine industry appears negligible, either as primary pathogens or as predisposing factors for circovirus-induced diseases.
Giovanni Franzo; Michele Drigo; Matteo Legnardi; Laura Grassi; Maria Luisa Menandro; Daniela Pasotto; Mattia Cecchinato; Claudia Maria Tucciarone. Porcine Gammaherpesviruses in Italian Commercial Swine Population: Frequent but Harmless. Pathogens 2021, 10, 47 .
AMA StyleGiovanni Franzo, Michele Drigo, Matteo Legnardi, Laura Grassi, Maria Luisa Menandro, Daniela Pasotto, Mattia Cecchinato, Claudia Maria Tucciarone. Porcine Gammaherpesviruses in Italian Commercial Swine Population: Frequent but Harmless. Pathogens. 2021; 10 (1):47.
Chicago/Turabian StyleGiovanni Franzo; Michele Drigo; Matteo Legnardi; Laura Grassi; Maria Luisa Menandro; Daniela Pasotto; Mattia Cecchinato; Claudia Maria Tucciarone. 2021. "Porcine Gammaherpesviruses in Italian Commercial Swine Population: Frequent but Harmless." Pathogens 10, no. 1: 47.
Bovine coronavirus (BoCV) is an important pathogen of cattle, causing severe enteric disease and playing a role in the bovine respiratory disease complex. Similar to other coronaviruses, a remarkable variability characterizes both its genome and biology. Despite their potential relevance, different aspects of the evolution of BoCV remain elusive. The present study reconstructs the history and evolution of BoCV using a phylodynamic approach based on complete genome and spike protein sequences. The results demonstrate high mutation and recombination rates affecting different parts of the viral genome. In the spike gene, this variability undergoes significant selective pressures—particularly episodic pressure—located mainly on the protein surface, suggesting an immune-induced selective pressure. The occurrence of compensatory mutations was also identified. On the contrary, no strong evidence in favor of host and/or tissue tropism affecting viral evolution has been proven. The well-known plasticity is thus ascribable to the innate broad viral tropism rather than mid- or long-term adaptation. The evaluation of the geographic spreading pattern clearly evidenced two clusters: a European cluster and an American–Asian cluster. While a relatively dense and quick migration network was identified in the former, the latter was dominated by the primary role of the United States (US) as a viral exportation source. Since the viral spreading pattern strongly mirrored the cattle trade, the need for more intense monitoring and preventive measures cannot be underestimated as well as the need to enforce the vaccination of young animals before international trade, to reduce not only the clinical impact but also the transferal and mixing of BoCV strains.
Giovanni Franzo; Michele Drigo; Matteo Legnardi; Laura Grassi; Daniela Pasotto; Maria Luisa Menandro; Mattia Cecchinato; Claudia Maria Tucciarone. Bovine Coronavirus: Variability, Evolution, and Dispersal Patterns of a No Longer Neglected Betacoronavirus. Viruses 2020, 12, 1285 .
AMA StyleGiovanni Franzo, Michele Drigo, Matteo Legnardi, Laura Grassi, Daniela Pasotto, Maria Luisa Menandro, Mattia Cecchinato, Claudia Maria Tucciarone. Bovine Coronavirus: Variability, Evolution, and Dispersal Patterns of a No Longer Neglected Betacoronavirus. Viruses. 2020; 12 (11):1285.
Chicago/Turabian StyleGiovanni Franzo; Michele Drigo; Matteo Legnardi; Laura Grassi; Daniela Pasotto; Maria Luisa Menandro; Mattia Cecchinato; Claudia Maria Tucciarone. 2020. "Bovine Coronavirus: Variability, Evolution, and Dispersal Patterns of a No Longer Neglected Betacoronavirus." Viruses 12, no. 11: 1285.
Outbreaks of inclusion body hepatitis (IBH) and adenoviral gizzard erosion have been anecdotally reported in Greece since approximately 2011. However, a relevant increase in clinical outbreaks compatible with IBH has been described since 2014. Unfortunately, with limited exceptions, only serological assays were performed, and involved strains were not properly characterized. In the present study, 35 outbreaks were investigated in the period between July 2017 and February 2018 in Greece. In addition to clinical and histopathological diagnosis, fowl adenovirus (FAdV) presence was investigated by PCR and sequencing. Thirty-four out of 35 samples tested FAdV positive. Twenty-nine (85.29%) and 5 (14.71%) strains were classified as FAdV-E and FAdV-D, respectively. Fowl adenovirus-E strains were genetically homogeneous and formed an independent cluster of Greek-only sequences, including the sole previously available sequence, suggesting the prolonged circulation of this species in Greece. On the contrary, FAdV-D strains were more heterogeneous and closely related to strains sampled in other European countries, testifying the occurrence of multiple introduction events. The evaluation of phylogenetic relationships, geographic clustering, age of infection, and origin of the broiler breeder flocks suggests that both vertical and horizontal transmission are important in FAdV epidemiology in Greece and highlights the limited efficacy of currently implemented control measures. Of note, a significantly higher mortality was observed in precociously infected flocks, likely because of the higher susceptibility of younger animals. This evidence stresses the need of preventing vertical and/or early infection to limit the economic impact of adenovirus-induced diseases.
Giovanni Franzo; Zoi Prentza; Thomas Paparounis; Vasilios Tsiouris; Giovanni Centonze; Matteo Legnardi; Elena Catelli; Claudia Maria Tucciarone; Konstantinos Koutoulis; Mattia Cecchinato. Molecular epidemiology of fowl adenoviruses in Greece. Poultry Science 2020, 99, 5983 -5990.
AMA StyleGiovanni Franzo, Zoi Prentza, Thomas Paparounis, Vasilios Tsiouris, Giovanni Centonze, Matteo Legnardi, Elena Catelli, Claudia Maria Tucciarone, Konstantinos Koutoulis, Mattia Cecchinato. Molecular epidemiology of fowl adenoviruses in Greece. Poultry Science. 2020; 99 (11):5983-5990.
Chicago/Turabian StyleGiovanni Franzo; Zoi Prentza; Thomas Paparounis; Vasilios Tsiouris; Giovanni Centonze; Matteo Legnardi; Elena Catelli; Claudia Maria Tucciarone; Konstantinos Koutoulis; Mattia Cecchinato. 2020. "Molecular epidemiology of fowl adenoviruses in Greece." Poultry Science 99, no. 11: 5983-5990.
In the present study one hundred and sixteen partial G gene sequences of Avian metapneumovirus (aMPV) subtype B, obtained during routine diagnostics in different European Countries in the last few years (2014‐2019), were analysed by sequence and phylogenetic analyses in order to draw an updated picture of the molecular characteristics of circulating strains. Nucleotide sequences were compared with other sequences of European and non‐European aMPV‐Bs collected prior to that period or retrieved from GenBank. Phylogenetic relationships among the aMPV‐B strains, reconstructed using the Maximum Likelihood method implemented in MEGA X, demonstrated that aMPV‐B has evolved in Europe from its first appearance, frequently displaying a clear relation with the geographic area of detection. The 40% of aMPV‐B viruses analysed were classified as vaccine‐derived strains, being phylogenetically related, and showing high nucleotide identity with live commercial vaccine strains licensed in Europe. The remaining 60% were classified as field strains since they clustered separately and showed a low nucleotide identity with vaccines and vaccine‐derived strains. The phylogenetic tree showed that the virus has continued to evolve from its first appearance in the ’80s since more recently detected strains belonged to clades phylogenetically distant from the older strains. Unlike vaccine‐derived strains, field strains tended to cluster according to their geographic origin and irrespective of the host species where the viruses had been detected. In conclusion, the molecular characterization of aMPV‐B and the differentiation between vaccines and field strains through G gene sequence analysis can be a useful tool towards correct diagnosis and should be routinely applied in order to better address the control strategies.
Giulia Mescolini; Caterina Lupini; Giovanni Franzo; Giulia Quaglia; Matteo Legnardi; Mattia Cecchinato; Claudia Maria Tucciarone; Angela Blanco; Vincent Turblin; Mar Biarnés; Fabrizio Tatone; Marco Falchieri; Elena Catelli. What is new on molecular characteristics of Avian metapneumovirus strains circulating in Europe? Transboundary and Emerging Diseases 2020, 68, 1314 -1322.
AMA StyleGiulia Mescolini, Caterina Lupini, Giovanni Franzo, Giulia Quaglia, Matteo Legnardi, Mattia Cecchinato, Claudia Maria Tucciarone, Angela Blanco, Vincent Turblin, Mar Biarnés, Fabrizio Tatone, Marco Falchieri, Elena Catelli. What is new on molecular characteristics of Avian metapneumovirus strains circulating in Europe? Transboundary and Emerging Diseases. 2020; 68 (3):1314-1322.
Chicago/Turabian StyleGiulia Mescolini; Caterina Lupini; Giovanni Franzo; Giulia Quaglia; Matteo Legnardi; Mattia Cecchinato; Claudia Maria Tucciarone; Angela Blanco; Vincent Turblin; Mar Biarnés; Fabrizio Tatone; Marco Falchieri; Elena Catelli. 2020. "What is new on molecular characteristics of Avian metapneumovirus strains circulating in Europe?" Transboundary and Emerging Diseases 68, no. 3: 1314-1322.
Avian Metapneumovirus (aMPV) has been recognized as a respiratory pathogen of turkey and chickens for a long time. Recently, a crescent awareness of aMPV, especially subtype B, clinical and economic impact has risen among European researchers and veterinarians. Nevertheless, the knowledge of its epidemiology and evolution is still limited. In the present study, the broadest available collection of partial G gene sequences obtained from European aMPV-B strains was analyzed using different phylodynamic and biostatistical approaches to reconstruct the viral spreading over time and the role of different hosts on its evolution. After aMPV-B introduction, approximatively in 1985 in France, the infection spread was relatively quick, involving the Western and Mediterranean Europe until the end of the 1990s, and then spreading westwards at the beginning of the new millennium, in parallel with an increase of viral population size. In the following period, a wider mixing among aMPV-B strains detected in eastern and western countries could be observed. Most of the within-country genetic heterogeneity was ascribable to single or few introduction events, followed by local circulation. This, combined with the high evolutionary rate herein demonstrated, led to the establishment of genetically and phenotypically different clusters among countries, which could affect the efficacy of natural or vaccine-induced immunity and should be accounted for when planning control measure implementation. On the contrary, while a significant strain exchange was proven among turkey, guinea fowl and chicken, no evidence of differential selective pressures or specific amino-acid mutations was observed, suggesting that no host adaptation is occurring.
Giovanni Franzo; Matteo Legnardi; Giulia Mescolini; Claudia Maria Tucciarone; Caterina Lupini; Giulia Quaglia; Elena Catelli; Mattia Cecchinato. Avian Metapneumovirus subtype B around Europe: a phylodynamic reconstruction. Veterinary Research 2020, 51, 1 -10.
AMA StyleGiovanni Franzo, Matteo Legnardi, Giulia Mescolini, Claudia Maria Tucciarone, Caterina Lupini, Giulia Quaglia, Elena Catelli, Mattia Cecchinato. Avian Metapneumovirus subtype B around Europe: a phylodynamic reconstruction. Veterinary Research. 2020; 51 (1):1-10.
Chicago/Turabian StyleGiovanni Franzo; Matteo Legnardi; Giulia Mescolini; Claudia Maria Tucciarone; Caterina Lupini; Giulia Quaglia; Elena Catelli; Mattia Cecchinato. 2020. "Avian Metapneumovirus subtype B around Europe: a phylodynamic reconstruction." Veterinary Research 51, no. 1: 1-10.
RNA viruses are characterized by high mutation and recombination rates, which allow a rapid adaptation to new environments. Most of the emerging diseases and host jumps are therefore sustained by these viruses. Rapid evolution may also hinder the understanding of molecular epidemiology, affect the sensitivity of diagnostic assays, limit the vaccine efficacy and favor episodes of immune escape, thus significantly complicating the control of even well-known pathogens. The history of infectious bronchitis virus (IBV) fits well with the above-mentioned scenario. Despite being known since the 1930s, it still represents one of the main causes of disease and economic losses for the poultry industry. A plethora of strategies have been developed and applied over time, with variable success, to limit its impact. However, they have rarely been evaluated objectively and on an adequate scale. Therefore, the actual advantages and disadvantages of IBV detection and control strategies, as well as their implementation, still largely depend on individual sensibility. The present manuscript aims to review the main features of IBV biology and evolution, focusing on their relevance and potential applications in terms of diagnosis and control.
Matteo Legnardi; Claudia Maria Tucciarone; Giovanni Franzo; Mattia Cecchinato. Infectious Bronchitis Virus Evolution, Diagnosis and Control. Veterinary Sciences 2020, 7, 79 .
AMA StyleMatteo Legnardi, Claudia Maria Tucciarone, Giovanni Franzo, Mattia Cecchinato. Infectious Bronchitis Virus Evolution, Diagnosis and Control. Veterinary Sciences. 2020; 7 (2):79.
Chicago/Turabian StyleMatteo Legnardi; Claudia Maria Tucciarone; Giovanni Franzo; Mattia Cecchinato. 2020. "Infectious Bronchitis Virus Evolution, Diagnosis and Control." Veterinary Sciences 7, no. 2: 79.
Infectious bronchitis virus (IBV) control is mainly based on wide vaccine administration. Although effective, its efficacy is not absolute, the viral circulation is not prevented and some side effects cannot be denied. Despite this, the determinants of IBV epidemiology and the factors affecting its circulation are still largely unknown and poorly investigated. In the present study, 361 IBV QX (the most relevant field genotype in Italy) sequences were obtained between 2012 and 2016 from the two main Italian integrated poultry companies. Several biostatistical and bioinformatics approaches were used to reconstruct the history of the QX genotype in Italy and to assess the effect of different environmental, climatic and social factors on its spreading patterns. Moreover, two structured coalescent models were considered in order to investigate if an actual compartmentalization occurs between the two integrated poultry companies and the role of a third “ghost” deme, representative of minor industrial poultry companies and the rural sector. The obtained results suggest that the integration of the poultry companies is an effective barrier against IBV spreading, since the strains sampled from the two companies formed two essentially-independent clades. Remarkably, the only exceptions were represented by farms located in the high densely populated poultry area of Northern Italy. The inclusion of a third deme in the model revealed the likely role of other poultry companies and rural farms (particularly concentrated in Northern Italy) as sources of strain introduction into one of the major poultry companies, whose farms are mainly located in the high densely populated poultry area of Northern Italy. Accordingly, when the effect of different environmental and urban parameters on IBV geographic spreading was investigated, no factor seems to contribute to IBV dispersal velocity, being poultry population density the only exception. Finally, the different viral population pattern observed in the two companies over the same time period supports the pivotal role of management and control strategies on IBV epidemiology. Overall, the present study results stress the crucial relevance of human action rather than environmental factors, highlighting the direct benefits that could derive from improved management and organization of the poultry sector on a larger scale.
Giovanni Franzo; Claudia Maria Tucciarone; Ana Moreno; Matteo Legnardi; Paola Massi; Giovanni Tosi; Tiziana Trogu; Raffaella Ceruti; Patrizia Pesente; Giovanni Ortali; Luigi Gavazzi; Mattia Cecchinato. Phylodynamic analysis and evaluation of the balance between anthropic and environmental factors affecting IBV spreading among Italian poultry farms. Scientific Reports 2020, 10, 1 -11.
AMA StyleGiovanni Franzo, Claudia Maria Tucciarone, Ana Moreno, Matteo Legnardi, Paola Massi, Giovanni Tosi, Tiziana Trogu, Raffaella Ceruti, Patrizia Pesente, Giovanni Ortali, Luigi Gavazzi, Mattia Cecchinato. Phylodynamic analysis and evaluation of the balance between anthropic and environmental factors affecting IBV spreading among Italian poultry farms. Scientific Reports. 2020; 10 (1):1-11.
Chicago/Turabian StyleGiovanni Franzo; Claudia Maria Tucciarone; Ana Moreno; Matteo Legnardi; Paola Massi; Giovanni Tosi; Tiziana Trogu; Raffaella Ceruti; Patrizia Pesente; Giovanni Ortali; Luigi Gavazzi; Mattia Cecchinato. 2020. "Phylodynamic analysis and evaluation of the balance between anthropic and environmental factors affecting IBV spreading among Italian poultry farms." Scientific Reports 10, no. 1: 1-11.
Porcine circovirus 2 (PCV-2) is one of the most impactful and widespread pathogens of the modern swine industry. Unlike other DNA viruses, PCV-2 is featured by a remarkable genetic variability, which has led to the emergence and recognition of different genotypes, some of which (PCV-2a, 2b, and 2d) have alternated over time. Currently, PCV-2d is considered the most prevalent genotype, and some evidence of differential virulence and vaccine efficacy have been reported. Despite the potential practical relevance, the data on PCV-2 epidemiology in Italy are quite outdated and do not quantify the actual circulation of this genotype in Italy. In the present study, 82 complete ORF2 sequences were obtained from domestic pigs and wild boars sampled in Northern Italy in the period 2013–2018 and merged with those previously obtained from Italy and other countries. A combination of phylogenetic, haplotype network, and phylodynamic analyses were used to genotype the collected strains and evaluate the temporal trend and the spatial and host spread dynamics. A rising number of PCV-2d detections was observed in domestic pigs, particularly since 2013, reaching a detection frequency comparable to PCV-2b. A similar picture was observed in wild boars, although a lower sequence number was available. Overall, the present study demonstrates the extreme complexity of PCV-2 molecular epidemiology in Italy, the significant spread across different regions, the recurrent introduction from foreign countries, and the frequent occurrence of recombination events. Although a higher viral flux occurred from domestic to wild populations than vice versa, wild boars seem to maintain PCV-2 infection and spread it over relatively long distances.
Giovanni Franzo; Susanna Tinello; Laura Grassi; Claudia Maria Tucciarone; Matteo Legnardi; Mattia Cecchinato; Giorgia Dotto; Alessandra Mondin; Marco Martini; Daniela Pasotto; Maria Luisa Menandro; Michele Drigo. Free to Circulate: An Update on the Epidemiological Dynamics of Porcine Circovirus 2 (PCV-2) in Italy Reveals the Role of Local Spreading, Wild Populations, and Foreign Countries. Pathogens 2020, 9, 221 .
AMA StyleGiovanni Franzo, Susanna Tinello, Laura Grassi, Claudia Maria Tucciarone, Matteo Legnardi, Mattia Cecchinato, Giorgia Dotto, Alessandra Mondin, Marco Martini, Daniela Pasotto, Maria Luisa Menandro, Michele Drigo. Free to Circulate: An Update on the Epidemiological Dynamics of Porcine Circovirus 2 (PCV-2) in Italy Reveals the Role of Local Spreading, Wild Populations, and Foreign Countries. Pathogens. 2020; 9 (3):221.
Chicago/Turabian StyleGiovanni Franzo; Susanna Tinello; Laura Grassi; Claudia Maria Tucciarone; Matteo Legnardi; Mattia Cecchinato; Giorgia Dotto; Alessandra Mondin; Marco Martini; Daniela Pasotto; Maria Luisa Menandro; Michele Drigo. 2020. "Free to Circulate: An Update on the Epidemiological Dynamics of Porcine Circovirus 2 (PCV-2) in Italy Reveals the Role of Local Spreading, Wild Populations, and Foreign Countries." Pathogens 9, no. 3: 221.
Background Canine parvovirus (CPV) represents one of the major infections in dogs. While supportive therapy significantly reduces mortality, other approaches have been reported to provide significant benefits. Unfortunately, the high cost of these treatments is typically a limiting factor. Consequently, a reliable prognostic tool allowing for an informed therapeutic approach would be of great interest. However, current methods are essentially based on ‘a priori’ selection of predictive variables, which could limit their predictive potential. Methods In the present study, the predictive performances in terms of CPV enteritis survival likelihood of an operator-validated logistic regression were compared with those of more flexible methods featured by automatic variable selection. Several anamnestic, clinical, haematological and biochemical parameters were collected from 134 dogs at admission in a veterinary practice. Animal status was monitored until dismissal or death (mortality=21.6%). Results The best automatic variable selection method (random forest) showed excellent discriminatory capabilities (AUC=0.997, sensitivity=0.941 and specificity=1) compared with the logistic regression model (AUC=0.831, sensitivity=0.882 and specificity=0.652), when evaluated on a fully independent test data set. The implemented approaches allowed to identify antithrombin, serum aspartate aminotransferase, serum lipase, monocyte and lymphocyte count as the clinical parameter combination with the highest predictive capability, thus limiting the panel of required tests. Conclusion The model validated in the present study allows prompt prediction of disease severity at admission and provides objective and reliable criteria to support the clinician in selection of the therapeutic approach.
Giovanni Franzo; Barbara Corso; Claudia Maria Tucciarone; Michele Drigo; Marco Caldin; Mattia Cecchinato. Comparison and validation of different models and variable selection methods for predicting survival after canine parvovirus infection. Veterinary Record 2020, 187, 1 .
AMA StyleGiovanni Franzo, Barbara Corso, Claudia Maria Tucciarone, Michele Drigo, Marco Caldin, Mattia Cecchinato. Comparison and validation of different models and variable selection methods for predicting survival after canine parvovirus infection. Veterinary Record. 2020; 187 (9):1.
Chicago/Turabian StyleGiovanni Franzo; Barbara Corso; Claudia Maria Tucciarone; Michele Drigo; Marco Caldin; Mattia Cecchinato. 2020. "Comparison and validation of different models and variable selection methods for predicting survival after canine parvovirus infection." Veterinary Record 187, no. 9: 1.
Infectious bronchitis (IB), caused by infectious bronchitis virus (IBV), account for severe economic losses in the poultry industry. The continuous emergence of a multitude of IBV variants poses many challenges for its diagnosis and control, and live attenuated vaccines, despite their routine use, still plays a significant role in driving IBV evolution, further complicating the epidemiological scenario. Unfortunately, the impact of different vaccination strategies on IB control, epidemiology, and diagnosis has rarely been investigated. This work presents the results of a large-scale diagnostic survey performed in Poland to study IBV molecular epidemiology and how vaccination may affect the viral circulation in the field. To this purpose, 589 samples were collected between May 2017 and January 2019, tested by reverse transcription-PCR for IBV and sequenced. Vaccine and field strains were discriminated based on genetic and anamnestic information. The most commonly detected lineages were 793B (79%) and variant 2 (17.4%), with sporadic detections of QX, Mass, and D274-like strains. Most of the detected strains had a vaccine origin: 46.3% matched one of the applied vaccines, while 36.5% were genetically related to vaccines not implemented in the respective protocol. Besides their practical value for the proper planning of vaccination protocols in Poland, these results suggest that only a fraction (17.2%) of the circulating strains are field ones, imposing a careful assessment of the actual IBV field menaces. Moreover, phenomena like vaccine spreading and persistence seem to occur commonly, stressing the need to further study the epidemiological consequences of the extensive use of live vaccines.
Matteo Legnardi; Giovanni Franzo; Konstantinos C. Koutoulis; Marek Wiśniewski; Elena Catelli; Claudia Maria Tucciarone; Mattia Cecchinato. Vaccine or field strains: the jigsaw pattern of infectious bronchitis virus molecular epidemiology in Poland. Poultry Science 2019, 98, 6388 -6392.
AMA StyleMatteo Legnardi, Giovanni Franzo, Konstantinos C. Koutoulis, Marek Wiśniewski, Elena Catelli, Claudia Maria Tucciarone, Mattia Cecchinato. Vaccine or field strains: the jigsaw pattern of infectious bronchitis virus molecular epidemiology in Poland. Poultry Science. 2019; 98 (12):6388-6392.
Chicago/Turabian StyleMatteo Legnardi; Giovanni Franzo; Konstantinos C. Koutoulis; Marek Wiśniewski; Elena Catelli; Claudia Maria Tucciarone; Mattia Cecchinato. 2019. "Vaccine or field strains: the jigsaw pattern of infectious bronchitis virus molecular epidemiology in Poland." Poultry Science 98, no. 12: 6388-6392.
Despite the fact that vaccine resistance has been typically considered a rare phenomenon, some episodes of vaccine failure have been reported with increasing frequency in intensively-raised livestock. Infectious bronchitis virus (IBV) is a widespread avian coronavirus, whose control relies mainly on extensive vaccine administration. Unfortunately, the continuous emergence of new vaccine-immunity escaping variants prompts the development of new vaccines. In the present work, a molecular epidemiology study was performed to evaluate the potential role of homologous vaccination in driving IBV evolution. This was undertaken by assessing IBV viral RNA sequences from the ORF encoding the S1 portion of viral surface glycoprotein (S) before and after the introduction of a new live vaccine on broiler farms in northern-Italy. The results of several biostatistics analyses consistently demonstrate the presence of a higher pressure in the post-vaccination period. Natural selection was detected essentially on sites located on the protein surface, within or nearby domains involved in viral attachment or related functions. This evidence strongly supports the action of vaccine-induced immunity in conditioning viral evolution, potentially leading to the emergence of new vaccine-escape variants. The great plasticity of rapidly-evolving RNA-viruses in response to human intervention, which extends beyond the poultry industry, is demonstrated, claiming further attention due to their relevance for animal and especially human health.
Giovanni Franzo; Matteo Legnardi; Claudia Maria Tucciarone; Michele Drigo; Marco Martini; Mattia Cecchinato. Evolution of infectious bronchitis virus in the field after homologous vaccination introduction. Veterinary Research 2019, 50, 1 -9.
AMA StyleGiovanni Franzo, Matteo Legnardi, Claudia Maria Tucciarone, Michele Drigo, Marco Martini, Mattia Cecchinato. Evolution of infectious bronchitis virus in the field after homologous vaccination introduction. Veterinary Research. 2019; 50 (1):1-9.
Chicago/Turabian StyleGiovanni Franzo; Matteo Legnardi; Claudia Maria Tucciarone; Michele Drigo; Marco Martini; Mattia Cecchinato. 2019. "Evolution of infectious bronchitis virus in the field after homologous vaccination introduction." Veterinary Research 50, no. 1: 1-9.
Respiratory diseases like infectious bronchitis virus (IBV) and avian metapneumovirus (aMPV) have been held accountable for major losses for poultry production. Nevertheless, scarce information was present dealing with the prevalence and molecular epidemiology of these infections in Greece and the efficacy of currently applied control strategies. To fill this gap, a specific epidemiological study was designed. A total of 106 broiler and layer farms, including 10 backyard and 96 commercial flocks, were sampled between March 2016 and May 2017, and the obtained tracheal swabs were tested for IBV and aMPV using RT-PCR based techniques followed by sequencing. For each farm, data regarding production type, flock features, clinical signs, and vaccination program were also recorded. Different associations between vaccination protocol, production type, animal category, birds density, age, presence of clinical signs, and IBV and/or aMPV infection were tested. Both IBV and aMPV field strain prevalence were proven high, approximately 20 and 30%, respectively, being the GI-19 lineage (14 out of 19; 73.6%) and B subtype (30 out of 30; 100%), the most commonly detected IBV and aMPV genetic types. Infection with IBV field strains was significantly associated with clinical sign presence (odds ratio = 8.55 [95CI = 2.17–42.90]). Remarkably, only the vaccination protocol involving a double vaccination at 1 D of age was proven protective against IBV-induced symptomatology, with the odds of developing disease being 4.14 [95CI = 1.34–14.51] times lower.
Marianna Andreopoulou; Giovanni Franzo; Claudia M Tucciarone; Zoi Prentza; Konstantinos Koutoulis; Mattia Cecchinato; Ilias Chaligianni. Molecular epidemiology of infectious bronchitis virus and avian metapneumovirus in Greece. Poultry Science 2019, 98, 5374 -5384.
AMA StyleMarianna Andreopoulou, Giovanni Franzo, Claudia M Tucciarone, Zoi Prentza, Konstantinos Koutoulis, Mattia Cecchinato, Ilias Chaligianni. Molecular epidemiology of infectious bronchitis virus and avian metapneumovirus in Greece. Poultry Science. 2019; 98 (11):5374-5384.
Chicago/Turabian StyleMarianna Andreopoulou; Giovanni Franzo; Claudia M Tucciarone; Zoi Prentza; Konstantinos Koutoulis; Mattia Cecchinato; Ilias Chaligianni. 2019. "Molecular epidemiology of infectious bronchitis virus and avian metapneumovirus in Greece." Poultry Science 98, no. 11: 5374-5384.
After its first identification in 1978, canine parvovirus (CPV) has been recognized all around the world as a major threat for canine population health. This ssDNA virus is characterized by a high substitution rate and several genetic and phenotypic variants emerged over time. Overall, the definition of 3 main antigenic variants was established based on specific amino acid markers located in a precise capsid position. However, the detection of several minor variants and incongruence observed between the antigenic classification and phylogeny have posed doubts on the reliability of this scheme. At the same time, CPV heterogeneity has favored the hypothesis of a differential virulence among variants, although no robust and consistent demonstration has been provided yet. The present study rejects the antigenic variant concept and attempts to evaluate the association between CPV strain phylogeny, reconstructed using the whole information contained in the VP2 coding gene, and several clinical and hemato-biochemical parameters, assessed from 34 CPV infected dogs at admission. By using different statistical approaches, the results of the present study show an association between viral phylogeny and host parameters ascribable to immune system, coagulation profile, acute phase response and, more generally, to the overall picture of the animal response. Particularly, a strong and significant phylogenetic signal was proven for neutrophil count and WBC. Therefore, despite the limited sample size, a relation between viral phylogeny and disease severity has been observed for the first time, suggesting that CPV virulence is an inherited trait. The likely existence of clades with different virulence highlights once more the relevance of intensive epidemiological monitoring and research on CPV evolution to better understand the virulence determinants, their epidemiology and develop adequate countermeasures.
Giovanni Franzo; Claudia Maria Tucciarone; Sira Casagrande; Marco Caldin; Martí Cortey; Tommaso Furlanello; Matteo Legnardi; Mattia Cecchinato; Michele Drigo. Canine parvovirus (CPV) phylogeny is associated with disease severity. Scientific Reports 2019, 9, 1 -8.
AMA StyleGiovanni Franzo, Claudia Maria Tucciarone, Sira Casagrande, Marco Caldin, Martí Cortey, Tommaso Furlanello, Matteo Legnardi, Mattia Cecchinato, Michele Drigo. Canine parvovirus (CPV) phylogeny is associated with disease severity. Scientific Reports. 2019; 9 (1):1-8.
Chicago/Turabian StyleGiovanni Franzo; Claudia Maria Tucciarone; Sira Casagrande; Marco Caldin; Martí Cortey; Tommaso Furlanello; Matteo Legnardi; Mattia Cecchinato; Michele Drigo. 2019. "Canine parvovirus (CPV) phylogeny is associated with disease severity." Scientific Reports 9, no. 1: 1-8.
Porcine circovirus 3 (PCV‐3) has emerged as a potential threat for swine industry, being consistently reported in presence of several clinical signs all around the world. Recently, its presence in wild boar has been demonstrated at high prevalence. This evidence is surprising since the lower density of wild populations might not be expected to sustain such efficient viral transmission. Porcine circoviruses were proven to exhibit a certain plasticity in the host tropism and were detected in unrelated species, like mice, dogs and ruminants. However, if this scenario applies also to wild animals remains to be established. Therefore, the present study aimed to investigate the presence of PCV‐3 in wild ungulates other than wild boar and in related hematophagous ectoparasites. One‐hundred and nine animals were sampled from different hilly and mountain areas of Friuli Venezia Giulia, including 9 chamois (Rupicapra rupicapra), 17 red deer (Cervus elaphus), 4 mouflons (Ovis musimon), 50 roe deer (Capreolus capreolus) and 29 wild boars (Sus scrofa). Additionally, host matched ectoparasites were collected when present. PCV‐3 was diagnosed using molecular techniques and sequencing. The present study results confirmed the high PCV‐3 occurrence in wild boar and reported for the first time its presence, at low prevalence, in chamois and roe deer. Moreover two ticks (Ixodes ricinus), one of which non‐engorged, collected from PCV‐3 negative roe deer, tested PCV‐3 positive. The genetic characterization of some of the strains collected from non‐swine hosts allowed to prove that, albeit clearly part of PCV‐3 species, they were genetically unique, demonstrating the absence of among‐samples contamination and thus confirming the actual presence of PCV‐3 genome in these new hosts. Therefore, the present study highlights an unexpected broad PCV‐3 distribution and circulation in the wild, rising further questions on porcine circoviruses infectious cycle, epidemiology and origin, which will deserve additional investigations. This article is protected by copyright. All rights reserved.
Giovanni Franzo; Laura Grassi; Claudia Maria Tucciarone; Michele Drigo; Marco Martini; Daniela Pasotto; Alessandra Mondin; Maria Luisa Menandro. A wild circulation: High presence of Porcine circovirus 3 in different mammalian wild hosts and ticks. Transboundary and Emerging Diseases 2019, 66, 1548 -1557.
AMA StyleGiovanni Franzo, Laura Grassi, Claudia Maria Tucciarone, Michele Drigo, Marco Martini, Daniela Pasotto, Alessandra Mondin, Maria Luisa Menandro. A wild circulation: High presence of Porcine circovirus 3 in different mammalian wild hosts and ticks. Transboundary and Emerging Diseases. 2019; 66 (4):1548-1557.
Chicago/Turabian StyleGiovanni Franzo; Laura Grassi; Claudia Maria Tucciarone; Michele Drigo; Marco Martini; Daniela Pasotto; Alessandra Mondin; Maria Luisa Menandro. 2019. "A wild circulation: High presence of Porcine circovirus 3 in different mammalian wild hosts and ticks." Transboundary and Emerging Diseases 66, no. 4: 1548-1557.
The genetic variability of Infectious bronchitis virus (IBV) is one of the main challenges for its control, hindering not only the development of effective vaccination strategies but also its classification and, consequently, epidemiology understanding. The 624/I and Q1 genotypes, now recognized to be part of the GI-16 lineage, represent an excellent example of the practical consequences of IBV molecular epidemiology limited knowledge. In fact, being their common origin unrecognized for a long time, independent epidemiological pictures were drawn for the two genotypes. To fix this misinterpretation, the present study reconstructs the history, population dynamics and spreading patterns of GI-16 lineage as a whole using a phylodynamic approach. A collection of worldwide available hypervariable region 1 and 2 (HVR12) and 3 (HVR3) sequences of the S1 protein was analysed together with 258 HVR3 sequences obtained from samples collected in Italy (the country where this genotype was initially identified) since 1963. The results demonstrate that after its emergence at the beginning of the XX century, GI-16 was able to persist until present days in Italy. Approximately in the late 1980s, it migrated to Asia, which became the main nucleus for further spreading to Middle East, Europe and especially South America, likely through multiple introduction events. A remarkable among-country diffusion was also demonstrated in Asia and South America. Interestingly, although most of the recent Italian GI-16 strains originated from ancestral viruses detected in the same country, a couple were closely related to Chinese ones, supporting a backward viral flow from China to Italy. Besides to the specific case-study results, this work highlights the misconceptions that originate from the lack of a unified nomenclature and poor molecular epidemiology data generation and sharing. This shortcoming appears particularly relevant since the described scenario could likely be shared by many other IBV genotypes and pathogens in general.
Giovanni Franzo; Mattia Cecchinato; Giovanni Tosi; Laura Fiorentini; Francesca Faccin; Claudia Maria Tucciarone; Tiziana Trogu; Ilaria Barbieri; Paola Massi; Ana Moreno. GI-16 lineage (624/I or Q1), there and back again: The history of one of the major threats for poultry farming of our era. PLOS ONE 2018, 13, e0203513 .
AMA StyleGiovanni Franzo, Mattia Cecchinato, Giovanni Tosi, Laura Fiorentini, Francesca Faccin, Claudia Maria Tucciarone, Tiziana Trogu, Ilaria Barbieri, Paola Massi, Ana Moreno. GI-16 lineage (624/I or Q1), there and back again: The history of one of the major threats for poultry farming of our era. PLOS ONE. 2018; 13 (12):e0203513.
Chicago/Turabian StyleGiovanni Franzo; Mattia Cecchinato; Giovanni Tosi; Laura Fiorentini; Francesca Faccin; Claudia Maria Tucciarone; Tiziana Trogu; Ilaria Barbieri; Paola Massi; Ana Moreno. 2018. "GI-16 lineage (624/I or Q1), there and back again: The history of one of the major threats for poultry farming of our era." PLOS ONE 13, no. 12: e0203513.
Infectious bronchitis (IB) control has a strong impact on poultry farming, because of the necessary epidemiological knowledge for planning the best strategy, the optimal strain association, the priming and boosting interventions. Broiler farming is even more problematic given the short and intense productive cycle, which requires an early onset of protection against most of the infectious threats, possibly with limited respiratory post-vaccination reactions that would have a direct impact on the bird health and productivity. For this purpose, gel vaccination has been proposed as a new approach for infectious bronchitis virus (IBV) control and vaccine intake, kinetics and compatibility of combined strains administered by gel have been analyzed in this study. After gel vaccination with single and combined 1/96 and B-48 strains on 4 groups of commercial broilers, a 21-d-long experimental trial has been conducted to monitor the vaccine safety by clinical assessment and vaccine kinetics by strain-specific real-time RT-PCR on choanal cleft swabs. The vaccine strains administered by gel were safe and negligible respiratory signs were detected, even when combined. Vaccine titers were compared among groups and within the same group among a 10-bird pooled sample and 10 swabs from individually sampled birds. 1/96 strain early reached high titers in all animals, while B-48 presence was less constant even though it was detected in almost all birds before the trial end. The individual and pooled sample comparison revealed a partial overestimation of vaccine titers in the pooled samples and the loss of the prevalence data, although the trend portrayed by the pooled swabs closely followed the individual ones.
Claudia Maria Tucciarone; Giovanni Franzo; Alice Bianco; Giacomo Berto; Gema Ramon; Pascal Paulet; Konstantinos Koutoulis; Mattia Cecchinato. Infectious bronchitis virus gel vaccination: evaluation of Mass-like (B-48) and 793/B-like (1/96) vaccine kinetics after combined administration at 1 day of age. Poultry Science 2018, 97, 3501 -3509.
AMA StyleClaudia Maria Tucciarone, Giovanni Franzo, Alice Bianco, Giacomo Berto, Gema Ramon, Pascal Paulet, Konstantinos Koutoulis, Mattia Cecchinato. Infectious bronchitis virus gel vaccination: evaluation of Mass-like (B-48) and 793/B-like (1/96) vaccine kinetics after combined administration at 1 day of age. Poultry Science. 2018; 97 (10):3501-3509.
Chicago/Turabian StyleClaudia Maria Tucciarone; Giovanni Franzo; Alice Bianco; Giacomo Berto; Gema Ramon; Pascal Paulet; Konstantinos Koutoulis; Mattia Cecchinato. 2018. "Infectious bronchitis virus gel vaccination: evaluation of Mass-like (B-48) and 793/B-like (1/96) vaccine kinetics after combined administration at 1 day of age." Poultry Science 97, no. 10: 3501-3509.