From Poultry to Wild Birds and Mammals: The Genetic Evolution of the HPAI H5N1 Virus and the Growing Concern Over Potential Human-to-Human Transmission 

Highly Pathogenic Avian Influenza (HPAI) A (H5Nx) viruses belonging to the A/Goose/Guangdong/1/1996 (Gs/Gd) lineage were first identified in China in 1996 and have since rapidly evolved into one of the major global health threats. Since the early 2000s, H5Nx viruses have caused severe and numerous outbreaks in poultry populations, resulting in substantial economic losses. Moreover, these viruses have demonstrated the capacity to infect a broad range of wild bird species and mammals, including humans (1).

Until 1997, highly pathogenic avian influenza viruses (HPAI) were confined to poultry, and outbreaks could be controlled effectively through culling of infected animals and preventive vaccination of healthy flocks. Prior to this, HPAI viruses had not spread to wild birds, which therefore played no role in virus transmission between domestic and wild avian populations (1).

Frequent replication and reassortment events between HPAI H5 viruses of the Gs/Gd lineage and low pathogenic avian influenza (LPAI) viruses circulating in wild birds have profoundly altered the genetic sequence encoding the hemagglutinin (HA) protein. This genetic diversification led to the emergence of multiple distinct evolutionary lineages, known as “clades” and “subclades”—groups of viruses closely related by common genetic features, descending from a shared ancestor (1).

From its initial localized presence in Southeast Asia, the virus rapidly expanded its geographic range. Since 2003, HPAI H5 Gs/Gd viruses have become enzootic in several countries across South and Southeast Asia (1). A crucial event occurred in 2005 with a large-scale mass mortality event among migratory birds at Qinghai Lake, China. This incident marked the onset of intercontinental spread of the Gs/Gd lineage, with the virus appearing for the first time in Europe and Africa during the autumn bird migration (1).

From 2005 onwards, the virus has spread extensively throughout Asia, Europe, Africa, and North America, becoming a global threat to poultry and endangered wild bird species. Concurrently, the zoonotic risk increased, with 976 confirmed human infections recorded from 2003 through May 2025, resulting in 470 mortalities, including one case in the United States reported on 6 January 2025. In Europe, only six human infections have been documented recently, all in the United Kingdom (2).

Currently, the clade 2.3.4.4, which emerged in China in 2008, plays a dominant role worldwide. This clade has been responsible for the most severe HPAI outbreaks in Europe during the epidemic waves of 2016–2017, 2020–2021, 2021–2022, 2022–2023 (3), and 2023–2024 (4), causing significant mortality in both domestic and wild birds. Additionally, sporadic involvement of various mammalian species has been observed since the 2020–2021 outbreak and continues to the present. During the summer of 2022, severe die-offs were recorded among wild birds, including marine species that had not been affected previously (3).


Global Impact

Starting from January 2021, an A(H5N1) virus closely related to strains circulating in Europe during the 2020–2021 epidemic spread to West Africa, subsequently reaching countries in Southern Africa (3). By the end of the same year, several A(H5N1) viruses belonging to clade 2.3.4.4b, genetically similar to those identified in Northern Europe, were also reported in South and East Asia as well as in North America.

In early 2022, a new introduction of the A(H5N1) virus, this time originating from Japan, was documented in North America. Here, the virus rapidly acquired new genetic segments through reassortment events with endemic low pathogenic avian influenza (LPAI) viruses circulating in wild North American birds (3).

In October of the same year, the virus reached Mexico and shortly thereafter South America, causing mass mortality events not only in poultry and wild birds but also affecting several mammalian species, including marine mammals. The Atlantic and Pacific coasts of the Americas experienced an unprecedented epizootic, particularly severe in Argentina, Chile, and Peru, with documented episodes of mammal-to-mammal transmission (5).

The overall picture outlined by the World Organisation for Animal Health (WOAH) clearly reflects the extent of the intercontinental spread of the HPAI H5 Gs/Gd lineage: between 2005 and 2024, these viruses have caused the loss—due to mortality or culling—of approximately 633 million farmed birds, peaking at 146 million in 2022, followed by a slight decrease in 2024 (6).

The growing international concern is driven by the ongoing geographic expansion of HPAI, which reached Latin America for the first time in 2022 and, more recently, even Antarctica in 2024 (7). The persistent circulation of clade 2.3.4.4b has promoted the emergence of numerous viral genotypes, resulting from frequent reassortment events between HPAI and LPAI viruses. Each new genotype exhibits a unique combination of its eight genomic segments (PB2, PB1, PA, HA, NP, NA, NS, M), with potential implications for both pathogenicity and adaptation to new hosts (3).

According to the Avian Influenza Overview September–December 2024 report (4), prepared by EFSA, ECDC, and the European Union Reference Laboratory for Avian Influenza and Newcastle Disease (EURL AI/ND) at the Istituto Zooprofilattico Sperimentale delle Venezie (IZSVe), a new increase in avian influenza cases among wild birds was recorded during the autumn months of 2024, coinciding with the start of the migratory season, along the coasts of Europe. However, the overall number of cases remained lower compared to the same periods in 2022 and 2023 (4). The most affected areas were in Central-Southern Europe, characterized by a high density of poultry farms.

In particular, the A(H5N5) virus, responsible for mortality events in wild birds, expanded its range both geographically and in terms of host species, involving 17 bird species including the lesser black-backed gull (Larus fuscus), the black-headed gull (Chroicocephalus ridibundus), and the common raven (Corvus corax) (4).

In Europe, from December 2024 to March 2025, HPAI (H5N1) viruses were detected in 31 countries, predominantly in central, western, and southern eastern regions. The wild birds most frequently involved belonged to the order Anseriformes, including swans and geese; contact between wild birds and free-range poultry remains the primary driver of virus spillover into domestic settings (7).


The Italian Context and the Case of the Yellow-Legged Gull in the Abruzzo Region

According to the aforementioned Avian Influenza Overview September–December 2024 (4), 23 poultry outbreaks were reported in Italy (22 primary and 1 secondary), all located in the northern regions of the country. A distinguishing feature of the latest epidemic wave was the greater involvement of small rural farms, particularly in the province of Treviso (Veneto Region), where there are no large-scale poultry operations and facilities are more easily accessible to wild birds.

During the same period, a significant increase in wild bird cases was observed across Europe: the number of affected individuals tripled compared to the previous quarter and was approximately one-third higher than during the same period of the previous epidemiological year. The most affected species belonged to the order Anseriformes, mainly detected along major European rivers such as the Danube, Oder, and Po. To a lesser extent, seabirds belonging to the Charadriiformes order were also involved, particularly along the coasts of the Arctic, Atlantic, and North Sea, and more locally along the Adriatic (4).

Within this complex scenario, a noteworthy case occurred in the Abruzzo region (central Italy), where the presence of the HPAI A(H5N1) virus was detected for the first time in a wild bird found within the region’s territory. The bird was a yellow-legged gull (Larus michahellis), discovered in a moribund state in late November 2024 in the town center of Ortona dei Marsi (AQ) (Figure 1), a medieval village nestled within the Abruzzo, Lazio and Molise National Park, specifically in the Marsica area—a historical-geographical region of inland Abruzzo.

The animal—a second-year male weighed approximately 850 grams and had a wingspan of around 140 cm was recovered thanks to the prompt intervention of local veterinary authorities (personal communication, Giulia Pace, Rewilding Apennines). (Figure 2 A and B). A necropsy was performed at the territorial diagnostic facility in Avezzano, part of the Istituto Zooprofilattico Sperimentale dell’Abruzzo e del Molise (IZS-Teramo), in accordance with the procedures established by the 2024 National Avian Influenza Surveillance Program.

Real-time RT-PCRfor/ targeting the M gene was carried out on samples from the brain, trachea, lungs, and intestine at the Virology Department of IZS Teramo, confirming the presence of the HPAI A(H5N1) virus. The samples were subsequently sent to the National and European Reference Laboratory (EURL AI/ND) at the IZSVe, where viral isolation, full genome sequencing, and phylogenetic analysis were performed. The virus was identified as belonging to clade 2.3.4.4b, genotype DI.2.


Figure 1.Map showing the location where the yellow-legged gull tested positive for HPAI H5N1 avian influenza virus in the municipality of Ortona dei Marsi (AQ), Abruzzo region.


Figure 2a.Yellow-legged gull positive for HPAI A(H5N1) avian influenza virus, ventral view.


Figure 2b.Yellow-legged gull positive for HPAI A(H5N1) avian influenza virus, dorsal view.

The presence of a yellow-legged gull in a mountainous area of central Italy—far from typical marine or lacustrine habitats—is not considered unusual. This species is well known for its adaptability to urban and peri-urban environments, including mountain towns, landfills, and agricultural areas. Juvenile individuals, in particular, tend to exhibit erratic dispersal behaviour, making it difficult to determine their area of origin.

Given the absence of active outbreaks in Abruzzo and central Italy at the time of detection, it is plausible that the bird originated from the Upper Adriatic region, where confirmed outbreaks were ongoing, and was migrating toward the lower Tyrrhenian Sea. This hypothesis is supported by previous studies on the migratory routes of yellow-legged gulls, conducted through bird-ringing techniques (8).

Specifically, during the 2024–2025 epidemiological year, between 25 October 2024 and 6 March 2025, a total of 15 yellow-legged gulls tested positive for HPAI A(H5N1) in various Italian provinces, including Venice, Padua, Macerata, Verona, Bologna, Parma, and Rimini. Previous cases had already been documented in the 2021–2022 period (4 in Veneto, 1 Campania) and 2022–2023 (4 in Veneto, 1 in Emilia-Romagna).

Other wild bird species in central and southern Italy have also been affected in recent years. Between 2021 and 2024, cases were reported in birds of prey (in the provinces of Salerno, Naples, and Perugia), as well as in a mute swan and a sandwich tern (in the province of Macerata, Marche region) (9).

All updated data on avian influenza virus circulation in wild birds are available on the Avian Flu Data Portal managed by the EURL AI/ND (EURL AI/ND, 2025. Avian Flu Data Portal https://eurlaidata.izsvenezie.it/).


New Affected Species and Spillover into Mammals

Over the past five years, HPAI viruses—particularly the H5N1 subtype of clade 2.3.4.4b—have shown a concerning ability to expand their host range well beyond domestic and wild birds. Since November 2020, numerous spillover events have been reported in mammals, spanning various regions of the world and diverse ecological settings.

As of September 2024, more than 700 HPAI infections have been documented in 73 different mammalian species, excluding humans. The most frequently affected taxonomic families include canids, felids, small carnivores, marine mammals, and more recently, bovids—especially dairy cattle in the United States (10).

For the first time since spring 2024, multiple detections of HPAI virus have occurred in domestic cats and wild carnivores in Europe (7).

The genetic evolution of the virus—driven by reassortment events and constant selective pressure in high-density animal environments—appears to have increased its ability to infect non-avian species, with significant implications for both animal and public health. Some of these cases involved exposed workers who developed mild forms of the disease, and the detection of infections in bridge species such as pigs has reignited concerns about a potential pandemic emergence.

The main events reported globally are as follows:

  • March 2024, Texas (USA) – First isolation of HPAI H5N1 clade 2.3.4.4b in dairy cattle exhibiting hypogalactia. The virus was identified as genotype B3.13, likely resulting from transmission by wild birds (11).
  • 6 January 2025, Louisiana (USA) – The first human fatality due to HPAI H5N1 in the United States, associated with genotype DI.1, heightened international concern regarding the virus’s pandemic potential (12).
  • 27 January 2025, West Midlands (United Kingdom), Europe – Isolation of the virus in a symptomatic man working at a poultry farm infected with HPAI H5N1 clade 2.3.4.4b, genotype DI.2. This genotype was the most prevalent in Europe during the 2024–2025 epidemic wave (13).
  • 31 January 2025, Nevada (USA) – Second independent event of direct transmission from wild bird to bovine, with isolation of genotype D1.1, already known to circulate among migratory birds, poultry, and marine mammals (14).
  • 13 February 2025, Arizona (USA) – Third event, similar to the one on 31 January, involving the isolation of a genetically distinct D1.1 virus, confirming the likelihood of multiple independent introductions from wildlife (14).
  • 24 March 2025, Yorkshire (United Kingdom), Europe – First isolation of HPAI H5N1 clade 2.3.4.4b virus from sheep milk (16).

In its 17 April 2025 report (14), the FAO-WHO-WOAH joint group stated that the risk of an H5N1 influenza A virus emergency is considered low for the general public, and low to moderate for individuals occupationally exposed, depending on the risk mitigation measures in place and the local epidemiological situation. Currently, there is no documented evidence of sustained human-to-human transmission of avian influenza viruses, although sporadic cases have been observed in the past between infected individuals and their caregivers (14).


Genetic Evolution of the Virus: Recent Mutations and Emerging Genotypes

During the 2023–2024 epidemiological year, genetic surveillance of circulating HPAI A(H5Nx) viruses in Europe revealed an evolving landscape characterized by the emergence and spread of new genotypes, while critical mutations associated with human adaptation remained relatively stable.

Between September and December 2024, reduced genetic diversity was observed among viruses circulating in Europe, with four predominant genotypes:

  • A(H5N1) EA-2022-BB
  • A(H5N1) EA-2023-DT
  • A(H5N1) EA-2024-DI
  • A(H5N5) EA-2021-I

Among these, the EA-2024-DI genotype assumed a central role, emerging at the end of 2023 and initially spreading in Eastern Europe. From September 2024 onwards, this genotype became the most frequently detected across Europe, particularly in Central and Eastern Europe. Molecular analyses revealed the presence of two subgroups within the DI genotype: DI.1 and DI.2. Both subgroups were isolated in Austria, Germany, Italy, and the United Kingdom, albeit with a geographically differentiated distribution among European countries (4).

From October 2024 to March 2025, the full genome sequences of approximately 600 HPAI A(H5) clade 2.3.4.4b viruses, primarily isolated from domestic birds and Anseriformes, were studied. Of these, 85% belonged to the EA-2024-DI genotype, with 90% of that subset classified as the DI.2 subtype (7).

Regarding mutations of zoonotic relevance, molecular analyses of circulating viruses in birds from October 2023 to March 2025 did not detect critical changes in the hemagglutinin (HA) cleavage site, such as those observed in previous influenza pandemics; thus, circulating viruses maintain strong avian species specificity (4; 7).

Since October 2024, some mutations in the PB2 protein, which enhance viral adaptability to mammals, have been observed in 35 viruses isolated from birds in Europe. Compared to the 2023–2024 epidemiological year, there appears to be an increased frequency of mutations in this protein (7).

Regarding the viruses isolated from cattle in the United States, genetic analyses of genotypes B3.13 and D1.1, isolated up to March 1, 2025, exclusively in North America, have revealed distinct characteristics:

  • Some D1.1 viruses isolated from cattle exhibit a mutation in the PB2 protein that increases the virus's adaptability to mammals; however, this mutation is absent in isolates from wild birds and poultry (14).
  • As of March 1, 2025, none of the viruses isolated from cattle possess mutations in the HA protein that significantly enhance the virus's ability to bind human receptors (14).
  • Sporadically, mutations compromising the efficacy of major antiviral drugs used in humans have been observed in genotypes isolated from human cases (14).

The risk of introduction of genotype B3.13 into Europe is considered high. In a recent scientific report, EFSA identified the potential pathways for virus entry into European countries via both the migration of Anseriformes birds passing through the North American Arctic and the importation of dairy cattle, beef, and raw milk-based products (15).


Control Strategies and Integrated Response: The European and Italian Approach to HPAI Virus Infections

The pandemic potential of these viruses requires close surveillance, especially in animal populations where transmission between poultry and mammals has been observed. It is essential that farmers strengthen biosecurity measures on their farms, that governments enforce policies aimed at reducing or eliminating transmission among animals and environmental contamination, and that they communicate risks effectively to workers in poultry operations so they protect themselves with appropriate personal protective equipment (14).

In this context, the international response has evolved. In 2024, the FAO and WOAH updated the Global Strategy for HPAI Avian Influenza (2024–2033), replacing the 2008 version to address the continuous emergence of new strains of the H5 Gs/Gd lineage (17). The new plan adopts a One Health approach, promoting public-private partnerships, the use of innovative tools such as genomic surveillance and AI-based outbreak prediction, and enhanced integration among animal, human, and environmental health sectors (17).

The WHO Global Influenza Surveillance and Response System (GISRS), in collaboration with international animal health organizations (FAO, WOAH, OFFLU, among others), continues to evaluate candidate vaccine viruses for pandemic preparedness (14).

To combat HPAI spread, all EU countries implement coordinated surveillance programs targeting poultry and wild birds, under Regulation (EU) 2016/429, aiming for early diagnosis, virological monitoring, and outbreak prevention in a context increasingly complicated by global ecological, climatic, and epidemiological changes. Recent strengthening of the EU surveillance system includes updated technical guidelines and coordinated response scenarios developed jointly by EFSA, ECDC, and the European Union Reference Laboratory for Avian Influenza and Newcastle Disease (EURL AI/ND). In January 2025, these agencies published a scientific opinion (18) and a One Health operational manual, which features flowcharts to address five potential zoonotic epidemic scenarios (19). In Italy, the national veterinary information system SIMAN, accessible via the Veterinary Information System-Vetinfo portal, integrates multiple veterinary surveillance systems to support digital reporting of avian influenza outbreaks. It includes Web GIS tools for real-time visualization and risk mapping, thus facilitating rapid responses by veterinary services (https://www.vetinfo.it).

In Italy, the national strategy is implemented through the Avian Influenza Surveillance Program – 2024, adopted by Ministerial Decree of 30 May 2023 (20). The program combines active and passive surveillance of poultry and wild birds, in line with EU requirements. Italian provinces are classified according to epidemiological risk: provinces in Abruzzo and central–southern Italy are considered low risk, while those in northern regions (Lombardy, Veneto, Emilia-Romagna, Piedmont)—which account for 70% of poultry farms—are classified as high risk.

National data are transmitted to the EURL AI/ND (IZSVe), which incorporates them into quarterly technical reports prepared jointly with EFSA and ECDC (4; 7). In response to the growing zoonotic risk, the Ministry of Health adopted EU recommendations by issuing an operational circular in 2025 to health and veterinary authorities (21).

Strengthening interdisciplinary cooperation, adopting flexible response tools, and ensuring integration between local, national, and international levels are now key elements for containing the risk posed by HPAI and preparing for future epidemic threats.


Acknowledgements

We would like to thank Valentina Zenobio and Francesca Dall’Acqua for their assistance with the scientific review and content organization.


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Elga Ersilia Tieri1, Berardina Costantini1, Stefania Centi1, Marzia Ciminelli1, Ambra Ciminelli1, Sandro Pelini1, Annamaria Sansone1, Nadia Sulli1, Ilaria Puglia1,2, Marialuigia Caporale1,2, Tetyana Petrova1, Leonardo Gentile3, Stefania Salucci1
1 Istituto Zooprofilattico Sperimentale dell’Abruzzo e del Molise “G. Caporale”
2PhD National Programme in One Health approaches to infectious diseases and life science research, Department of Public Health, Experimental and Forensic Medicine, University of Pavia, 27100, Italy
3Parco Nazionale d’Abruzzo Lazio e Molise, Servizio Veterinario, Pescasseroli (AQ)

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