Emerg Infect Dis . Highly Pathogenic Avian Influenza A(H5N1) Virus Clade 2.3.4.4b Infections in Wild Terrestrial Mammals, United States, 2022

[tetano]

Emerg Infect Dis


. 2023 Dec;29(12):2451-2460.
doi: 10.3201/eid2912.230464.
Highly Pathogenic Avian Influenza A(H5N1) Virus Clade 2.3.4.4b Infections in Wild Terrestrial Mammals, United States, 2022

Elizabeth J Elsmo, Arno Wünschmann, Kimberlee B Beckmen, Liam E Broughton-Neiswanger, Elizabeth L Buckles, Jayne Ellis, Scott D Fitzgerald, Robert Gerlach, Shawna Hawkins, Hon S Ip, Julia S Lankton, Erin M Lemley, Julianna B Lenoch, Mary L Killian, Kristina Lantz, Lindsey Long, Roger Maes, Marta Mainenti, Julie Melotti, Megan E Moriarty, Shotaro Nakagun, Rachel M Ruden, Valerie Shearn-Bochsler, Danielle Thompson, Mia K Torchetti, Arnaud J Van Wettere, Annabel G Wise, Ailam L Lim

• PMID: 37987580
• DOI: 10.3201/eid2912.230464

Abstract

We describe the pathology of natural infection with highly pathogenic avian influenza A(H5N1) virus of Eurasian lineage Goose/Guangdong clade 2.3.4.4b in 67 wild terrestrial mammals throughout the United States during April 1‒July 21, 2022. Affected mammals include 50 red foxes (Vulpes vulpes), 6 striped skunks (Mephitis mephitis), 4 raccoons (Procyon lotor), 2 bobcats (Lynx rufus), 2 Virginia opossums (Didelphis virginiana), 1 coyote (Canis latrans), 1 fisher (Pekania pennanti), and 1 gray fox (Urocyon cinereoargenteus). Infected mammals showed primarily neurologic signs. Necrotizing meningoencephalitis, interstitial pneumonia, and myocardial necrosis were the most common lesions; however, species variations in lesion distribution were observed. Genotype analysis of sequences from 48 animals indicates that these cases represent spillover infections from wild birds.

Keywords: United States; avian influenza; bobcat; clade 2.3.4.4b; coyote; fisher; fox; highly pathogenic avian influenza virus; influenza; influenza A(H5N1); meningitis/encephalitis; opossum; raccoon; respiratory infections; skunk; viruses; wild terrestrial mammals; zoonoses.

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Among the 58 animals found alive, most (n = 54) had neurologic abnormalities, comprising seizures (n = 29), ataxia (n = 23), tremors (n = 17), lack of fear of humans (n = 7), vocalization (n = 5), circling (n = 4), blindness (n = 3), torticollis (n = 2), nystagmus (n = 1), and grimace (n =1) (Appendix Table 3). Less frequently recorded abnormalities were lethargy (n = 28), fever (n = 7), diarrhea (n = 2), unconsciousness (n = 2), recumbence (n = 1), paralysis (n = 1), and vomiting (n = 1). Dyspnea was reported in 2 skunks, 1 bobcat, and 1 red fox.

Figure 2,. Gross photographs of postmortem lesions from red foxes naturally infected with highly pathogenic avian influenza virus, United States. A) Lungs have failed to collapse and are diffusely edematous and mottled...

Gross postmortem observations were recorded in 58 animals. Most animals were in fair to good nutritional condition (n = 39). Lung lesions were consistently observed (n = 49) and included congestion (n = 42), edema (n = 22), failure to collapse (n = 18), hemorrhage (n = 18), and pleural effusion (n = 6) (Figure 2, panel A). The most common brain lesions were hemorrhage (n = 11) and congestion (n = 7). Other lesions included pallor (n = 8), congestion (n = 7), enlargement (n = 6), and hemorrhage (n = 1) in the liver, as well as congestion (n = 4) and cortical hemorrhage (n = 1) in the kidney. Pericardial effusion (n = 3), petechia (n = 2), and myocardial pallor (n = 2) were infrequently noted in the heart (Figure 2, panel B). In the gastrointestinal tract, nematode parasitism was relatively common (n = 15), but other rarely observed lesions included congestion, hemorrhage, and loose feces. Three red foxes had gastric contents that included feathers (Figure 2, panel C). Three red foxes had mild ocular discharge. The gray fox had severe hemorrhage in all body cavities.

Figure 3. Histopathology of lesions in red foxes naturally infected with highly pathogenic avian influenza virus, United States. A) Throughout the brain, there are multifocal regions of necrosis and hypercellularity. Original magnification...

Histopathologic findings were recorded for 55 animals (Table 1; Appendix Table 4). Of 54 animals with >1 section of brain suitable for histopathologic evaluation, all but 2 skunks and the gray fox had brain lesions. The most consistently affected brain region was the frontal lobe (16 animals of 16 tested, 100%), followed by the cerebral cortex (46/53, 87%), brainstem (22/29, 76%), thalamus (20/29, 69%), hippocampus (17/29, 59%), and cerebellum (12/33, 36%). Brain lesions had a multifocal and random distribution, affected gray and white matter, and sometimes exhibited a periventricular distribution. Lesions primarily consisted of regions of malacia and inflammation (Figure 3, panel A). Acidophilic neuronal necrosis was prominent and often associated with satellitosis (Figure 3, panel B) or karyorrhectic debris (Figure 3, panel C). Laminar neuronal necrosis within the hippocampus was striking in some cases (Figure 3, panel D). Low-to-moderate numbers of predominantly lymphocytes and plasma cells infiltrated the leptomeninges and Virchow-Robin spaces, often extending into the parenchyma (Figure 3, panels A, B). In some presumptively subacute lesions, reactive histiocytes predominated. Histopathologic lesions in the brain were absent to mild in all skunks. In the 2 opossum joeys, brain lesions primarily affected the cerebral meninges.

Multifocal necrotizing interstitial pneumonia was the second most commonly reported microscopic lesion (n = 47). Alveoli contained fibrin, edema, hemorrhage, macrophages, and occasionally neutrophils (Figure 3, panel E). Alveolar septa were thickened by neutrophils, macrophages, perivascular lymphocytes and plasma cells, and aggregates of fibrin. Type II pneumocyte hyperplasia was rare, and few animals had bronchopneumonia. Most lung lesions were acute, except in 1 fox and 1 bobcat. Concurrent lungworm parasitism was noted in 3 raccoons, 1 bobcat, and the fisher.

Multifocal myocardial necrosis, most commonly affecting the left ventricular wall, was present in roughly half of the animals (n = 29). Mineralization of affected cardiomyocytes was often noted (Figure 3, panel F). Mild lymphoplasmacytic or histiocytic infiltrates and regions of fibrosis were infrequently reported in conjunction with myocardial necrosis. No heart lesions were observed in the striped skunks, the opossum joeys, the fisher, or the gray fox.

Random foci of acute liquefactive to coagulative hepatic necrosis were observed in 22 animals and in all 5 striped skunks. Dystrophic mineralization of hepatocytes and mixed inflammation associated with regions of necrosis were reported in some cases.
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