Pathobiology of avian influenza virus infection in minor gallinaceous species: a review

Figures & data

Table 1. Infectious period, incubation time, and clinical signs following natural or experimental LPAIV infections in minor gallinaceous species.

Species	AIV	Type of infection ^a	Route ^b of infection (dose) ^c	Oral shedding (duration; N/total) ^d	Cloacal shedding (duration; N/total) ^d	Clinical signs (duration; N/total or%) ^e	MDT (N/total or%) ^e	Transmission confirmation	Reference
Japanese quail (Coturnix c. japonica)	H5N2 (2 isolates)	E	IN or IM (10^5.7–5.9)	ND	ND	None	None	Yes	(Alexander et al., 1986)
J. quail	H9N2	E	O + IO + IN + IT (5×10^7). Second challenge with the same dose 14 days after	ND (9 days; 2 to 10/10)	ND	Ruffled feathers, excess mucus, diarrhoea, cyanosis of the tongue, egg dropping (10/10)	None	ND	(Lavoie et al., 2007)
J. quail	Various subtypes	E	IN + O+IO (5×10^6)	6.8 (3 days; 3/3)	3.8 (3 days; 1/3)	Non-specific signs (6/6 of H10)	ND (2/6 of H10)	Yes (H10, H7)	(Makarova et al., 2003)
J. quail	Avian/swine H9N2	E	IN + IT + O (10^7)	4.0 (7 days; 3/3)	None	None	None	Yes	(Perez et al., 2003b)
J. quail	Various H9 subtypes	E	IN + IT + O (5×10^6)	6.0 (7 days; 3/3)	Occasionally	None	None	Yes	(Perez et al., 2003a)
J. quail	H9N2	E	IN (10^6.3)	ND	ND	Up to 60% reduction in egg production, reduction in feed and water consumption. Non-specific signs, diarrhoea, nasal and eye discharges (from 6 dpi)	None	ND	(Nili et al., 2007)
J. quail	H7N6	N	–	ND	ND	None	None	ND	(Sugiura et al., 2009)
J. quail	H9N2	E	IN (10^6.8)	ND	ND	Reduction in egg production, reduction in feed and water consumption. Non-specific signs, diarrhoea, nasal and eye discharges (from 2 to 6 dpi; 100%)	None	Yes	(Ebrahimi et al., 2011)
J. quail	H3N2	E	IN + O (10^6)	3.0 (5 days; 3/5)	H3N2: 0.9 (1 day; 2/5)	None	None	Yes	(Thontiravong et al., 2012b)
J. quail	H9N2	E	ON (10^3, 10^4, 10^5, 10^6)	10^3: 4 days (100%), 10 days (65%); 10^4: 4 days (100%), 10 days (65%), 28 days (1/5); 10^5: 4 days (100%), 10 days (65%), 28 days (1/5); 10^6: 4 days (100%), 10 days (65%), 28 days (1/5)	10^3: 3 days (100%), 7 days (75%); 10^4: 3 days (100%), 7 days (75%); 10^5: 3 days (100%), 7 days (75%); 10^6: 3 days (100%), 7 days (75%), 28 days (2/5)	10^3: depression, impaired breathing (from 4 dpi; 1/5); 10^5: non-specific signs (from 4 dpi; 5/5); 10^6: non-specific signs (from 3 dpi; 5/5)	10^3: 10 dpi (1/5)	Yes	(Bonfante et al., 2013)
European quail (Coturnix c. coturnix)	H7N2	E	IN (10^6)	28.66 Ct ^f (9 days; 8/8)	34.41 Ct ^f (3 days; 1/8)	None	None	Yes	(Bertran et al., 2013)
Ring-necked pheasant (Phasianus colchicus)	Various subtypes	E	IO + IN + IT (10^7)	5.5 (≤10 days; 0 to 3/3) 5.5 (≥14 days; 0 to 3/3)	5.5 (≤10 days; 0 to 3/3) 4.5 (≥14 days; 0 to 3/3)	None	None	Yes	(Humberd et al., 2006)
R. pheasant	H10N9	E	IO + IN + IT (10^7)	ND (10 days; 87.5%)	5.25 (29 days; 0 to 3/3)	None	None	Yes	(Humberd et al., 2007)
Chukar partridge (Alectoris chukar)	Various subtypes	E	ND	6.25 (≤10 days; 0 to 3/3)	3.5 (≤10 days; 0 to 3/3)	None	None	Yes	(Humberd et al., 2006)
C. partridge	H9N2	E	IN + IO (10^7)	ND	ND	Depression, decreased feed and water consumption, coughing and sneezing (5 to 7 dpi)	None	ND	(Nili et al., 2013)
Red-legged partridge (Alectoris rufa)	H7N9	E	IN (10^6)	5.22 (8 days; 1 to 6/8)	2.37 (1 day; 1/8)	None	None	No	(Bertran et al., 2011)
Pearl guineafowl (Numida meleagris)	H7N1	N	–	ND	ND	Conjunctivitis, respiratory signs, neurologic signs	ND (30%)	ND	(Mutinelli et al., 2003)

^a E, experimental; N, natural.

^b Routes: IC, intrachoanal; IM, intramuscular; IN, intranasal; IO, intraocular; IT, intratracheal; NC, nasochoanal; O, oral: ON, oronasal.

^c Dose: in median egg infectious doses (EID₅₀).

^d Maximum oral and cloacal shedding titres are expressed as log₁₀ of mean tissue culture infectious dose (TCID₅₀) or EID₅₀. N/total is the number of infected birds shedding virus over the total number of infected birds. ND, not determined.

^e MDT expressed in dpi N/total or percentage of infected birds exhibiting clinical signs or dying.

^f Results are expressed as cycle threshold (Ct).

Figure 1. Gross lesions in H7N1 HPAIV-infected R. partridges (Bertran et al., 2011). 1a: Kidney lesions consisting of parenchymal pallor, lobular surface architecture and urate deposits in the ureters, 7 dpi 1b: Petechial haemorrhages on the fasciae sheaths of the muscles of rear legs, 8 dpi 1c: Brain congestion, 8 dpi 1d: Thymus atrophy, 7 dpi

Figure 2. Microscopic lesions and positive viral antigen cells in H7N1 HPAIV-infected R. partridges (Bertran et al., 2011). 2a: Kidney and adrenal gland, 5 dpi Necrosis of the tubular epithelial cells of the renal cortex, multifocal to coalescent areas of necrosis of corticotrophic and corticotropic adrenal cells (haematoxylin and eosin [HE]). 2b: Kidney and adrenal gland, 5 dpi Tubular epithelial cells of the kidney, corticotrophic and corticotropic adrenal cells (IHC). 2c: Brain, 5 dpi Focal areas of malacia (HE). 2d: Brain, 5 dpi Neurons, ependymal cells, and glial cells (IHC). 2e: Nasal turbinates, 6 dpi Necrosis of single cells of the olfactory epithelium (HE). 2f: Nasal turbinates, 6 dpi Olfactory epithelial cells (IHC). 2g: Gizzard, 3 dpi Focal areas of degeneration and necrosis of the gastric glands (HE). 2h: Gizzard, 3 dpi Epithelial cells of the gastric glands (IHC).

Figure 3. Distribution of viral antigen in positive tissues of a quail challenged intranasally with H5N1 HPAIV (Bertran et al., 2013). 3a: Brain, 7 dpi 3b: Positive staining in nucleus and cytoplasm of neurons and glial cells. 3c: Heart, 5 dpi 3d: Positive staining in the nucleus and cytoplasm of cardiomyocytes.

Table 2. Infectious period, incubation time, and clinical signs following natural or experimental HPAIV infections in minor gallinaceous species.

Species	AIV	Type of infection ^a	Route ^b of infection (dose) ^c	Oral shedding (duration; N/total) ^d	Cloacal shedding (duration; N/total) ^d	Clinical signs (duration; N/total or%) ^e	MDT (N/total or%) ^e	Transmission confirmation	Reference
Japanese quail (Coturnix c. japonica)	H5 (six isolates)	E	IN or IM (10^5.2 to 10^6.2)	ND	ND	Rare, sudden death (1 to 10/10)	4.8 to 7.7 dpi (1 to 10/10)	Yes	(Alexander et al., 1986)
J. quail	H5N1	E	IN (10^5.8 to 10^6.2)	ND	ND	Lethargy (100%), increased faecal fluids (100%), neurologic signs (2 dpi; 8%)	2 dpi (100%)	ND	(Perkins & Swayne, 2001)
J. quail	H7N1	N	–	ND	ND	Anorexia, lethargy	ND (100%)	ND	(Mutinelli et al., 2003)
J. quail	H5N1	E	IN (10^8)	ND	ND	Neurologic signs (2/6)	2 to 4 dpi (100%)	ND	(Isoda et al., 2006)
J. quail	H5N1	E	IN (10^6.5)	5.0 (5 days)	2.5 (5 days)	Lethargy (100%)	4.8 dpi (100%)	Yes	(Jeong et al., 2009)
J. quail	H5N1	E	IN (10^6)	2.9 (4 days; 3/5)	None	Sudden death (100%)	1 to 3.4 dpi (100%)	ND	(Saito et al., 2009)
J. quail	H5N1 (three isolates: DK383, DK378, DK212)	E	IN (10^6)	DK383: 4.07 (3 days; 2/2); DK378: 3.53 (3 days; 3/3); DK212: 3.12 (3 days; 3/3)	DK383: 4.2 (3 days; 2/2); DK378: 2.78 (3 days; 3/3); DK212: 2.62 (3 days; 3/3)	ND	DK383: 2.3 dpi (100%); DK378: 2.4 dpi (83.3%); DK212: 3 dpi (83.3%)	Yes	(Sun et al., 2011)
European quail (Coturnix c. coturnix)	H7N1	E	IN (10^6)	25.12 Ct ^f (15 days; 8/8)	29.64 Ct ^f (12 days; 6/8)	Non-specific signs towards neurologic signs (6 dpi; 17%), sudden neurologic signs (7 dpi; 17%), sudden death (33%)	6.6 dpi (63%)	Yes	(Bertran et al., 2013)
E. quail	H5N1	E	IN (10^6)	25.25 Ct ^f (9 days; 8/8)	30.91 Ct ^f (4 days; 5/8)	Non-specific signs towards neurological signs (4 dpi; 58%), sudden neurologic signs (5 dpi; 25%), sudden death (8%)	5.3 dpi (88%)	Yes	(Bertran et al., 2013)
Bobwhite quail (Colinus virginianus)	H5N1	E	IN (10^5.8 to 10^6.2)	ND	ND	Lethargy (100%), increased faecal fluids (100%), mucous diarrhoea with strings of urate faeces (100%), neurologic signs (3 dpi; 14%)	2.25 dpi (100%)	ND	(Perkins & Swayne, 2001)
Pearl guinea fowl (Numida meleagris)	H5N1	E	IN (10^5.8 to 10^6.2)	ND	ND	Lethargy (100%), increased faecal fluids (100%), neurologic signs	2.5 dpi (100%)	ND	(Perkins & Swayne, 2001)
P. guinea fowl	H7N1	N	–	ND	ND	Anorexia, lethargy, neurologic signs	ND (100%)	ND	(Mutinelli et al., 2003)
Ring-necked pheasant (Phasianus colchicus)	H5N1	E	IN (10^5.8 to 10^6.2)	ND	ND	Lethargy (100%), increased faecal fluids (100%), mucous diarrhoea with strings of urates faeces (100%), neurologic signs (3 dpi; 13%)	3.25 dpi (100%)	ND	(Perkins & Swayne, 2001)
R. pheasant	H7N1	N	–	ND	ND	Anorexia, lethargy, neurologic signs	ND (100%)	ND	(Mutinelli et al., 2003)
Chukar partridge (Alectoris chukar)	H5N1	E	IN (10^5.8 to 10^6.2)	ND	ND	Lethargy (100%), increased faecal fluids (100%), mucous diarrhoea with strings of urate faeces (100%), neurologic signs (4 dpi; 28%)	4.5 dpi (75%)	ND	(Perkins & Swayne, 2001)
Red-legged partridge (Alectoris rufa)	H7N1	E	IN (10^6)	6.09 (8 days; 100%)	7.28 (7 days; 100%)	Non-specific signs (3 dpi; 100%), neurologic signs (8 dpi; 75%)	6.42 dpi (100%)	Yes	(Bertran et al., 2011)

^a E, experimental; N, natural.

^b Routes: IC, intrachoanal; IM, intramuscular; IN, intranasal; IO, intraocular; IT, intratracheal; NC, nasochoanal; O, oral: ON, oronasal.

^c Dose: in median egg infectious doses (EID₅₀).

^d Maximum oral and cloacal shedding titres are expressed as log₁₀ of mean tissue culture infectious dose (TCID₅₀) or EID₅₀. N/total is the number of infected birds shedding virus over the total number of infected birds. ND: not determined.

^e MDT expressed in dpi N/total or percentage of infected birds exhibiting clinical signs or dying.

^f Results are expressed as cycle threshold (Ct).

Table 3. Gross pathology, histological lesions, and distribution of AIV antigen in minor gallinaceous species following natural or experimental HPAIV infections.

Species	AIV	Type of infection ^a	Route of infection (dose) ^b	Gross pathology	Histological lesions	Distribution of AIV antigen	Reference
Japanese quail (Coturnix c. japonica)	H5N1	E	IN (10^5.8 to 10^6.2)	Pulmonary oedema and congestionSplenomegalyRenomegalyHaemorrhages in enteric lymphoid areasHaemorrhages on epicardium	Nasal epithelial necrosis, rhinitis, sinusitisInterstitial pneumoniaEnteritis, enteric lymphoid depletion, enteric epithelial necrosis, pancreatic necrosisAdrenal necrosisBone marrow cellular depletion and necrosisSpleen, bursa, thymus lymphoid depletionMyocyte necrosisMyocarditisNeuronal necrosis, gliosis	Nasal, sinus epitheliumPulmonary endotheliumPancreatic acinar epitheliumSplenic phagocytes, endotheliumCorticotrophic and cortical cellsMyeloid cellsBursal phagocytic leukocytesThymic epithelium, phagocytesCardiomyocytesBrain neurons, glial cells, ependymal and choroid epitheliumEpithelium of the feather folliclesThecal cells	(Perkins & Swayne, 2001)
J. quail	H7N1	N	–	Pancreatic necrosis	Pancreatic necrosis	Pancreatic acinar epitheliumBrain neurons	(Mutinelli et al., 2003)
J. quail	H5N1	N	–	ND	ND	Epithelium and muscular layer of the trachea	(Antarasena et al., 2006)
						Pulmonary endothelium of the septum
						Mucosal epithelium of the rectum
						Endothelium lining of the spleen
						Renal tubular epithelium
						Cardiomyocytes
						Oviduct epithelium
J. quail	H5N1	E	IN (10^8)	ND	Encephalitis with laminar encephalomalacia	CardiomyocytesBrain neurons	(Isoda et al., 2006)
European quail (Coturnix c. coturnix)	H7N1	E	IN (10^6)	Multifocal petechia on the proventriculus–gizzard junction mucosaSplenomegaly with pallor or parenchymal mottlingPancreatic necrosis	Necrosis and lymphoplasmacytic infiltrate in the gizzardPancreatic lytic necrosis with lymphoplasmacytic infiltrateMyocardial necrosis with lymphoplasmacytic infiltrateNeuronal necrosis, gliosis in brainNecrosis of the ependyma and neuropil of spinal cord	Epithelium of the ventricular glands of the gizzardPancreatic acinar cellsCardiomyocytesBrain neurons, glial cells, ependymal and choroid epithelium	(Bertran et al., 2013)
E. quail	H5N1	E	IN (10^6)	Multifocal petechia on the proventriculus–gizzard junction mucosaSplenomegaly with pallor or parenchymal mottlingPancreatic necrosis	Necrosis and lymphoplasmacytic infiltrate in the gizzardEpithelial degeneration and lymphoplasmacytic infiltrate in rectumRenal necrosis with heterophilic infiltratePancreatic lytic necrosis with lymphoplasmacytic infiltrateMyocardial necrosis with lymphoplasmacytic infiltrateNeuronal necrosis, gliosis in brain	Epithelium of the ventricular glands of the gizzardLamina propria of caecal tonsilMuscularis externa of the lamina propria of rectumPancreatic acinar cellsRenal tubular epitheliumCardiomyocytesBrain neurons, glial cells, ependymal and choroid epithelium	(Bertran et al., 2013)
Bobwhite quail (Colinus virginianus)	H5N1	E	IN (10^5.8 to 10^6.2)	SplenomegalyRenomegalyPulmonary oedema and congestionHaemorrhages in caecal tonsilHaemorrhages on epicardiumPancreatic necrosis	Nasal epithelial necrosisRhinitis, sinusitisInterstitial pneumoniaEnteritis, enteric lymphoid depletionEnteric epithelial necrosisPancreatic necrosisAdrenal necrosisBone marrow cellular depletion and necrosisSpleen, bursa, thymus lymphoid depletionMyocyte necrosisNeuronal necrosis, gliosis	Nasal, sinus epitheliumPulmonary endotheliumPancreatic acinar epitheliumSplenic phagocytes, endotheliumCorticotrophic and cortical cellsMyeloid cellsBursal phagocytic leukocytesThymic epithelium, phagocytesCardiomyocytesBrain neurons, glial cells, ependymal and choroid epitheliumEpithelium of the feather folliclesThecal cells	(Perkins & Swayne, 2001)
Pearl guineafowl (Numida meleagris)	H5N1	E	IN (10^5.8 to 10^6.2)	SplenomegalyRenomegalyPulmonary oedema and congestionHaemorrhages in lymphoid areas of intestinal tractHaemorrhage in bursaHaemorrhage in submucosal lymphoid tissue of the palateHaemorrhage in skeletal muscleHaemorrhages on epicardiumConjunctival hyperaemia and oedema	Nasal epithelial necrosisRhinitis, sinusitisInterstitial pneumoniaEnteritis, enteric lymphoid depletion Enteric epithelial necrosisPancreatic necrosisAdrenal necrosisBone marrow cellular depletion and necrosisSpleen, bursa, thymus lymphoid depletionMyocyte necrosisMyocarditisNeuronal necrosis, gliosisSubcutaneous oedema	Nasal, sinus epitheliumPulmonary endotheliumPancreatic acinar epitheliumSplenic phagocytes, endotheliumCorticotrophic and cortical cellsMyeloid cellsBursal phagocytic leukocytesThymic epithelium, phagocytesCardiomyocytesBrain neurons, glial cells, ependymal and choroid epitheliumEpithelium of the feather folliclesThecal cells	(Perkins & Swayne, 2001)
Ring-necked pheasant (Phasianus colchicus)	H5N1	E	IN (10^5.8 to 10^6.2)	SplenomegalyRenomegalyPulmonary oedema and congestionHaemorrhages in caecal tonsilHaemorrhages in skeletal muscleHaemorrhages on the epicardium	Nasal epithelial necrosisRhinitis, sinusitisInterstitial pneumoniaEnteritis, enteric lymphoid depletionAdrenal necrosisBone marrow cellular depletion and necrosisSpleen, bursa, thymus lymphoid depletionMyocyte necrosisMyocarditisNeuronal necrosis, gliosis	Nasal, sinus epitheliumPulmonary endothelial cellsPancreatic acinar epitheliumSplenic phagocytes, endotheliumCorticotrophic and cortical cellsMyeloid cellsBursal phagocytic leukocytesThymic epithelium, phagocytesCardiomyocytesBrain neurons, glial cells, ependymal and choroid epitheliumEpithelium of the feather folliclesThecal cells	(Perkins & Swayne, 2001)
Chukar partridge (Alectoris chukar)	H5N1	E	IN (10^5.8 to 10^6.2)	SplenomegalyRenomegalyPulmonary oedema and congestionHaemorrhages in caecal tonsilHaemorrhages on epicardiumPancreatic necrosis	Nasal epithelial necrosis, rhinitis, sinusitisInterstitial pneumoniaEnteritis, enteric lymphoid depletion, enteric epithelial necrosisPancreatic necrosisAdrenal necrosisBone marrow cellular depletion and necrosisSpleen, bursa, thymus lymphoid depletionMyocyte necrosisMyocarditisNeuronal necrosis, gliosis	Nasal, sinus epitheliumPulmonary endotheliumPancreatic acinar epitheliumSplenic phagocytes, endotheliumCorticotrophic and cortical cellsMyeloid cellsBursal phagocytic leukocytesThymic epithelium, phagocytesCardiomyocytesBrain neurons, glial cells, ependymal and choroid epitheliumEpithelium of the feather follicles	(Perkins & Swayne, 2001)
Red-legged partridge (Alectoris rufa)	H7N1	E	IN (10^6)	Haemorrhages in rear legs’ musclesThymus atrophyKidney parenchymal pallor with urate deposits in the uretersBrain congestion	Pancreatic necrosis with heterophilic infiltrateRenal necrosis with heterophilic infiltrateAdrenal necrosis with heterophilic infiltrateMyocyte necrosis with heterophilic infiltrateMyocarditis with heterophilic infiltrateNeuronal necrosis, gliosis in brain and spinal cordNecrosis of the epidermal collar epithelium with heterophilic infiltrate	Olfactory and respiratory epithelium of nasal turbinatesPseudostratified epithelium of the tracheaAir capillaries of the lungEpithelium of the gastric glands of the gizzardPancreatic acinar epitheliumCorticotrophic and cortical cellsRenal tubular epitheliumKupffer cellsCardiomyocytesMyocytesBrain neurons, glial cells, ependymal and choroid epitheliumSpinal cord neurons, ependymal cells, leptomeningesEpithelium of the epidermal collar of feather follicles	(Bertran et al., 2011)

ND, not determined.

^a E, experimental; N, natural.

^b Dose: in median egg infectious doses (EID₅₀). Routes: IC, intrachoanal; IM, intramuscular; IN, intranasal; IO, intraocular; IT, intratracheal; NC, nasochoanal; O, oral: ON, oronasal.

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