The Acquisition and Retention of Lumpy Skin Disease Virus by Blood-Feeding Insects Is Influenced by the Source of Virus, the Insect Body Part, and the Time since Feeding

TY - JOUR

T1 - The Acquisition and Retention of Lumpy Skin Disease Virus by Blood-Feeding Insects Is Influenced by the Source of Virus, the Insect Body Part, and the Time since Feeding

AU - Sanz-Bernardo, Beatriz

AU - Suckoo, Rey

AU - Haga, Ismar R.

AU - Wijesiriwardana, Najith

AU - Harvey, Alice

AU - Basu, Sanjay

AU - Larner, Will

AU - Rooney, Sara

AU - Sy, Victoria

AU - Langlands, Zoe

AU - Denison, Eric

AU - Sanders, Christopher

AU - Atkinson, John

AU - Batten, Carrie

AU - Alphey, Luke

AU - Darpel, Karin E.

AU - Gubbins, Simon

AU - Beard, Philippa M.

N1 - Publisher Copyright: © 2022 American Society for Microbiology. All rights reserved.

PY - 2022/8/10

Y1 - 2022/8/10

N2 - Lumpy skin disease virus (LSDV) is a poxvirus that causes severe systemic disease in cattle and is spread by mechanical arthropod-borne transmission. This study quantified the acquisition and retention of LSDV by four species of Diptera (Stomoxys calcitrans, Aedes aegypti, Culex quinquefasciatus, and Culicoides nubeculosus) from cutaneous lesions, normal skin, and blood from a clinically affected animal. The acquisition and retention of LSDV by Ae. aegypti from an artificial membrane feeding system was also examined. Mathematical models of the data were generated to identify the parameters which influence insect acquisition and retention of LSDV. For all four insect species, the probability of acquiring LSDV was substantially greater when feeding on a lesion compared with feeding on normal skin or blood from a clinically affected animal. After feeding on a skin lesion LSDV was retained on the proboscis for a similar length of time (around 9 days) for all four species and for a shorter time in the rest of the body, ranging from 2.2 to 6.4 days. Acquisition and retention of LSDV by Ae. aegypti after feeding on an artificial membrane feeding system that contained a high titer of LSDV was comparable to feeding on a skin lesion on a clinically affected animal, supporting the use of this laboratory model as a replacement for some animal studies. This work reveals that the cutaneous lesions of LSD provide the high-titer source required for acquisition of the virus by insects, thereby enabling the mechanical vector-borne transmission.

AB - Lumpy skin disease virus (LSDV) is a poxvirus that causes severe systemic disease in cattle and is spread by mechanical arthropod-borne transmission. This study quantified the acquisition and retention of LSDV by four species of Diptera (Stomoxys calcitrans, Aedes aegypti, Culex quinquefasciatus, and Culicoides nubeculosus) from cutaneous lesions, normal skin, and blood from a clinically affected animal. The acquisition and retention of LSDV by Ae. aegypti from an artificial membrane feeding system was also examined. Mathematical models of the data were generated to identify the parameters which influence insect acquisition and retention of LSDV. For all four insect species, the probability of acquiring LSDV was substantially greater when feeding on a lesion compared with feeding on normal skin or blood from a clinically affected animal. After feeding on a skin lesion LSDV was retained on the proboscis for a similar length of time (around 9 days) for all four species and for a shorter time in the rest of the body, ranging from 2.2 to 6.4 days. Acquisition and retention of LSDV by Ae. aegypti after feeding on an artificial membrane feeding system that contained a high titer of LSDV was comparable to feeding on a skin lesion on a clinically affected animal, supporting the use of this laboratory model as a replacement for some animal studies. This work reveals that the cutaneous lesions of LSD provide the high-titer source required for acquisition of the virus by insects, thereby enabling the mechanical vector-borne transmission.

KW - Aedes aegypti

KW - control

KW - Culex quinquefasciatus

KW - Culicoides nubeculosus

KW - flies

KW - lumpy skin disease

KW - midges

KW - mosquitoes

KW - poxvirus

KW - Stomoxys calcitrans

KW - transmission

KW - vector

UR - http://www.scopus.com/inward/record.url?scp=85136339725&partnerID=8YFLogxK

U2 - 10.1128/jvi.00751-22

DO - 10.1128/jvi.00751-22

M3 - Article

C2 - 35867566

AN - SCOPUS:85136339725

SN - 0022-538X

VL - 96

JO - JOURNAL OF VIROLOGY

JF - JOURNAL OF VIROLOGY

IS - 15

M1 - e00751-22

ER -