Evaluation of the cost-effectiveness of ASF detection with or without the use of on-field tests in different scenarios, in Sardinia

Stefano Cappai; Federica Loi; Sandro Rolesu; Annamaria Coccollone; Alberto Laddomada; Francesco Sgarangella; Sergio Masala; Giuseppe Bitti; Vincenzo Floris; Pietro Desini

doi:10.4142/jvs.2020.21.e14

Journal List > J Vet Sci > v.21(2) > 1144493

Go to TopGo to Top Go to BottomGo to Bottom

TOOLS

Cappai, Loi, Rolesu, Coccollone, Laddomada, Sgarangella, Masala, Bitti, Floris, and Desini: Evaluation of the cost-effectiveness of ASF detection with or without the use of on-field tests in different scenarios, in Sardinia

Original Article Epidemiology

J Vet Sci 2020;21(2):e14.

Published online: 4 March 2020

DOI: https://doi.org/10.4142/jvs.2020.21.e14

Evaluation of the cost-effectiveness of ASF detection with or without the use of on-field tests in different scenarios, in Sardinia

Stefano Cappai^1,^2,^*, Federica Loi^1,², Sandro Rolesu^1,², Annamaria Coccollone^1,², Alberto Laddomada², Francesco Sgarangella³, Sergio Masala³, Giuseppe Bitti³, Vincenzo Floris³, Pietro Desini³

¹Osservatorio Epidemiologico Veterinario Regionale della Sardegna, via XX Settembre, 09125 Cagliari, Italy

²Istituto Zooprofilattico Sperimentale della sardegna “G.Pegreffi”, Via Duca degli Abruzzi 8, 07100 Sassari, Italy

³ATS Sardegna, ASSL Sassari, Servizio di Sanità Animale, 07100 Sassari, Italy

^*Corresponding author: Stefano Cappai Osservatorio Epidemiologico Veterinario Regionale della Sardegna, via XX Settembre, 09125 Cagliari, Italy. E-mail: Stefano.cappai@izs-sardegna.it

Received 27 August 2019 Revised 14 October 2019 Accepted 21 November 2019

This is an Open Access article distributed under the terms of the Creative Commons Attribution Non-Commercial License (http://creativecommons.org/licenses/by-nc/4.0/) which permits unrestricted non-commercial use, distribution, and reproduction in any medium, provided the original work is properly cited.

Abstract

African swine fever (ASF) is a highly contagious disease of domestic pigs and wild boars (WBs). Without a vaccine, early antibody and antigen detection and rapid diagnosis are crucial for the effective prevention of the disease and the employment of control measures. In Sardinia, where 3 different suid populations coexisted closely for a long time, the disease persists since 1978. The recent ASF eradication plan involves more stringent measures to combat free-ranging pigs and any kind of illegality in the pig industry. However, critical issues such as the low level of hunter cooperation with veterinary services and the time required for ASF detection in the WBs killed during the hunting season still remain. Considering the need to deliver true ASF negative carcasses as early as possible, this study focuses on the evaluation and validation of a duplex pen-side test that simultaneously detects antibodies and antigens specific to ASF virus, to improve molecular diagnosis under field conditions. The main goal was to establish the specificity of the two pen-side tests performed simultaneously and to determine their ability to detect the true ASF negative carcasses among the hunted WBs. Blood and organ samples of the WBs hunted during the 2018/2019 hunting seasons were obtained. A total of 160 animals were tested using the pen-side kit test; samples were collected for virological and serological analyses. A specificity of 98% was observed considering the official laboratory tests as gold standards. The new diagnostic techniques could facilitate faster and cost-effective control of the disease.

Keywords: African swine fever, pen-side test, ost effectiveness analysis, Sardinia, hunting season management

References

1. Alonso C, Borca M, Dixon L, Revilla Y, Rodriguez F, Escribano JM. Ictv Report Consortium. ICTV virus taxonomy profile: Asfaviridae. J Gen Virol. 2018; 99:613–614.

2. Dixon LK, Twigg SR, Baylis SA, Vydelingum S, Bristow C, Hammond JM, Smith GL. Nucleotide sequence of a 55 kbp region from the right end of the genome of a pathogenic African swine fever virus isolate (Malawi LIL20/1). J Gen Virol. 1994; 75:1655–1684.

3. Dixon LK, Escribano JM, Martins C, Rock DL, Salas ML. Asfarviridae. Fauquet CM, Mayo MA, Maniloff J, Desselberger U, Ball LA, editors. (eds.).Virus Taxonomy. VIII Report of the ICTV. pp.p. 135–143. Elsevier/Academic Press;London: 2005.

4. Anderson EC, Hutchings GH, Mukarati N, Wilkinson PJ. African swine fever virus infection of the bushpig (Potamochoerus porcus) and its significance in the epidemiology of the disease. Vet Microbiol. 1998; 62:1–15.

5. Penrith ML, Thomson GR, Bastos AD, Etter EM. African swine fever. Coetzer JAW, Tustin RC, editors. (eds.).Infectious Diseases of Livestock. 2nd ed.pp.p. 1088–1119. Oxford University Press;Cape Town: 2004.

6. Blome S, Gabriel C, Beer M. Pathogenesis of African swine fever in domestic pigs and European wild boar. Virus Res. 2013; 173:122–130.

7. Beltran-Alcrudo D, Falco JR, Raizman E, Dietze K. Transboundary spread of pig diseases: the role of international trade and travel. BMC Vet Res. 2019; 15:64.

8. Couacy-Hymann E, Kouakou KV, Achenbach JE, Kouadio L, Koffi YM, Godji HP, Adjé KE, Oulaï J, Pell-Minhiaud HJ, Lamien CE. Re-emergence of genotype I of African swine fever virus in Ivory Coast. Transbound Emerg Dis. 2019; 66:882–896.

9. Zhou X, Li N, Luo Y, Liu Y, Miao F, Chen T, Zhang S, Cao P, Li X, Tian K, Qiu HJ, Hu R. Emergence of African swine fever in China, 2018. Transbound Emerg Dis. 2018; 65:1482–1484.

10. Komba EVG, Karimuribo ED, Kanemanema MC. Socioeconomic impact of African swine fever outbreak of 2011 and its epidemiology in Isoka District of Zambia. Tanzan Vet J. 2018; 29:37–47.

11. Zepeda C. Chapter 1.3. The social impact of disease control and eradication programs: case studies. Morilla A, Yoon KJ, Zimmerman JJ, editors. (eds.).Trends in Emerging Viral Infections of Swine. pp.p. 17–20. Iowa State Press;Iowa City: 2002.

12. Saatkamp HW, Berentsen PB, Horst HS. Economic aspects of the control of classical swine fever outbreaks in the European Union. Vet Microbiol. 2000; 73:221–237.

13. World Animal Health Information Database (WAHIS Interface). African Swine Fever, Hungary, (Follow-up report No. 11). World Organisation for Animal Health (OIE);Paris: 2019.

14. Jori F, Vial L, Penrith ML, Pérez-Sánchez R, Etter E, Albina E, Michaud V, Roger F. Review of the sylvatic cycle of African swine fever in sub-Saharan Africa and the Indian ocean. Virus Res. 2013; 173:212–227.

15. Penrith ML, Bastos AD, Etter EM, Beltrán-Alcrudo D. Epidemiology of African swine fever in Africa today: sylvatic cycle versus socio-economic imperatives. Transbound Emerg Dis. 2019; 66:672–686.

16. Anon. Bruciati Ventimila Maiali. Il Messaggero Sardo;Cagliari: 1978.

17. Baggiani P. La Peste Suina è Arrivata nel Nuorese. Il Messaggero Sardo;Cagliari: 1978.

18. Laddomada A, Patta C. La Peste Suina Africana a Dieci Anni Dalla Sua Introduzione in Sardegna. Vol.2:Quaderni dell'Istituto Zooprofilattico;Cagliari: 1988.

19. Martínez-López B, Perez AM, Feliziani F, Rolesu S, Mur L, Sánchez-Vizcaíno JM. Evaluation of the risk factors contributing to the African swine fever occurrence in Sardinia, Italy. Front Microbiol. 2015; 6:314.

20. Mur L, Atzeni M, Martínez-López B, Feliziani F, Rolesu S, Sanchez-Vizcaino JM. Thirty-five-year presence of African swine fever in Sardinia: history, evolution and risk factors for disease maintenance. Transbound Emerg Dis. 2016; 63:e165–177.

21. Cappai S, Rolesu S, Coccollone A, Laddomada A, Loi F. Evaluation of biological and socio-economic factors related to persistence of African swine fever in Sardinia. Prev Vet Med. 2018; 152:1–11.

22. Jurado C, Fernández-Carrión E, Mur L, Rolesu S, Laddomada A, Sánchez-Vizcaíno JM. Why is African swine fever still present in Sardinia? Transbound Emerg Dis. 2018; 65:557–566.

23. Laddomada A, Rolesu S, Loi F, Cappai S, Oggiano A, Madrau MP, Sanna ML, Pilo G, Bandino E, Brundu D, Cherchi S, Masala S, Marongiu D, Bitti G, Desini P, Floris V, Mundula L, Carboni G, Pittau M, Feliziani F, Sanchez-Vizcaino JM, Jurado C, Guberti V, Chessa M, Muzzeddu M, Sardo D, Borrello S, Mulas D, Salis G, Zinzula P, Piredda S, De Martini A, Sgarangella F. Surveillance and control of African swine fever in free-ranging pigs in Sardinia. Transbound Emerg Dis. 2019; 66:1114–1119.

24. Wilkinson P. The persistence of African swine fever in Africa and the Mediterranean. Prev Vet Med. 1984; 2:71–82.

25. Laddomada A, Patta C, Oggiano A, Caccia A, Ruiu A, Cossu P, Firinu A. Epidemiology of classical swine fever in Sardinia: a serological survey of wild boar and comparison with African swine fever. Vet Rec. 1994; 134:183–187.

26. Mannelli A, Sotgia S, Patta C, Sarria A, Madrau P, Sanna L, Firinu A, Laddomada A. Effect of husbandry methods on seropositivity to African swine fever virus in Sardinian swine herds. Prev Vet Med. 1997; 32:235–241.

27. Mannelli A, Sotgia S, Patta C, Oggiano A, Carboni A, Cossu P, Laddomada A. Temporal and spatial patterns of African swine fever in Sardinia. Prev Vet Med. 1998; 35:297–306.

28. Rolesu S, Aloi D, Ghironi A, Oggiano N, Oggiano A, Puggioni G, Patta C, Farina S, Montinaro S. Geographic information systems: a useful tool to approach African swine fever surveillance management of wild pig populations. Vet Ital. 2007; 43:463–467.

29. Contini A, Cossu P, Rutili D, Firinu A. African swine fever in Sardinia. Wilkinson PJ, editor. (ed.).CEC/FAO Expert Consultation on African Swine Fever Research. CEC Publication;Sardinia: 1983.

30. Sastre P, Gallardo C, Monedero A, Ruiz T, Arias M, Sanz A, Rueda P. Development of a novel lateral flow assay for detection of African swine fever in blood. BMC Vet Res. 2016; 12:206.

31. Cappai S, Coccollone A, Rolesu S, Oggiano A, Madrau P, Loi F. Costi e benefici nell'utilizzo del pen side test per la ricerca anticorpale nei confronti della Peste Suina Africana. SUMMA Anim Reddito. 2016; 9:57–62.

32. Cappai S, Loi F, Coccollone A, Cocco M, Falconi C, Dettori G, Feliziani F, Sanna ML, Oggiano A, Rolesu S. Evaluation of a commercial field test to detect African swine fever. J Wildl Dis. 2017; 53:602–606.

33. Cappai S, Sanna G, Loi F, Coccollone A, Marrocu E, Oggiano A, Brundu D, Rolesu S, Bandino E. African swine fever detection on field with antigen rapid kit test. J Anim Sci Res. 2018; 2:118.

34. European Food Safety Authority (EFSA). Boklund A, Cay B, Depner K, Földi Z, Guberti V, Masiulis M, Miteva A, More S, Olsevskis E, Šatrán P, Spiridon M, Stahl K, Thulke HH, Viltrop A, Wozniakowski G, Broglia A, Cortinas Abrahantes J, Dhollander S, Gogin A, Verdonck F, Amato L, Papanikolaou A, Gortázar C. Epidemiological analyses of African swine fever in the European Union (November 2017 until November 2018). EFSA J. 2018; 16:e05494.

35. Liu L, Atim S, LeBlanc N, Rauh R, Esau M, Chenais E, Mwebe R, Nelson WM, Masembe C, Nantima N, Ayebazibwe C, Ståhl K. Overcoming the challenges of pen-side molecular diagnosis of African swine fever to support outbreak investigations under field conditions. Transbound Emerg Dis. 2019; 66:908–914.

36. Obuchowski NA. Sample size tables for receiver operating characteristic studies. AJR Am J Roentgenol. 2000; 175:603–608.

37. King DP, Reid SM, Hutchings GH, Grierson SS, Wilkinson PJ, Dixon LK, Bastos AD, Drew TW. Development of a TaqMan PCR assay with internal amplification control for the detection of African swine fever virus. J Virol Methods. 2003; 107:53–61.

38. Gardner MJ, Altman DG. Statistics with Confidence: Confidence Intervals and Statistical Guidelines. p. 140. pp,. British Medical Journal;London: 1989.

39. Cebul RD, Hershey JC, Williams SV. Using multiple tests: series and parallel approaches. Clin Lab Med. 1982; 2:871–890.

40. Loi F, Cappai S, Coccollone A, Rolesu S. Standardized risk analysis approach aimed to evaluate the last African swine fever eradication program performance, in Sardinia. Front Vet Sci. 2019; 6:299.

Table 1.

The contingency table showing the detection of African swine fever virus Ag using the PS tests, compared to that using PCR technique

Ag PS test	PCR technique
Ag PS test	Positive	Negative
Positive	0 (0%)	4 (2%)
Negative	0 (0%)	156 (98%)
Total	0 (0%)	160 (100%)

Ag, antigen; PS, pen-side; PCR, polymerase chain reaction.

Table 2.

The contingency table showing the detection of African swine fever virus Ab using the PS tests, compared to that using ELISA test + IB

Ab PS test	ELISA test + IB
Ab PS test	Positive	Negative
Positive	2 (1.4%)	3 (2%)
Negative	1 (0.6%)	154 (96%)
Total	3 (2%)	157 (98%)

The results are expressed as percentages (%). Ab, antibody; PS, pen-side; ELISA, enzyme-linked immunosorbent assay; IB, immunoblotting test.

Table 3.

Individual and combined (sequential or in parallel) accuracies of Ag PS test and Ab PS test in detecting ASFV Ag and ASFV Ab in the blood samples of WBs from the areas endemic for ASFV in Sardinia

Accuracy	Ag PS test	Ab PS test	Parallel testing
Sensitivity	66.7 (9.4–99.1)	–	66.7 (9.4–99.1)
Specificity	98.1 (94.5–99.6)	97.5 (93.7–99.3)	95.5 (91.0–98.2)
PPV	40.0 (5.2–85.3)	–	22.2 (2.8–60)
NPV	99.3 (96.4–99.9)	100 (96.3–100)	99.3 (96.4–99.9)

The results are expressed as percentages (%) and 95% confidence interval. Ag, antigen; PS, pen-side; Ab, antibody; ASFV, African swine fever virus; WB, wild boar; PPV, positive predictive value; NPV, negative predictive value.

Table 4.

Table showing the laboratory tests performed, corresponding waiting period (days) for laboratory results, and total number of WBs showing positive results, during the hunting season of 2018/2019 in Istituto Zooprofilattico Sperimentale della Sardegna

Laboratory test	WBs tested	No. of tests	Total positive	Day waiting period^*
ELISA	10,554	10,671	549	3.26 ± 2.60 (0–40)
IB	574	575	111	4.16 ± 2.48 (1–18)
PCR	5,603	6,502	5	2.99 ± 2.33 (0–40)
Total	12,728^†	17,748	116^‡	–

WB, wild boar; ELISA, enzyme-linked immunosorbent assay; IB, immunoblotting test; PCR, polymerase chain reaction.* The values of day waiting period are expressed as mean ± standard deviation (range);

^† The total number of WBs tested is not equal to the sum of animals tested using ELISA, IB, and PCR, because ELISA is a screening test performed before IB. The same animal could be tested using ELISA alone (negative ELISA result) or using ELISA and IB (positive ELISA result);

^‡ The total number of positives were calculated considering that each WB could serologically be defined as ASF positive only if it is IB positive.

Table 5.

Total cost (€) of hunting season management based on scenario A (actual hunting management) and scenario B (hunting management using Ag PS test and Ab PS test), considering laboratory or on-field test costs and veterinarians' remunerations

Scenarios	Type of tests	Costs of lab/field tests (€)	Cost for positive sample test	Remuneration for veterinarians (€)	Total costs for managing hunting season (€)^*
Scenario A^†	ELISA	41,296.8^‡	1,701.9^§	358,293.2^∥	542,546.1
	IB	8,625^¶	1,165^**
	PCR	134,331.3^††	103.3^‡‡
Scenario B^§§	Ag PS test	43,911.6^∥∥	16,544.7^¶¶	114,857.5^***	219,225.4
	Ab PS test	43,911.6^†††

Ag, antigen; Ab, antibody; PS, pen-side; ELISA, enzyme-linked immunosorbent assay; IB, immunoblotting test; PCR, polymerase chain reaction; WB, wild boar.

^* The total cost of the hunting season has been calculated as sum veterinarian cost and test cost; Scenario based on

^† actual hunting management and

^§§ possible hunting management using PS tests;

^‡ The total cost of the ELISA tests performed during the 2018/2019 WB-HS has been calculated as the product of 3.87 € (cost of single exam) and 10,671 (the number of exams performed);

^§ The total cost of ELISA tests in the animals tested positive using ELISA has been calculated as the product of 3.87 € (cost of single exam) and 549 (the number of animals tested positive; Table 4);

^∥ The total veterinarian cost in scenario A has been calculated as the product of 28.15 € (cost for testing a single animal) and 12,728 (number of WBs tested);

^¶ The total cost of the IB tests performed during the 2018/2019 WB-HS has been calculated as the product of 15.00 € (cost of single exam) and 575 (the number of exams performed);

^** The total cost of IB in the animals tested positive using IB has been calculated the product of 15.00 € (cost of single exam) and 111 (the number of animals tested positive; Table 4);

^†† The total cost of real-time PCR analyses performed during the 2018/2019 WB-HS has been calculated as the product of 20.66 € (cost of single exam) and 5,603 (the number of exams performed);

^‡‡ The total cost of real-time PCR in the animals tested positive using real-time PCR has been calculated as the product of 20.66 € (cost of single exam) and 5 (the number of animals tested positive; Table 4);

^{∥∥,†††} The total cost of PS tests (Ag and Ab) has been calculated as the product of 3.45 € (cost of single PS kit) and the number of WBs hypothesised to be tested during the hunting season 2018/2019;

^¶¶ The total cost for the conventional testing of the animals that showed positive results based on PS tests has been calculated as the sum of

^§ ,

^** , and

^‡‡ [(549 × 3.87 €) + (111 × 15.00 €) + (5 × 20.66 €)];

^*** The total veterinarian cost in scenario B has been calculated as the product of 9.02 € (cost for testing a single animal) and 12,728 (number of WBs tested).

TOOLS

Similar articles