Abstract
Effective biosecurity at farm, state, national and international levels to prevent and control the spread of important production animal diseases, is essential to minimise the risk of disease outbreaks. Assurance is crucial with regard to the disease status of a population of animals in a growing global livestock market. Assurance is achieved by using testing methods that have a high sensitivity and specificity, i.e. the ability to detect infected and non-infected animals and groups of animals, and ideally are cost effective. The enzyme-linked immunosorbent assay (ELISA) is such a test, being highly versatile, inexpensive and easy to perform. For some production animal diseases, current ELISAs demonstrate poor sensitivity, i.e. detect a lower proportion of infected animals. This poor detection rate may permit the maintenance of infection within livestock populations, posing risks to all levels of biosecurity. Due to the higher concentrations of immunoglobulins (Igs) present in colostrum when compared to serum, colostrum should be able to improve the detection of some important infectious diseases of production animals, improving the assurance of absence of disease. This review presents the underpinning physiological basis of Ig transfer into colostrum, indicates the relative Ig concentrations in serum and colostrum and describes how ELISAs work. Although not the focus of this review, different parameters that can be used for the assessment of diagnostic utility are presented. Targeted production animal diseases investigated in this PhD study are described, and the outcomes of the research into the diagnostic utility of colostrum using vaccinated animals as models of disease, as well as a field study of Johne’s disease are presented. Overall, the premise of this PhD study regarding higher antibody concentrations in colostrum was valid, as the diagnostic sensitivities of the ELISAs were improved when using colostrum compared to serum, while also maintaining diagnostic specificity.
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Ameri-Mahabadi M, Zhou E-M, Hsu W (2005) Comparison of two swine Mycoplasma hyopneumoniae enzyme-linked immunosorbent assays for detection of antibodies from vaccinated pigs and field serum samples. J Vet Diagn Invest 17:61–64
Bakker D, Willemsen PTJ, van Zijderveld FG (2000) Paratuberculosis recognized as a problem at last: a review. Vet Quart 22:200–204
Baumrucker CR, Burkett AM, Magliaro-Macrina AL, Dechow CD (2010) Colostrogenesis: mass transfer of immunoglobulin G1 into colostrum. J Dairy Sci 93:3031–3038
Beaudeau F, Belloc C, Seegers H, Assie S, Sellal E, Joly A (2001) Evaluation of a blocking ELISA for the detection of bovine viral diarrhoea virus (BVDV) antibodies in serum and milk. Vet Microbiol 80:329–337
Beer AE, Billingham RE, Head J (1974) The immunologic significance of the mammary gland. J Investig Dermatol 63:65–74
Bender JS, Irwin CK, Shen H-G, Schwartz KJ, Opriessnig T (2011) Erysipelothrix spp. genotypes, serotypes, and surface protective antigen types associated with abattoir condemnations. J Vet Diagn Invest 23:139–142
Bianchi ATJ, Moonen-Leusen HWM, van der Heijden PJ, Bokhout BA (1995) The use of double antibody sandwich ELISA and monoclonal antibodies for the assessment of porcine IgM, IgG and IgA concentrations. Vet Immunol Immunop. 44:309–317
Bokhout BA, van Asten-Noorduk JJL, Stok W (1986) Porcine IgG. Isolation of two IgG-subclasses and anti-IgG class- and subclass-specific antibodies. Mol Immunol 23:675–683
Bourne FJ (1977) The mammary gland and neonatal immunity. Vet Sci Commun. 1:141–151
Brooke CJ, Riley TV (1999) Erysipelothrix rhusiopathiae: bacteriology, epidemiology and clinical manifestations of an occupational pathogen. J Med Microbiol 48:789–799
Campbell SG, Siegel MJ, Knowlton BJ (1977) Sheep immunoglobulins and their transmission to the neonatal lamb. New Zeal Vet J. 25:361–365
Casal C, Diez-Guerrier A, Alvarez J, Rodriguez-Campos S, Mateos A, Linscott R, Martel E, Lawrence JC, Whelan C, Clarke J, O’Brien A, Dominguez L, Aranaz A (2014) Strategic use of serology for the diagnosis of bovine tuberculosis after intradermal skin testing. Vet Microbiol 170:342–351
Cervenak J, Kacskoviks I (2009) The neonatal Fc receptor plays a crucial role in the metabolism of IgG in livestock animals. Vet Immunol Immunopathol 128:171–177
Chanlun A, Naslund K, Aiumlamai S, Bjorkman C (2002) Use of bulk milk for detection of Neospora caninum infection in dairy herds in Thailand. Vet Parasitol 110:35–44
Cockcroft PD, Jenvey CJ, Reichel MP (2014) Role for colostrum and whey testing for bovine TB and Johne’s disease? Vet Rec 175:597
Colavita G, Vergara A, Ianieri A (2006) Deferment of slaughtering in swine affected by cutaneous erysipelas. Meat Sci 72:203–220
Conneely M, Berry DP, Sayers R, Murphy JP, Lorenz I, Doherty ML, Kennedy E (2013) Factors associated with the concentration of immunoglobulin G in the colostrum of dairy cows. Animal 7:1824–1832
Cripps AW, Husband AJ, Scicchitano R, Sheldrake RF (1985) Quantitation of sheep IgG1, IgG2, IgA, IgM and albumin by radioimmunoassay. Vet Immunol Immunopathol 8:137–147
Crowther JR (2009) The ELISA guidebook. Humana Press, New York
Curtis J, Bourne FJ (1971) Immunoglobulin quantitation in sow serum, colostrum and milk and the serum of young pigs. Biochim Biophys Acta 236:319–332
Deeks JJ, Altman DG (2004) Diagnostic tests 4: likelihood ratios. Brit Med J. 329:168–169
Devillers N, Farmer C, Le Dividich J, Prunier A (2007) Variability of colostrum yield and colostrum intake in pigs. Animal 1:1033–1041
Djordjevic SP, Eamens GJ, Romalis LF, Saunders MM (1994) An improved enzyme linked immunosorbent assay (ELISA) for the detection of porcine serum antibodies against Mycoplasma hyopneumoniae. Vet Microbiol 39:261–274
Durham PJK, Hassard LE (1990) An enzyme-linked immunosorbent assay (ELISA) for antibodies to Bovine Viral Diarrhoea Virus. Vet Microbiol 22:1–10
Eamens GJ, Chin JC, Nicholls PJ (1989) Comparison of inoculation regimes for the experimental production of swine erysipelas arthritis. II Serological findings in a gel diffusion test and enzyme-linked immunosorbent assay. Aust Vet J 66:216–220
Elfstrand L, Lindmark-Mansson H, Paulsson M, Nyberg L, Akesson B (2002) Immunoglobulins, growth factors and growth hormone in bovine colostrum and the effects of processing. Int Dairy J 12:879–887
Eriksson H, Jansson DS, Johansson K-E, Baverud V, Chirico J, Aspan A (2009) Characterization of Erysipelothrix rhusiopathiae isolates from poultry, pigs, emus, the poultry red mite and other animals. Vet Microbiol 137:98–104
Erlandson KR, Evans RB, Thacker BJ, Wegner MW, Thacker EL (2005) Evaluation of three serum antibody enzyme-linked immunosorbent assays for Mycoplasma hyopneumoniae. J Swine Health Prod 13:198–203
Eusebi P (2013) Diagnostic accuracy measures. Cerebrovasc Dis 36:267–272
Frenyo VL, Butler JE, Guidry AJ (1986) The association of extrinsic bovine IgG1, IgG2, SIgA and IgM with the major fractions and cells of milk. Vet Immunol Immunop. 13:239–254
Frey J, Haldimann A, Kobisch M, Nicolet J (1994) Immune response against the L-lactate dehydrogenase of Mycoplasma hyopneumoniae in enzootic pneumonia of swine. Microb Pathog 17:313–322
Gilbert RP, Gaskins CT, Hillers JK, Parker CF, McGuire TC (1988) Genetic and environmental factors affecting immunoglobulin G1 concentrations in ewe colostrum and lamb serum. J Anim Sci 66:855–863
Glas AS, Lijmer JG, Prins MH, Bonsel GJ, Bossuyt PMM (2003) The diagnostic odds ratio: a single indicator of test performance. J Clin Epidemiol 56:1129–1135
Greiner M, Pfeiffer D, Smith RD (2000) Principles and practical application of the receiver-operating characteristic analysis for diagnostic tests. Prev Vet Med 45:23–41
Gwozdz J (2010) SCAHLS Quality Plan for Johne’s disease testing. Australian and New Zealand Standard Diagnostic Procedures. Sub-Committee on Animal Health Laboratory Standards. http://www.scahls.org.au/Procedures/Documents/ANZSDP/Johnes_Disease_Quality_Plan_2010.pdf. Accessed 23 Sep 2013
Halliday R (1974) Variations in immunoglobulin concentrations in Merino and Scottish black face lambs. Anim Prod 19:301–308
Halliday R (1978) Variation in immunoglobulin transfer from ewes to lambs. Ann Rech Vet 9:367–374
Hendrick SH, Duffield TF, Kelton DF, Leslie KE, Lissemore KD, Archambault M (2005) Evaluation of enzyme-linked immunosorbent assays performed on milk and serum samples for detection of paratuberculosis in lactating dairy cows. J Am Vet Med A. 226:424–428
Hope AF, Kluver PF, Jones SL, Condron RJ (2000) Sensitivity and specificity of two serological tests for the detection of ovine paratuberculosis. Aust Vet J 78:850–856
Houe H (2003) Economic impact of BVDV infection in dairies. Biologicals 31:137–143
Howard CJ, Taylor G (1985) Immune responses to mycoplasma infections of the respiratory tract. Vet Immunol Immunop. 10:3–32
Hurley WL, Theil PK (2011) Perspectives on immunoglobulins in colostrum and milk. Nutrients 3:442–474
Husband AJ (1987) Perspectives in mucosal immunity: A ruminant model. Vet Immunol Immunopathol 17:357–365
Imada Y, Mori Y, Daizoh M, Kudoh K, Sakano T (2003) Enzyme-linked immunosorbent assay employing a recombinant antigen for detection of protective antibody against swine erysipelas. J Clin Microbiol 41:5015–5021
Jenvey CJ, Reichel MP, Cockcroft PD (2015) Investigation of the comparative sensitivity of serum, colostrum and whey for detection of specific antibodies in sheep vaccinated against Johne’s disease. Small Ruminant Res 123:193–195
Jenvey CJ, Reichel MP, Cockcroft PD (2015) Erysipelothrix rhusiopathiae and Mycoplasma hyopneumoniae: The sensitivities of enzyme-linked immunosorbent assays for detecting vaccinated sows of unknown disease status using serum and colostrum, and the correlation of the results for sow serum, colostrum, and piglet serum. J Vet Diagn Invest 27:211–216
Jenvey CJ, Weir AM, Reichel MP, Cockcroft PD (2015) Performance characteristics of ELISA to detect Bovine Viral Diarrhoea Virus (BVDV) antibodies using colostrum. Open J Vet Med 5:35–41
Jenvey CJ, Reichel MP, Cockcroft PD (2015) The diagnostic performance of an antibody ELISA using serum and colostrum to determine the disease status of a Jersey dairy herd infected with Mycobacterium avium subspecies paratuberculosis. J Vet Diagn Invest (Accepted manuscript)
Kehoe SI, Jayarao BM, Heinrichs AJ (2007) A survey of bovine colostrum composition and colostrum management practices on Pennsylvania dairy farms. J Dairy Sci 90:4108–4116
Kirchhoff H, Dubenkropp H, Kerlen G, Steffens H-W, Hermanns W, Trautwein G, Bohm KH (1985) Application of the indirect enzyme immunoassay for the detection of antibodies against Erysipelothrix rhusiopathiae. Vet Microbiol 10:549–559
Klimes J, Jagos P, Bouda J, Gajdusek S (1986) Basic qualitative parameters of cow colostrum and their dependence on season and post partum time. Acta Vet Brno. 55:23–39
Klobasa F, Habe F, Werhahn E, Butler JE (1985) Changes in the concentrations of serum IgG1, IgA and IgM of sows throughout the reproductive cycle. Vet Immunol Immunopathol 10:341–353
Klobasa F, Werhahn E, Butler JE (1987) Composition of sow milk during lactation. J Anim Sci 64:1458–1466
Korhonen H, Marnila P, Gill HS (2000) Bovine antibodies for health. Brit J Nutr. 84:S135–S146
Korhonen H, Marnila P, Gill HS (2000) Milk immunoglobulins and complement factors. Brit J Nutr 84:S75–S80
Lanyon SR, Rogers J, Kessell A, Reichel MP (2012) Economic analysis of an acute outbreak of bovine viral diarrhoea virus (BVDv) in a South Australian dairy herd—a case study. In: XXVII World Buiatrics Congress. Lisbon
Lanyon SR, Anderson ML, Bergman E, Reichel MP (2013) Validation and evaluation of a commercially available ELISA for the detection of antibodies specific to bovine viral diarrhoea virus (bovine pestivirus). Aust Vet J 91:52–56
Lanyon SR, Hill FI, Reichel MP, Brownlie J (2014) Bovine viral diarrhoea: pathogenesis and diagnosis. Vet J 199:201–209
Lanyon SR, McCoy R, Bergman E, Reichel MP (2014) Milk as a diagnostic sample for the identification of bovine viral diarrhoea (BVD) infected dairy herds using a commerically available antibody ELISA. Aust Vet J 92:269–273
Lee CS, Lascelles AK (1970) Antibody-producing cells in antigenically stimulated mammary glands and in the gastro-intestinal tract of sheep. Aust J Exp Biol Med. 48:525–535
Lindberg ALE, Alenius S (1999) Principles for eradication of bovine viral diarrhoea virus (BVDV) infections in cattle populations. Vet Microbiol 64:197–222
Loisel F, Farmer C, Ramaekers P, Quesnel H (2013) Effects of high fiber intake during late pregnancy on sow physiology, colostrum production, and piglet performance. J Anim Sci 91:5269–5279
Lombard JE, Byrem TM, Wagner BA, McCluskey BJ (2006) Comparison of milk and serum enzyme–linked immunosorbent assays for diagnosis of Mycobacterium avium subspecies paratuberculosis infection in dairy cattle. J Vet Diagn Invest 18:448–458
Lugton IW (2004) Cross-sectional study of risk factors for the clinical expression of ovine Johne’s disease on New South Wales farms. Aust Vet J 82:355–365
Madureira AR, Pereira CI, Gomes AMP, Pintado ME, Malcata FX (2007) Bovine whey proteins—overview on their main biological properties. Food Res Int 40:1197–1211
Maes D, Segales J, Meyns T, Sibila M, Pieters M, Haesebrouck F (2008) Control of Mycoplasma hyopneumoniae infections in pigs. Vet Microbiol 126:297–309
Marnila P, Korhonen H (2011) Milk- Colostrum. In: Fuquay JW (ed) Encyclopedia of dairy sciences, 2nd edn. Academic Press, Waltham, pp 591–597
Marnila P, Korhonen H (2011) Milk proteins—immunoglobulins. In: Fuquay JW (ed) Encyclopedia of dairy sciences, 2nd edn. Academic Press, Waltham, pp 807–815
McGuire TC, Regnier J, Kellom T, Gates NL (1983) Failure in passive transfer of immunoglobulin G1 to lambs: Measurement of immunoglobulin G1 in ewe colostrums. Am J Vet Res 44:1064–1067
McGuirk SM, Collins M (2004) Managing the production, storage, and delivery of colostrum. Vet Clin N Am Food A. 20:593–603
McManaman JL, Neville MC (2003) Mammary phsiology and milk secretion. Adv Drug Deliver Rev 55:629–641
Milner AR, Mack WN, Coates KJ, Hill J, Gill I, Sheldrick P (1990) The sensitivity and specificity of a modified ELISA for the diagnosis of Johne’s disease from a field trial in cattle. Vet Microbiol 25:193–198
Newby TJ, Bourne J (1977) The nature of the local immune system of the bovine mammary gland. J Immunol. 118:461–465
Nguyen D-AD, Neville MC (1998) Tight junction regulation in the mammary gland. J Mammary Gland Biol 3:233–246
Pahud JJ, Mach JP (1970) Identification of secretory IgA, free secretory piece and serum IgA in ovine and caprine species. Immunochemistry 7:679–686
Park YW, Juarez M, Ramos M, Haenlein GFW (2007) Physico-chemical characteristics of goat and sheep milk. Small Rumin Res 68:88–113
Porter P (1969) Transfer of immunoglobulins IgG, IgA and IgM to lacteal secretions in the parturient sow and their absorbtion by the neonatal piglet. Biochem Biophys Acta. 181:381–392
Quesnel H (2011) Colostrum production by sows: variability of colostrum yield and immunoglobulin G concentrations. Animal 5:1546–1553
Quesnel H, Farmer C, Devillers N (2012) Colostrum intake, influence on piglet performance and factors of variation. Livest Sci 146:105–114
Reichel MP, Kittelberger R, Penrose ME, Meynell RM, Cousins D, Ellis T, Mutharia LM, Sugden EA, Johns AH, de Lisle GW (1999) Comparison of serological tests and faecal culture for the detection of Mycobacterium avium subsp. paratuberculosis infection in cattle and analysis of the antigens involved. Vet Microbiol 66:135–150
Reneau J, Hunter AG, Williams JB (1973) Factors affecting immunoglobulin G concentration in day old lambs. J Dairy Sci 56:670
Saah AJ, Hoover DR (1997) “Sensitivity” and “specificity” recognised: the meaning of these terms in analytical and diagnostic settings. Ann Intern Med 126:91–94
Saliki JT, Huchzermeier R, Dubovi EJ (2006) Evaluation of a new sandwich ELISA kit that uses serum for the detection of cattle persistently infected with BVD virus. Ann N Y Acad Sci 916:358–363
Sato H, Yamazaki Y, Tsuchiya K, Aoyama T, Akaba N, Suzuki S, Yokoyama A, Saito H, Maehara N (1998) Use of the protective antigen of Erysipelothrix rhusiopathiae in the enzyme-linked immunosorbent assay and latex agglutination. J Vet Med B. 45:407–420
Shennan DB, Peaker M (2000) Transport of milk constituents by the mammary gland. Physiol Rev 80:925–951
Sibila M, Pieters M, Molitor T, Maes D, Haesebrouck F, Segalés J (2009) Current perspectives on the diagnosis and epidemiology of Mycoplasma hyopneumoniae infection. Vet J 181:221–231
Simundic A-M (2008) Measures of diagnostic accuracy: basic definitions. Med Biol Sci. 22:61–65
Smith WD, Dawson AA, Wells PW, Burrows C (1975) Immunoglobulin concentrations in ovine body fluids. Res Vet Sci 19:355–386
Smith WD, Wells PW, Burrows C, Dawson AM (1976) Maternal immunoglobulins and parainfluenza 3 virus inhibitors in the nasal and lachrymal secretions and serum of newborn lambs. Clin Exp Immunol 23:544–553
Smith RD (2006) Veterinary clinical epidemiology. Taylor and Francis, Boca Raton
Smithers GW (2008) Whey and whey proteins—from ‘gutter-to-gold’. Int Dairy J 18:695–704
Sørensen V, Ahrens P, Barfod K, Feenstra AA, Feld NC, Friis NF, Bille-Hansen V, Jensen NE, Pedersen MW (1997) Mycoplasma hyopneumoniae infection in pigs: duration of the disease and evaluation of four diagnostic assays. Vet Microbiol 54:23–34
Stelwagen K, Carpenter E, Haigh B, Hodgkinson A, Wheeler TT (2009) Immune components of colostrum and milk. J Anim Sci 87:3–9
Taylor LF (2010) Findings of an Australia wide serological survey of beef and dairy herds for Bovine Viral Diarrhoea Virus conducted between 2007 and 2009. Aust Cattle Vet 57:14–28
Thobokwe G, Heuer C, Hayes DP (2004) Validation of a bulk tank milk antibody ELISA to detect dairy herds likely infected with Bovine Viral Diarrhoea Virus in New Zealand. New Zeal Vet J 52:394–400
Van de Perre P (2003) Transfer of antibody via mother’s milk. Vaccine 21:3374–3376
Wagstrom EA, Yoon KJ, Zimmerman JJ (2000) Immune components in porcine mammary secretions. Viral Immunol 13:383–397
Wang QN, Chang BJ, Riley TV (2010) Erysipelothrix rhusiopathiae. Vet Microbiol 140:405–417
Watson D, Lascelles AK (1973) Comparisons of immunoglobulin secretion in the salivary and mammary glands of sheep. Aust J Biol Med. 51:255–258
Weaver DM, Tyler JW, VanMetre DC, Hostetler DE, Barrington GM (2000) Passive transfer of colostral immunoglobulins in calves. J Vet Intern Med 14:569–577
Weir A, Heuer C, McDougall S, Voges H (2013) Use of an enzyme-linked immunosorbent assay for detecting Bovine Viral Diarrhoea Virus antibodies in individual cow milk samples. New Zeal Vet J 61:305–309
Yokomizo Y, Yugi H, Merkal S (1985) A method for avoiding false-positive reactions in an enzyme-linked immunosorbent assay (ELISA) for the diagnosis of bovine paratuberculosis. Jpn J Vet Sci 47:111–119
Yokoyama H, Peralta R, Sendo S, Ikemori Y, Kodama Y (1993) Detection of passage and absorption of chicken egg yolk immunoglobulins in the gastrointestinal tract of pigs by use of enzyme-linked immunosorbent assay and fluorescent antibody testing. Am J Vet Res 54:867–872
Youden WJ (1950) Index for rating diagnostic tests. Cancer 3:32–35
Zervens L, Nielsen S, Jungersen G (2013) Characterisation of an ELISA detecting immunoglobulin G to Mycobacterium avium subsp. paratuberculosis in bovine colostrum. Vet J. 197:889–891
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Jenvey, C.J., Cockcroft, P.D. & Reichel, M.P. Production Animal Diseases: The Diagnostic Utility of Colostrum. Springer Science Reviews 3, 141–151 (2015). https://doi.org/10.1007/s40362-015-0036-4
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DOI: https://doi.org/10.1007/s40362-015-0036-4