Implications

This review shows that the passive immune status of beef-suckler calves on commercial farms may not be superior to dairy calves. The current knowledge deficit pertaining to factors affecting colostrum immunoglobulin mass (colostrum volume × immunoglobulin concentration) production of beef-suckler cows and consumption by their calves, coupled with difficulty in accurate quantification of immunoglobulin concentrations using existing laboratory tests, is a major limiting factor curtailing the provision of recommendations to ensure adequate passive transfer. Consequently, further research is warranted in this area.

Analysis of bovine immunoglobulin

Historically, radial immunodiffusion (RID) has been the only method that directly measures and quantifies immunoglobulin G (IgG); however, recent studies have reported IgG concentrations in colostrum, milk and blood measured using ELISA (Gelsinger et al., Reference Gelsinger, Smith, Jones and Heinrichs2015). Direct tests (e.g. RID and ELISA, for colostrum and blood) quantify the absolute concentration of immunoglobulin, whereas indirect tests for colostrum (e.g. brix refractometry) and blood (e.g. Zinc Sulphate Turbidity) provide an approximation of the immunoglobulin concentration; alternatively, assessment of the blood levels of other components of colostrum, which are similarly absorbed as immunoglobulins (e.g. gamma-glutamyl transferase activity), can be measured to give an indication of the level of passive immunity (Vandeputte et al., Reference Vandeputte, Detilleux and Rollin2014; Hogan et al., Reference Hogan, Doherty, Fagan, Kennedy, Conneely, Brady, Ryan and Lorenz2015; Dunn et al., Reference Dunn, Duffy, Gordon, Morrison, Argűello, Welsh and Earley2018). However, tests for quantification of IgG in bovine colostrum and serum can vary substantially in their accuracy, sensitivity and/or specificity (precision) (Hogan et al., Reference Hogan, Doherty, Fagan, Kennedy, Conneely, Brady, Ryan and Lorenz2015). Recent studies comparing single RID (sRID) and ELISA for quantification of IgG concentrations have found a poor level of agreement between the methods (Gelsinger et al., Reference Gelsinger, Smith, Jones and Heinrichs2015; Dunn et al., Reference Dunn, Duffy, Gordon, Morrison, Argűello, Welsh and Earley2018). For example, Dunn et al. (Reference Dunn, Duffy, Gordon, Morrison, Argűello, Welsh and Earley2018) using the Bland and Altman method showed a substantial fixed bias, a wide limit of agreement and a poor concordance coefficient between ELISA and sRID for colostrum and serum IgG concentrations. In both studies the absolute concentration of IgG was almost two-fold higher when measured using RID compared to ELISA (×1.9, Gelsinger et al., Reference Gelsinger, Smith, Jones and Heinrichs2015; × 1.8, Dunn et al., Reference Dunn, Duffy, Gordon, Morrison, Argűello, Welsh and Earley2018).

Considering these methodological aspects, it is difficult to prescribe discrete industry-wide standards or cut-off points for colostrum ‘quality’ or successful passive immunity in calf serum or plasma (see later). In addition, it also implies that interpreting published IgG concentrations particularly where different laboratory techniques are used, can be perilous.

Colostrum

Colostrum, the first secretions of the mammary gland after parturition, is rich in nutrients and non-nutrient biologically active components, including carbohydrates, proteins, growth factors, enzymes, enzyme inhibitors, nucleotides and nucleosides, cytokines, fats, minerals and vitamins (Hammon et al., Reference Hammon, Steinhoff-Wagner, Flor, Schönhusen and Metges2013; McGrath et al., Reference McGrath, Fox, McSweeney and Kelly2016). Colostrum is an essential source of dietary nutrients for the neonatal calf; McGee et al. (Reference McGee, Drennan and Caffery2005 and Reference McGee, Drennan and Caffery2006) reported that beef-suckler cow colostrum had a mean dry matter (DM) concentration of 245 to 285 g/kg, and CP, fat, lactose and ash concentrations (g/kg DM) of 150 to 184, 48 to 70, 26 to 30 and 10 to 13, respectively. In addition, colostral components influence neonatal gastrointestinal microbiome, morphological and functional development, and digestion and absorption, and also have systemic effects on calf metabolism and development (Hammon et al., Reference Hammon, Steinhoff-Wagner, Flor, Schönhusen and Metges2013).

Immunoglobulin antibodies in bovine colostrum are central to the immunological link that occurs when the mother transfers passive immunity to the offspring (Hurley and Theil, Reference Hurley and Theil2011). There are three major immunoglobulin isotypes or classes: IgG (subclasses IgG1 and IgG2), IgM and IgA. In beef-suckler cow colostrum, IgG1 predominates (91%), followed by IgM (5%), IgA (2%) and IgG2 (2%) (McGee et al., Reference McGee, Drennan and Caffery2005 and Reference McGee, Drennan and Caffery2006). Most published research pertaining to calf passive immunity only emphasises IgG or IgG1. Although the focus of this paper is passive immunity in relation to immunoglobulins, in terms of immuno-protection, it is recognised that colostrum contains a wide variety of other immune-related factors (Hurley and Theil, Reference Hurley and Theil2011; McGrath et al., Reference McGrath, Fox, McSweeney and Kelly2016).

Colostrogenesis

Colostrum is formed during late pregnancy when mammary cells are proliferating and differentiating in preparation for lactation; this process is called colostrogenesis (Baumrucker et al., Reference Baumrucker, Burkett, Magliaro-Macrina and Dechow2010). Colostral immunoglobulins arise from systemic and local sources (Hurley and Theil, Reference Hurley and Theil2011). Bovine IgG1 is specifically transported by a process of transcytosis across the mammary epithelial cells during colostrogenesis by an IgG1-specific receptor, FcRn (Hurley and Theil, Reference Hurley and Theil2011). In beef-suckler cows, systemic concentrations of IgG1 and IgG2 in blood are approximately equal (McCutcheon et al., Reference McCutcheon, Caffrey, Kelleher and Brophy1991; McGee et al., Reference McGee, Drennan and Caffery2005 and Reference McGee, Drennan and Caffery2006). Concentrations of IgG1 start to decrease about 3 to 4 weeks prepartum and cease close to calving, whereas conversely, concentrations of blood IgG2 generally increase prepartum (Olson et al., Reference Olson, Woodard, Bull and Everson1981a; McCutcheon et al., Reference McCutcheon, Caffrey, Kelleher and Brophy1991; Guy et al., Reference Guy, McFadden, Cockrell and Besser1994; McGee et al., Reference McGee, Drennan and Caffery2005 and Reference McGee, Drennan and Caffery2006). The appearance of blood IgG2 in bovine colostrum is thought to occur via leaky-tight junctions in the blood-milk barrier (Samarütel et al., Reference Samarütel, Baumrucker, Gross and Dechow2016). However, the specific mechanisms of colostrogenesis remain undefined.

The decrease in blood IgG1 concentrations prepartum is much greater in dairy (Guy et al., Reference Guy, McFadden, Cockrell and Besser1994) and beef × dairy (McGee et al., Reference McGee, Drennan and Caffery2005; Murphy et al., Reference Murphy, Drennan, O’Mara and Earley2005; Earley et al., Reference Earley, Tiernan, Duffy, Dunn, Waters, Morrison and McGee2018) cows compared to beef breed cows, implying that more IgG1 is transferred into colostrum for the dairy and dairy crossbred genotypes. Within several weeks postpartum, concentrations of blood IgG1 are equivalent to pre-colostrogenesis (McGee et al., Reference McGee, Drennan and Caffery2005 and Reference McGee, Drennan and Caffery2006).

There are inconsistent effects across studies on changes in beef-suckler cow blood IgM concentrations prepartum with declines observed in some but not other experiments (Olson et al., Reference Olson, Woodard, Bull and Everson1981a; McGee et al., Reference McGee, Drennan and Caffery2005 and Reference McGee, Drennan and Caffery2006); concentrations of maternal blood IgA were found to be relatively constant (McGee et al., Reference McGee, Drennan and Caffery2005 and Reference McGee, Drennan and Caffery2006). This is not overly surprising as IgM and IgA found in bovine colostrum are produced by plasma cells in mammary tissue (Hurley and Theil, Reference Hurley and Theil2011).

Blood IgG1 (Norman et al., Reference Norman, Hohenboken and Kelley1981), and IgG1, IgG2 and IgA (McGee et al., Reference McGee, Drennan and Caffery2006) concentrations were reported to be higher in older/multiparous compared to younger/primiparous beef cows, but IgM did not differ in either study.

Colostrum yield

Few published studies have quantified colostrum yield in beef-suckler cows (Figure 1). Considerable between-animal variation in first-milking colostrum yield is evident in beef breeds (Logan, Reference Logan1977; Field et al., Reference Field, Bretzlaff, Elmore and Rupp1989; McGee et al., Reference McGee, Drennan and Caffery2005), dairy breeds (Kehoe et al., Reference Kehoe, Heinrichs, Moody, Jones and Long2011; Conneely et al., Reference Conneely, Berry, Sayers, Murphy, Lorenz, Doherty and Kennedy2013; Samarütel et al., Reference Samarütel, Baumrucker, Gross and Dechow2016; Silva-del-Rio et al., Reference Silva-del-Río, Rolle, García-Muñoz, Rodríguez-Jiménez, Valldecabres, Lago and Pandey2017) and their crosses, that is, beef × dairy (McGee et al., Reference McGee, Drennan and Caffery2005 and Reference McGee, Drennan and Caffery2006). For example, in multiparous beef-suckler cows managed similarly, McGee et al. (Reference McGee, Drennan and Caffery2005) reported that first-milking colostrum yield ranged from 740 to 5490 ml for Charolais and from 1660 to 7230 ml for beef × Friesian animals.

Figure 1 Mean first-milking colostrum yield (kilogram or litres*) in beef and dairy cows/heifers. For interpretation of volume v. weight values, the density of colostrum is ~1.05 g/ml. References for this figure are provided in the text or Supplementary Material S1.

Compared to beef-suckler cows, mean first-milking colostrum yields reported for dairy cows are generally much higher (Figure 1); mean colostrum yield reported for beef-suckler cows is 2.7 (range 0.6 to 5.6) l; corresponding values for dairy cows are 6.7 (3.7 to 9.5). Differences in genotype, parity and maternal nutrition are likely contributory factors to some of this variance within the beef and dairy categories (see later). Overall, considering that dairy cows are genetically selected for milk production the higher values are expected. Correspondingly, the higher first-milking colostrum yield of beef × dairy cows compared to beef breed cows (Table 1), also reflects their milk yield (Murphy et al., Reference Murphy, Drennan, O’Mara and Earley2005).

Table 1 Effect of beef-suckler cow breed type on first-milking colostrum yield and/or immunoglobulin concentrations

^a,b Within column and individual experiment, values with different superscripts differ significantly (at least P < 0.05).

¹ References for this Table are provided in the text or Supplementary Material S1.

² A = Angus; AA = Aberdeen Angus; B = Brahman; BA = Blonde d’Aquitaine; BB = Belgian Blue; BG = Blue Grey; C = Charolais; F = Friesian; H = Hereford; J = Jersey; K = Kiwi; L = Limousin; S = Simmental; and their crosses.

³ Yield = litres (l) or kilogram.

⁴ Suckled (v. milked).

First-milking colostrum yield was found to be higher in multiparous beef × dairy cows compared to first-parity animals (Table 2). Similarly, Langholz et al. (Reference Langholz, Schmidt, Derenbach and Kim1987) reported that colostrum intake of calves born to multiparous beef-suckler cows was higher, both on an absolute basis (×1.67) and relative to birth weight (×1.44), compared to calves born to heifers. This likely reflects the lower mammary gland development in heifers. Likewise, a higher colostrum yield in multiparous than primiparous dairy cows was observed in many (e.g. × 1.38, Conneely et al., Reference Conneely, Berry, Sayers, Murphy, Lorenz, Doherty and Kennedy2013) but not all (e.g. × 1.03, Kehoe et al., Reference Kehoe, Heinrichs, Moody, Jones and Long2011) studies.

Table 2 Effect of beef-suckler cow parity/age on first-milking colostrum yield and/or immunoglobulin concentrations

^a,b Within column and individual experiment, values with different superscripts differ significantly (at least P < 0.05).

¹ References for this Table are provided in the text or Supplementary Material S1.

² PP = primiparous; MP = multiparous.

³ Yield = litres (l) or kilogram.

⁴ γ-Globulin.

Although there is an industry-wide perception that colostrum yield of beef-suckler cows is reduced through under-nutrition prepartum, this effect is not clearly evident (Table 3). Ambiguity between studies may be partially attributed to large variance combined with relatively small numbers of experimental animals used, but also to the degree of underfeeding and the cows ability to mobilise body-fat reserves, which negates the effect of nutrient restriction. Likewise, recent research with dairy cows has shown no effect of dry-period dietary energy level on first-milking colostrum yield (Mann et al., Reference Mann, Leal Yepes, Overton, Lock, Lamb, Wakshlag and Nydam2016; Dunn et al., Reference Dunn, Ashfield, Earley, Welsh, Gordon, McGee and Morrison2017a).

Table 3 Effect of prepartum dietary nutrition or body condition score (BCS) on first-milking colostrum yield and/or immunoglobulin concentrations in beef-suckler cows

NRC = National Research Council; ME = metabolisable energy.

¹ References for this Table are provided in the text or Supplementary Material S1.

² These studies used only heifers.

³ Colostrum yield (litre (l) or kg).

⁴ = no statistically significant difference (P > 0.05); ↑ statistically significant increase; ↓statistically significant decrease.

⁵ Grass silage @75% dry matter digestibility (DMD).

Colostrum immunoglobulin concentration

Within beef and beef × dairy breeds (McGee et al., Reference McGee, Drennan and Caffery2005; Dunn et al., Reference Dunn, Duffy, Gordon, Morrison, Argűello, Welsh and Earley2018) and dairy breeds (Conneely et al., Reference Conneely, Berry, Sayers, Murphy, Lorenz, Doherty and Kennedy2013; Dunn et al., Reference Dunn, Ashfield, Earley, Welsh, Gordon and Morrison2017b), there is substantial variation between cows in colostrum IgG (and immunoglobulin subclass) concentration at first milking. Within-quarter fractions of first-milking colostrum have similar concentrations of immunoglobulins in beef × dairy (IgG1, IgG2, IgM and IgA; McGee et al., Reference McGee, Drennan and Caffery2006) and dairy (IgG1; Le Cozler et al., Reference Le Cozler, Guatteo, Le Drean, Turba, Leboeuf, Pecceu and Guinard-Flament2016) cows. In beef-suckler cows immunoglobulin concentrations were found not to differ significantly between the front and rear quarters of the udder (IgG1, IgG2, IgM, Halliday et al., Reference Halliday, Russel, Williams and Peart1978; IgG1, Earley et al., Reference Earley, McGee, Fallon, Drennan, Murray and Farrell2000; IgG1, IgG2, IgM, IgA, McGee et al., Reference McGee, Drennan and Caffery2006), although Langholz et al. (Reference Langholz, Schmidt, Derenbach and Kim1987) reported lower concentrations (IgG: −5%, IgM: −16% IgA: −19%) in the front compared to the rear quarters. Similarly, in dairy cows, mean concentrations of immunoglobulin were shown not to differ significantly between the front and rear quarters, although variation between individual quarters was large (IgG, IgG2, Samarütel et al., Reference Samarütel, Baumrucker, Gross and Dechow2016), whereas in contrast, Le Cozler et al. (Reference Le Cozler, Guatteo, Le Drean, Turba, Leboeuf, Pecceu and Guinard-Flament2016) reported that IgG1 concentration was lower (−6%) in front than hind quarters.

In dairy cows, there is normally a negative, but relatively weak, association (r = −0.16 to −0.37) between colostrum volume/weight and IgG concentration (Morin et al., Reference Morin, Nelson, Reid, Nagy, Dahl and Constable2010; Kehoe et al., Reference Kehoe, Heinrichs, Moody, Jones and Long2011; Conneely et al., Reference Conneely, Berry, Sayers, Murphy, Lorenz, Doherty and Kennedy2013; Silva-del-Rio et al., Reference Silva-del-Río, Rolle, García-Muñoz, Rodríguez-Jiménez, Valldecabres, Lago and Pandey2017), although in some studies no statistically significant relationship was found (Baumrucker et al., Reference Baumrucker, Burkett, Magliaro-Macrina and Dechow2010; Samarütel et al., Reference Samarütel, Baumrucker, Gross and Dechow2016). Similarly, Odde (Reference Odde1988) reported a correlation of −0.43 between colostrum volume and IgG1 concentration in beef heifers, whereas conversely, Logan (Reference Logan1977) found no relationship in beef cows, which may be due to the particularly low colostrum yield obtained in that study (Table 1).

In dairy cow studies colostral IgG concentrations are usually negatively associated with interval from calving-to-first-milking, although the rate of decline can vary substantially; 1.1% (Conneely et al., Reference Conneely, Berry, Sayers, Murphy, Lorenz, Doherty and Kennedy2013) to 3.7% (Morin et al., Reference Morin, Nelson, Reid, Nagy, Dahl and Constable2010) per hour. In general, a decline in colostral IgG concentration is not readily obvious until after approximately 12 h postpartum (Conneely et al., Reference Conneely, Berry, Sayers, Murphy, Lorenz, Doherty and Kennedy2013; Dunn et al., Reference Dunn, Ashfield, Earley, Welsh, Gordon and Morrison2017b). Although this occurrence has not been quantified in beef-suckler cows, the aforementioned duration before there is an appreciable decline in colostral immunoglobulin concentration far exceeds time to first-suckling for beef calves in most situations (see later).

Like first-milking colostrum, there is also considerable variance in the immunoglobulin concentration of second- (and subsequent) milking colostrum in beef-suckler (McGee et al., Reference McGee, Drennan and Caffery2005 and Reference McGee, Drennan and Caffery2006) and dairy (Silva-del-Rio et al., Reference Silva-del-Río, Rolle, García-Muñoz, Rodríguez-Jiménez, Valldecabres, Lago and Pandey2017) cows, some of which may partly reflect residual effects of first-milking colostrum. Nevertheless, immunoglobulin (subclass) concentrations in second-milking colostrum are substantially lower (~0.5) than first-milking colostrum in beef (Vann et al., Reference Vann, Holloway, Carstens, Boyd and Randel1995; McGee et al., Reference McGee, Drennan and Caffery2005), beef × dairy (Logan, Reference Logan1977; McGee et al., Reference McGee, Drennan and Caffery2005 and Reference McGee, Drennan and Caffery2006) and dairy (Silva-del-Rio et al., Reference Silva-del-Río, Rolle, García-Muñoz, Rodríguez-Jiménez, Valldecabres, Lago and Pandey2017) cows.

It is clear from the few within-study comparisons of dairy and beef cows published that beef cows have greater first-milking colostrum IgG1 concentrations (e.g. 113.4 v. 42.7 mg/ml; Guy et al., Reference Guy, McFadden, Cockrell and Besser1994); however, this is not as apparent across studies. The variance in mean colostrum IgG concentrations (determined using only one-of-two recognised quantitative methods, RID and ELISA) across studies for beef and dairy cows (Figure 2), is substantial; mean IgG/IgG1 concentration reported for beef cows is 99 mg/ml (range 31 to 200) and dairy cows is 66 mg/ml (27 to 117). Again, across-study differences in factors such as genotype, parity and maternal nutrition are likely contributory causes to some of the variance within the beef and dairy cow categories (see later) but clearly, there is a large overlap. The upper ends of the range in immunoglobulin concentrations for dairy cows are values more customarily associated with beef-suckler cows. Possible reasons proposed by the authors of those studies for such deviations include, relatively low milk-yielding cow genotypes, short calving-to-colostrum-collection interval, superior nutritional and health-related management of the cow, dissimilarities in sample preparation, and crucially, differences associated with laboratory tests, as discussed earlier. Again, this substantial variance begs the question, how comparable are ‘quantitative’ values across studies and what concentration of IgG or IgG1 constitutes ‘good-quality’ colostrum?

Figure 2 Mean first-milking colostrum IgG (IgG1*) concentrations (mg/ml) in beef and dairy cows/heifers determined using single radial immune diffusion or ELISA**. References for this figure are provided in the text or Supplementary Material S1.

Colostrum immunoglobulin concentrations are mainly equivalent between beef × dairy, beef × (beef × dairy), beef × beef and the common (pure) beef breeds (Table 1). This seems counterintuitive as by crossing a beef breed with a dairy breed, the crossbred would be expected to produce colostrum with an immunoglobulin concentration, which is intermediate.

Differences in colostrum immunoglobulin (subclass) concentrations between primiparous and multiparous beef-suckler cows are generally relatively small and do not differ statistically (Table 2). Contrastingly, in dairy breeds, usually older cows have higher colostrum immunoglobulin concentrations than younger cows (Kehoe et al., Reference Kehoe, Heinrichs, Moody, Jones and Long2011; Le Cozler et al., Reference Le Cozler, Guatteo, Le Drean, Turba, Leboeuf, Pecceu and Guinard-Flament2016; Dunn et al., Reference Dunn, Ashfield, Earley, Welsh, Gordon and Morrison2017b; Silva-del-Rio et al., Reference Silva-del-Río, Rolle, García-Muñoz, Rodríguez-Jiménez, Valldecabres, Lago and Pandey2017), although clear divergence among primiparous and multiparous dairy cows is only evident in some studies (Conneely et al., Reference Conneely, Berry, Sayers, Murphy, Lorenz, Doherty and Kennedy2013).

Analogous to the situation with colostrum yield, in commercial practice it is perceived that maternal under-nutrition during gestation has an adverse effect on colostrum ‘quality’. However, in most published studies dietary energy and/or protein restriction during pregnancy, or reduced body condition score (BCS) at parturition (a proxy for maternal under-nutrition), has no adverse effect on colostrum immunoglobulin concentrations in beef-suckler cows or heifers (Table 3). Similarly, in dairy cows, concentrate supplementation of grass silage during the dry period had no effect on first-milking colostrum IgG concentration (Dunn et al., Reference Dunn, Ashfield, Earley, Welsh, Gordon, McGee and Morrison2017a). Indeed, Mann et al. (Reference Mann, Leal Yepes, Overton, Lock, Lamb, Wakshlag and Nydam2016) reported that feeding dairy cows 150% of energy requirements during the dry period resulted in a lower colostrum IgG concentration compared to those fed to requirements.

Although not as applicable to beef-suckler cows commercially, there is evidence in dairy cows that shortening the dry period from about 8 to 4 weeks has little effect on colostrum IgG concentration (but reduces first-milking colostrum yield), and that omitting the dry period negatively affects both the volume and IgG concentration in colostrum (e.g. Mayasari et al., Reference Mayasari, de Vries Reilingh, Nieuwland, Remmelink, Parmentier, Kemp and van Knegsel2015).

Colostrum immunoglobulin mass

Colostrum immunoglobulin mass is the volume × concentration of immunoglobulin (or subclasses) of that colostrum (McGee et al., Reference McGee, Drennan and Caffery2005). Ultimately, an optimum mass of colostrum IgG needs to be absorbed by the newborn calf within a relatively short time period after birth (see later). In line with the substantial variation in colostrum yield and immunoglobulin concentration discussed earlier, there is also considerable variation in colostrum immunoglobulin mass produced by beef-suckler (McGee et al., Reference McGee, Drennan and Caffery2005 and Reference McGee, Drennan and Caffery2006; Vann et al., 2005;) and dairy (Baumrucker et al., Reference Baumrucker, Burkett, Magliaro-Macrina and Dechow2010; Morin et al., Reference Morin, Nelson, Reid, Nagy, Dahl and Constable2010; Samarütel et al., Reference Samarütel, Baumrucker, Gross and Dechow2016) cows.

This infers that beef-suckler cows producing higher volumes of colostrum rather than colostrum with greater concentrations of IgG1 will likely have a greater mass of IgG1. In other words, colostrum ‘quantity’ rather than ‘quality’ is the likely limiting factor with beef-suckler cows, which is in direct contrast to the dairy cow (Baumrucker et al., Reference Baumrucker, Burkett, Magliaro-Macrina and Dechow2010). The source of colostrum immunoglobulin mass variation is not well understood.

Although hardly any studies have quantified both colostrum yield and immunoglobulin concentration of beef-suckler cows (Figure 1 and Tables 1 to 3), even fewer have reported colostrum immunoglobulin mass production. Nevertheless, first-milking colostrum immunoglobulin mass was shown to be affected by cow genotype (Vann et al., Reference Vann, Holloway, Carstens, Boyd and Randel1995; McGee et al., Reference McGee, Drennan and Caffery2005), parity and maternal nutrition level in late gestation (McGee et al., Reference McGee, Drennan and Caffery2006). In addition, induction of calving by 2 weeks before expected parturition reduced colostrum IgG mass by 43% in beef cows (Field et al., Reference Field, Bretzlaff, Elmore and Rupp1989).

Passive immunity in the neonatal calf

Efficiency of immunoglobulin absorption

In beef-suckler cows, mass of colostrum IgG1 consumed per kilogram birth weight within 1 h postpartum was the most significant variable determining calf passive immune status (McGee and Drennan, Reference McGee and Drennan2007). Unlike dairy calf studies, there is little published information on AEA of immunoglobulin (subclasses) in beef-suckler calves, as the quantity of colostrum consumed is much more difficult to assess, and thus rarely determined. Typical mean AEA for dairy calves across studies ranges from 16% to 45%, although this varies widely within study, from 8% to 60% (mean 28%), despite standardised feeding (Halleran et al., Reference Halleran, Sylvester and Foster2017). Beef-suckler calves offered approximately 4% to 5% of birth weight in first-milking colostrum within 1 h postpartum had mean AEA at 8 h post-feeding of 0.36 to 0.43, 0.34 to 0.46, 0.44 to 0.64, 0.42 to 0.56 and 0.37 to 0.44 for IgG1, IgG2, IgM, IgA and Ig-total, respectively (McGee et al., Reference McGee, Drennan and Caffery2005 and Reference McGee, Drennan and Caffery2006).

It is evident that the passive immune status of suckler-bred calves is superior to dairy-bred calves under controlled research farm conditions, where it is ensured that calves suckle the dam and/or are fed sufficient colostrum in a timely manner post-parturition (Earley et al., Reference Earley, McGee, Fallon, Drennan, Murray and Farrell2000; Dunn et al., Reference Dunn, Duffy, Gordon, Morrison, Argűello, Welsh and Earley2018). However, on commercial farms beef-suckler calves do not necessarily have a superior passive immune status compared to dairy calves (e.g. Todd et al., Reference Todd, McGee, Tiernan, Crosson, O’Riordan, McClure, Lorenz and Earley2018). Reasons for such a discrepancy are likely to be multifaceted, involving a number of the key factors shown in Figure 3.

Figure 3 Key factors affecting passive immunity in beef-suckler calves.

Within beef-suckler cow genotypes, generally passive immunity of calves from the common beef breeds is similar, but lower than calves from beef × dairy cows (Table 4). As discussed earlier, this effect can largely be attributed to the significantly greater colostrum immunoglobulin mass produced by beef × dairy compared to beef breeds (McGee et al., Reference McGee, Drennan and Caffery2005). Similarly, there is evidence that passive immunity is greater in calves from ‘dual-purpose’ breeds, for example, Simmental (Murphy et al., Reference Murphy, Drennan, O’Mara and Earley2005). This highlights the importance of milk production-related ‘maternal’ traits in the beef dam, and has implications for beef breeding policies. Apparent efficiency of absorption of colostral immunoglobulins does not seem to differ between purebred and crossbred beef calves (Vann et al., Reference Vann, Holloway, Carstens, Boyd and Randel1995) or between calves from beef and beef × dairy dams (McGee et al., Reference McGee, Drennan and Caffery2005).

Table 4 Effect of beef-suckler cow breed type on blood immunoglobulin concentrations in their calves at 24 to 72 h postpartum

^a,b Within column and individual experiment, values with different superscripts differ significantly (at least P < 0.05).

¹ References for this Table are provided in the text or Supplementary Material S1.

² PP = primiparous; MP = multiparous; A = Angus; AA = Aberdeen Angus; BA = Blonde d’Aquitaine; BB = Belgian Blue; BG = Blue Grey; C = Charolais; F = Friesian; H = Hereford; J = Jersey; K = Kiwi; L = Limousin; S = Simmental; and their crosses.

³ Zinc Sulphate Turbidity (ZST) test.

⁴ Blood sampled between 2 and 8 days postpartum.

⁵ P = 0.07.

Calves from older beef-suckler cows generally have a higher immune status than those from younger and principally, primiparous cows (Table 5). This differential is likely to be due to a lower colostrum immunoglobulin mass produced by primiparous cows primarily attributed to a lower colostrum yield (McGee et al., Reference McGee, Drennan and Caffery2006), rather than lower immunoglobulin concentration (Table 2).

Table 5 Effect of beef-suckler cow parity/age on blood immunoglobulin concentrations in their calves at 24 to 72 h postpartum

^a,b,c Within column and individual experiment, values with different superscripts differ significantly (at least P < 0.05).

¹ References for this Table are provided in the text or Supplementary Material S1.

² PP = primiparous; MP = multiparous; C = Charolais; F = Friesian; L = Limousin; and their crosses.

³ Zinc Sulphate Turbidity (ZST) test.

⁴ Blood sampled between 2 and 8 days postpartum.

⁵ Effect of age, P < 0.001.

⁶ P = 0.08.

Most published research has shown no adverse impact of maternal dietary restriction, or low cow BCS, on passive immunity of beef-suckler calves (Table 6). Similarly, Dunn et al. (Reference Dunn, Ashfield, Earley, Welsh, Gordon, McGee and Morrison2017a) found no effect of concentrate supplementation of dairy cows during the dry period on calf serum IgG or AEA at 24 h after birth. A small number of studies have reported negative effects of maternal under-nutrition which are most likely not related to colostrum immunoglobulin concentration (Table 3) but rather a lower colostrum immunoglobulin mass, and also, possibly inhibitory effects on immunoglobulin absorption (Table 3; McGee et al., Reference McGee, Drennan and Caffery2006). There is some evidence that trace-mineral supplementation of the beef cow during late pregnancy may be important in relation to calf passive immunity (Table 4). Genetic, environmental and management factors affecting ‘length of pregnancy’ may have direct and indirect effects on calf passive immunity, although there is little quantifiable research published in this area. Calves from cows induced to calve 2 weeks before expected parturition were shown to have decreased serum IgG concentrations, in the order of 50% (Field et al., Reference Field, Bretzlaff, Elmore and Rupp1989); this inferior passive immunity may be attributed to a reduction in colostrum IgG mass produced, reduced absorption of IgG by the induced calves, or both. Alternatively, a prolonged gestation, due to differences in factors including dam and sire genotype, cow parity and calf sex may result in relative oversize of the calf and thus have an adverse effect on passive transfer of immunity, as discussed previously.

Table 6 Effect of maternal prepartum dietary nutrition or body condition score (BCS) of beef-suckler cows on blood immunoglobulin concentrations in their calves at 24 to 72 h postpartum

¹ References for this Table are provided in the text or Supplementary Material S1.

² TMR = Total Mixed Ration; NRC = National Research Council; ARC = Agricultural Research Council.

³ These studies used only beef heifers.

⁴ = no statistically significant difference (P > 0.05); ↑ statistically significant increase; ↓statistically significant decrease.

⁵ Blood sampled between 2 and 8 days postpartum.

⁶ Zinc Sulphate Turbidity (ZST) test.

⁷ Grass silage @ 75% dry matter digestibility (DMD).

⁸ No effect of maternal nutrition on calf IgG but calves fed colostrum from restricted cows had less (P < 0.07) circulating IgG.

More ‘targeted’ passive immunity in beef-suckler calves can be achieved through vaccination of the pregnant cow against particular diseases (Earley et al., Reference Earley, Tiernan, Duffy, Dunn, Waters, Morrison and McGee2018).

Similar to colostrum immunoglobulin concentration, there is considerable within- and especially across-study variance in beef calf blood immunoglobulin (subclass) concentrations (Tables 4 and 5). Reasons for such variability may be attributed to a combination of the factors discussed previously and illustrated in Figure 3, but also laboratory methodology-related impacts (see earlier). Likewise, large variation in mean calf blood IgG concentration is evident across dairy calf studies, even when a relatively large volume of colostrum is fed soon after birth, for example, 20.7 (Dunn et al., 2017) to 39.1 mg/ml (Conneely et al., Reference Conneely, Berry, Murphy, Lorenz, Doherty and Kennedy2014) IgG.

Passive immunity test results are generally categorised for FPT using test-specific cut-off values. For dairy calves cut-off points applied for FPT can vary from 3.5 to 18 mg/ml blood serum/plasma IgG (Raboisson et al., Reference Raboisson, Trillat and Cahuzac2016), but the most commonly used cut-off is 10 mg/ml IgG (e.g. Hogan et al., Reference Hogan, Doherty, Fagan, Kennedy, Conneely, Brady, Ryan and Lorenz2015; Raboisson et al., Reference Raboisson, Trillat and Cahuzac2016), although the basis of such widespread adoption is not clearly apparent. Moreover, cut-offs for tests that indirectly estimate IgG concentration are most often established by simply identifying the test equivalent to 10 mg/ml serum IgG (Hogan et al., Reference Hogan, Doherty, Fagan, Kennedy, Conneely, Brady, Ryan and Lorenz2015). Similarly, multiple IgG cut-off values, ranging between 8 and 24 mg/ml, have been applied to classify FPT in beef calves (Raboisson et al., Reference Raboisson, Trillat and Cahuzac2016). Clearly, the ‘prevalence’ of FPT can fluctuate depending on what cut-off value is assumed or how it is classified. Collectively, these observations suggest that more research is needed to validate various test cut-off values for beef calves, based on their relationships with key health and performance outcome measures, such as morbidity, mortality and growth (e.g. Todd et al., Reference Todd, McGee, Tiernan, Crosson, O’Riordan, McClure, Lorenz and Earley2018). Furthermore, cognisance of potential vagaries associated with test methodologies used to measure blood immunoglobulin concentrations must be borne in mind when interpreting results, particularly concerning cut-off points for FPT; absolute values may be an artefact of the test used.