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.
Introduction
The importance of colostrum-derived passive immunity, through intestinal absorption of colostral immunoglobulins, to the mortality, morbidity and subsequent growth and welfare of a newborn beef calf is recognised internationally (Hickson et al., Reference Hickson, Back, Martin, Kenyon and Morris2016; Raboisson et al., Reference Raboisson, Trillat and Cahuzac2016; Homerosky et al., Reference Homerosky, Timsit, Pajor, Kastelic and Windeyer2017; Todd et al., Reference Todd, McGee, Tiernan, Crosson, O’Riordan, McClure, Lorenz and Earley2018). In addition, the negative economic impact that failure of passive transfer (FPT) has on beef farming enterprises has been quantified (Raboisson et al., Reference Raboisson, Trillat and Cahuzac2016). However, in comparison to dairy calves, there is much less research carried out on passive immunity and associated factors in beef-suckler calves. Furthermore, the numerous existing reviews in the scientific literature on bovine neonatal immunity almost exclusively relate to dairy calves. Although much of the underlying biology associated with passive immunity applies equally to dairy and beef calves, nevertheless genetic, environmental and management circumstances are usually extremely different, often resulting in them having a very diverse immune status. Therefore, the objective of this paper is to provide a comprehensive review of the scientific literature, including work conducted in our research centre, on factors affecting passive immunity of beef-suckler calves. To put findings in context, appropriate comparison with dairy cows and calves, mainly Holstein-Friesian, is made. The contrast between dairy and beef breeds is also pertinent as in some countries replacement breeding heifers for the beef cow herd are often sourced from the dairy herd, that is, beef × dairy cows.
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.
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).
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.
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).
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?
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
Immunoglobulin absorption
Ingestion of colostrum is essential for providing the neonatal calf with systemic immunologic protection during at least the first 2 to 4 weeks of life until its own active immune system is functional. It is recommended that beef calves should stand and suckle within 2 h of calving; if not, the dam should be restrained and the calf should be assisted. If the calf is unable or unwilling to suckle, the cow should be milked out by hand and the calf fed colostrum with a nipple/teat-bottle or oesophageal/‘stomach’ tube-feeder (Larson et al., Reference Larson, Tyler, Schultz, Tessman and Hostetler2004).
Time of colostrum ingestion
It is well established that immunoglobulin absorption by pinocytosis across the intestinal epithelium into the neonatal circulation decreases with time postpartum, and ceases after 24 to 48 h; this is known as ‘closure’. Consequently, for the newborn calf, the length of time between birth and first suckling is fundamental in the acquisition of passive immunity. For example, Langholz et al. (Reference Langholz, Schmidt, Derenbach and Kim1987) reported that beef-suckler calves which suckled within 3 h postpartum, had serum IgG, IgM and IgA concentrations at 36 h postpartum that were proportionately 1.68, 1.57 and 1.66, higher, respectively, compared to calves that suckled after 3 h. In terms of colostrum management, one of the obvious primary differences between dairy and beef calves is that the beef-suckler calf usually remains with and suckles its dam, whereas typically, the dairy calf is removed from its dam soon after birth and generally receives colostrum through artificial means.
For the beef calf to ingest sufficient colostrum, it must first stand, walk, find the dam’s teat and suckle, while simultaneously the dam must stand, have a good maternal bond with the calf, produce an adequate volume of colostrum with adequate concentrations of immunoglobulins and have teats that can be grasped by the calf (Larson et al., Reference Larson, Tyler, Schultz, Tessman and Hostetler2004). Circumstances that impinge on these behavioural elements have a negative impact on passive immunity in beef calves.
The mean interval between birth and first standing-up for beef-suckler calves varies from 30 min to almost 2 h; the mean time to first suckling without assistance generally ranges from 60 to 260 min, but it can be much longer for individual animals (Langholz et al., Reference Langholz, Schmidt, Derenbach and Kim1987; Odde, Reference Odde1988; Le Neindre and Vallet, Reference Le Neindre and Vallct1992; Hickson et al., Reference Hickson, Lopez-Villalobos, Kenyon and Morris2008). In beef herds with easy calvings, most calves suckle within 4 h (Le Neindre and Vallet, Reference Le Neindre and Vallct1992; Homerosky et al., Reference Homerosky, Timsit, Pajor, Kastelic and Windeyer2017).
Differences in the latency to first suckle is influenced by breed – usually longer for dairy breeds than beef breeds, parity – usually longer for primiparous than multiparous; and, anatomical differences in the udder and teat, which can be related to breed and parity (Langholz et al., Reference Langholz, Schmidt, Derenbach and Kim1987; Mayntz and Sender, Reference Mayntz and Sender2006). For instance, more outward-pointing teats are associated with improved colostrum status of beef calves (Hickson et al., Reference Hickson, Back, Martin, Kenyon and Morris2016). Dystocia has a large influence on time to first suckling. This can manifest itself as less vigorous calves resulting in a longer interval from calving-to-standing, but also a poorer mothering score, a measure of cow-calf bonding (Odde, Reference Odde1988; Homerosky et al., Reference Homerosky, Timsit, Pajor, Kastelic and Windeyer2017). Compared to beef calves that experienced a non-assisted birth, assisted calves took longer to attempt to stand (×2.03), to successfully stand (×1.39) and to suckle (×1.88) (Hickson et al., Reference Hickson, Lopez-Villalobos, Kenyon and Morris2008). Similarly, Homerosky et al. (Reference Homerosky, Timsit, Pajor, Kastelic and Windeyer2017) reported that the proportion of beef calves that failed to consume colostrum by 4 h after birth was 0.14, 0.39 and 0.64 for unassisted, easy assist and difficult assist deliveries, respectively. Consequently, factors influencing feto-maternal disproportion need to be managed in order to reduce calving difficulty and negative effects on calf vigour.
Voluntary colostrum consumption and feeding
Mean duration of first suckling, until full, for newborn beef-suckler calves is between 20 and 26 min (e.g. Langholz et al., Reference Langholz, Schmidt, Derenbach and Kim1987). When calves are limited to two sucklings, 4 and 9 h after birth, they can suckle equivalent to 8% of their BW (Le Neindre and Vallet, Reference Le Neindre and Vallct1992). Langholz et al. (Reference Langholz, Schmidt, Derenbach and Kim1987) reported that beef-suckler calves voluntarily suckled 1.6 kg of colostrum, equivalent to 4.1% of BW, at birth, and by 12 h postpartum had consumed a total of 2.8 kg of colostrum, equivalent to 7.4% of BW. Similarly, earlier reports (pre-1997) in the literature have shown that on average, at first feed, beef and dairy calves will voluntarily drink between 1.9 and 2.7 l from a bucket, suckle between 1.6 and 2.6 l from a teat-bottle, or voluntarily suckle from its dam between 1.5 and 2.5 kg of colostrum (McGee et al., Reference McGee, Drennan and Caffery2006). However, recent studies indicate a higher mean voluntary consumption of colostrum via teat-bottle (3.4 l, 7.3% of birth weight) by dairy calves at their first feed (Bonk et al., Reference Bonk, Nadalin, Heuwieser and Veira2016).
Compared to suckling the dam, artificial feeding has the benefit that a known volume of colostrum is administered. When properly used, oesophageal feeding has the advantage over a teat-bottle that relatively large volumes of colostrum can be fed, and rapidly, for example, 3 l fed in 5.2 v. 17.6 min (Desjardins-Morrissette et al., Reference Desjardins-Morrissette, van Niekerk, Haines, Sugino, Oba and Steele2018). It is generally accepted that the oesophageal groove reflex is not triggered when using a tube-feeder resulting in deposition of colostrum in the reticulorumen, compared to directly in the omasum and abomasum when suckling; nevertheless, controlled studies have shown similar IgG concentrations in calves fed relatively high volumes (3.0 to 3.4 l) of colostrum with a stomach-tube compared to a teat-bottle (Bonk et al., Reference Bonk, Nadalin, Heuwieser and Veira2016; Desjardins-Morrissette et al., Reference Desjardins-Morrissette, van Niekerk, Haines, Sugino, Oba and Steele2018). However, Godden et al. (Reference Godden, Haines, Konkol and Peterson2009) found no difference in calf passive immunity between a teat-bottle and tube-feeder when feeding a large volume (3 l) of colostrum ‘replacer’, but higher immunity and greater apparent efficiency of absorption (AEA) for the teat-bottle when feeding a smaller volume (1.5 l). This indicates that colostrum entering the rumen may have a more demonstrable effect on abomasal emptying rates, and AEA of IgG when relatively small rather than large volumes of colostrum are fed (Desjardins-Morrissette et al., Reference Desjardins-Morrissette, van Niekerk, Haines, Sugino, Oba and Steele2018). In this regard, these latter findings may be more applicable to calves from lower-yielding beef cows.
In practice, colostrum feeding of the newborn beef-suckler calf is often based on modified dairy calf guidelines, although in most circumstances this is probably inappropriate. For dairy calves, colostral management recommendations for adequate passive immunity transfer include providing a colostrum IgG mass of at least 150 to 200 g, equivalent to feeding 3 l of colostrum within 2 h after birth by oesophageal-tube (Chigerwe et al., Reference Chigerwe, Tyler, Schultz, Middleton, Stevens and Spain2008). More recently, Conneely et al. (Reference Conneely, Berry, Murphy, Lorenz, Doherty and Kennedy2014) concluded that serum IgG and AEA of IgG was greatest in dairy calves fed 8.5% of birth weight in colostrum, equivalent to 3.2 (range 2.0 to 4.2) l, using a stomach-tube within 2 h postpartum. Similarly, Dunn et al. (Reference Dunn, Ashfield, Earley, Welsh, Gordon, McGee and Morrison2017a) recommended that dairy calves be fed 10% of birth weight in colostrum imminently after birth.
However, with beef-suckler cows these volume-targets would often not be possible to achieve (Figure 1), especially with lower-yielding genotypes (McGee et al., Reference McGee, Drennan and Caffery2005) and primiparous animals (McGee et al., Reference McGee, Drennan and Caffery2006). Considering the generally higher immunoglobulin concentration in colostrum from beef-suckler cows compared to dairy cows (about 1.5-fold, albeit with large variation; Figure 2), consequently, an equivalent immunoglobulin mass can be achieved with a lower (two-thirds) colostrum volume, for example, 2 rather than 3 l.
From a practical perspective, similarly, our research has shown that feeding the beef-suckler calf 5% of birth weight in colostrum volume using a tube-feeder within 1 h post-calving, with subsequent suckling of the dam (or a second feed) 6 to 8 h later, ensures adequate passive immunity, equivalent to a well-managed suckling situation where the calf suckles ‘naturally’ within 1 h after birth, with unlimited access to the dam subsequently (McGee et al., Reference McGee, Drennan and Caffery2006). Correspondingly, Langholz et al. (Reference Langholz, Schmidt, Derenbach and Kim1987) reported that an increase in serum immunoglobulin concentration in beef-suckler calves was only observed up to a consumption of 2 kg of colostrum at first suckling.
In situations where sufficient or suitable colostrum is unavailable, colostrum supplements (provide exogenous IgG from bovine lacteal secretions or bovine serum) or replacers (in addition to exogenous IgG, also provide nutrients – energy, protein, minerals and vitamins) may be used; however, published data concerning their efficacy is inconsistent (Cabral et al., Reference Cabral, Chapman and Erickson2013).
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.
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).
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).
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.
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.
Conclusion
This review has summarised the published research pertaining to the main factors affecting the passive immune status of beef-suckler calves (illustrated in Figure 3). It is clear that compared to the dairy calf, there is much less research and consequently, much less is known about factors affecting the failure of the neonatal beef calf to absorb adequate colostral immunoglobulins. Deficiencies in the literature are highlighted; in particular, published studies evaluating colostrum yield and ultimately colostrum immunoglobulin mass produced by beef-suckler cows, and correspondingly colostrum consumption by their calves are scant. Accurate and precise measurement of immunoglobulin concentrations in colostrum and blood seems to be a challenge; consequently, interpreting absolute values or cut-offs as a means of identifying the ‘quality’ of colostrum and immune ‘status’ of calves may be hazardous. Evidence is also provided that, commercially at least, the passive immunity of beef calves may not be as high as dairy calves. Further research is needed on colostrum-related factors limiting passive immunity of beef calves, and on the validation of laboratory test cut-off points for determining FPT in beef calves, based on their relationships with key health and performance measures.
Acknowledgements
This research was supported under the DAFM Research Stimulus Fund (11/S/131).
Declaration of interest
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Ethics statement
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Supplementary material
To view supplementary material for this article, please visit https://doi.org/10.1017/S1751731118003026