Effect of passive transfer status on preweaning growth performance in dairy lambs

Genesio Massimini School of Medicine and Surgery, University of Catanzaro Magna Græcia, Viale Europa Campus Universitario di Germaneto, I-88100 Catanzaro, Italy.

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Domenico Britti School of Medicine and Surgery, University of Catanzaro Magna Græcia, Viale Europa Campus Universitario di Germaneto, I-88100 Catanzaro, Italy.

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Angelo Peli Department of Veterinary Clinical Sciences, School of Veterinary Medicine, University of Bologna Alma Mater Studiorum, Via Tolara di Sopra 50, I-40064 Ozzano Emilia, Bologna, Italy.

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Stefano Cinotti Department of Veterinary Clinical Sciences, School of Veterinary Medicine, University of Bologna Alma Mater Studiorum, Via Tolara di Sopra 50, I-40064 Ozzano Emilia, Bologna, Italy.

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Abstract

Objective—To evaluate the effect of passive transfer status, determined by measuring serum IgG concentration 24 hours after parturition, on preweaning growth performance in dairy lambs.

Design—Prospective observational study.

Animals—20 healthy Sardinian dairy lambs.

Procedures—Serum IgG concentration was meaured 24 hours after birth. Body weight was measured at birth and at the time of weaning 28 days (ie, 27 to 29 days) after birth. Mean daily gain from birth to day 28 and day 28 weight were used as measures of preweaning growth performance. Regression analysis was used to evaluate associations between serum IgG concentration 24 hours after birth and measures of preweaning growth performance.

Results—Mean ± SD serum IgG concentration 24 hours after birth was 24.6 ± 17.5 mg/mL. Mean body weights at birth and weaning were 2,696 ± 937 g and 9,253 ± 2,116 g, respectively, and mean daily gain was 234 ± 63 g/d. No significant association was detected between serum IgG concentration 24 hours after birth and birth weight. However, serum IgG concentration 24 hours after birth was significantly associated with mean daily gain (R2 = 0.25). Each 1 mg/mL increase in serum IgG concentration 24 hours after birth was associated with a 1.8 g/d increase in mean daily gain and a 60.8-g increase in day 28 weight.

Conclusions and Clinical Relevance—Results indicated that passive transfer status, determined as serum IgG concentration 24 hours after birth, was a significant source of variation in preweaning growth performance in dairy lambs.

Abstract

Objective—To evaluate the effect of passive transfer status, determined by measuring serum IgG concentration 24 hours after parturition, on preweaning growth performance in dairy lambs.

Design—Prospective observational study.

Animals—20 healthy Sardinian dairy lambs.

Procedures—Serum IgG concentration was meaured 24 hours after birth. Body weight was measured at birth and at the time of weaning 28 days (ie, 27 to 29 days) after birth. Mean daily gain from birth to day 28 and day 28 weight were used as measures of preweaning growth performance. Regression analysis was used to evaluate associations between serum IgG concentration 24 hours after birth and measures of preweaning growth performance.

Results—Mean ± SD serum IgG concentration 24 hours after birth was 24.6 ± 17.5 mg/mL. Mean body weights at birth and weaning were 2,696 ± 937 g and 9,253 ± 2,116 g, respectively, and mean daily gain was 234 ± 63 g/d. No significant association was detected between serum IgG concentration 24 hours after birth and birth weight. However, serum IgG concentration 24 hours after birth was significantly associated with mean daily gain (R2 = 0.25). Each 1 mg/mL increase in serum IgG concentration 24 hours after birth was associated with a 1.8 g/d increase in mean daily gain and a 60.8-g increase in day 28 weight.

Conclusions and Clinical Relevance—Results indicated that passive transfer status, determined as serum IgG concentration 24 hours after birth, was a significant source of variation in preweaning growth performance in dairy lambs.

Lambs depend on the passive transfer of colostral IgG to provide humoral immunity during the neonatal period, and adequate passive transfer of immunity, determined by measuring serum IgG concentration, is a critical determinant of short-term health and survival for neonatal lambs. To ensure adequate passive transfer of immunity, lambs should receive a sufficient volume and concentration of colostrum within the first 12 hours of life.1,2 When ingestion or absorption of colostral IgG is not adequate, FPT is the result. However, FPT of immunity is not a disease itself but, rather, a secondary immunodeficiency condition that predisposes ruminant neonates to the development of disease.3,4 Lambs with FPT have an increased risk of illness and death until at least 2 weeks of age,1,2,5–12 and in neonatal lambs < 2 days old, an increased risk of illness and death is associated with serum IgG concentration < 16 mg/mL (ie, 1,600 mg/dL).5–8,13

Although much has been written on the association between passive transfer of immunity and the risk of illness and death in neonatal lambs, the potential longterm effects of passive transfer status have largely been neglected. Passive transfer of immunity seems to have predictive value for health and productivity outcomes in juvenile calves4 and lambs,1,2 both before and after weaning. Further, it has been reported that a significantly higher percentage of lambs with high postcolostral serum immunoglobulin concentrations survived to 6 months of age, compared with lambs with lower immunoglobulin concentrations.1,2 In addition, lambs that survive despite FPT reportedly grow slowly.1,2 Nevertheless, little is known on the effects of passive transfer status on growth performance in dairy lambs.

Robison et al14 demonstrated that serum IgG concentration 24 to 48 hours after parturition was a significant source of variation in MDG through the first 180 days of life in dairy heifer calves. The effect of passive transfer status on calf growth appeared strongest 70 to 105 days after parturition, which period coincided with the age at weaning. In a subsequent study,15 calf serum IgG concentration 24 to 48 hours after parturition was a significant source of variation in mature milk and fat production, and heifers that survived despite FPT had lower milk production during their first lactation. In similar studies16,17 of the influence of passive transfer status on preand postweaning health and growth performance of crossbreed calves, passive transfer status 24 hours after parturition was found to have an indirect effect on MDG and weaning weight because of the effect of FPT on calf morbidity rate.

To the authors' knowledge, the predictive value of passive transfer status for preweaning growth performance in dairy lambs has not been reported. The purpose of the study reported here, therefore, was to evaluate the potential effect of passive transfer status, determined by measuring serum IgG concentration 24 hours after parturition, on preweaning growth performance in dairy lambs. Measures of growth performance that were evaluated were MDG and body weight 28 days after parturition. It is expected that such information will help producers decide whether it is economically feasible to adjust management procedures to optimize passive transfer in dairy lambs.

Materials and Methods

Animals—Twenty healthy Sardinian lambs from a single dairy farm in central Italy were used in the study. All dams were housed on the farm under standard management procedures for the farm. Other than routine vaccines against clostridial diseases and deworming agents, drugs and other compounds were not administered to the dams during gestation or parturition. Four weeks before the expected lambing date, dams received a 2-mL booster dose of a formalin-inactivated vaccine containing Clostridium chauvoei, Clostridium septicum, Clostridium novyi type B,Clostridium haemolyticum (C novyi type D), Clostridium tetani, and Clostridium perfringens types C (beta) and D (epsilon) bacterin-toxoid with potash alum adjuvant.a Only lambs resulting from observed parturitions were included in the study.

After parturition, all lambs were weighed. Lambs were then allowed to naturally suckle their dams until 24 hours (ie, 23.5 to 24.5 hours) after parturition. No attempt was made to ensure that lambs suckled, and no supplemental colostrum was fed. After this period, lambs were removed from the dams and fed fresh pooled whole milk (obtained from ewes through their first 6 milkings after parturition) twice daily until 1 week of age. Thereafter, lambs were fed milk replacerb (crude protein, 24%; crude fat, 24%; 220 g of powder/L of fresh water) dispensed ad libitum from a custom made lamb-bar. All lambs had ad libitum access to a 19% crude protein lamb commercial starterc beginning at 10 days of life. Lambs were weaned 28 days (ie, 27 to 29 days) after parturition and weighed at the time of weaning. Vaccines, drugs, and other compounds were not administered to lambs during the study.

Only lambs that survived until the time of weaning were included in the study. Thus, 4 additional lambs that were initially enrolled in the study were excluded because they died prior to weaning. One lamb died at 1 week of age and had gross lesions indicative of enteritis and pneumonia. The other 3 lambs died at 2 weeks of age, and death was not attributed to infectious disease.

The 20 lambs included in the study were considered by the producer to be healthy, and no clinical abnormalities were detected during physical examinations. Adequacy of passive transfer, health status, management interventions, and other animal factors (ie, dam age, lamb sex, litter number, duration of gestation, and dam and lamb behaviour) were not considered as independent variables in the study.

Sample collection and processing—Blood samples were collected by means of jugular venipuncture from the lambs 24 hours (ie, 23.5 to 24.5 hours) after parturition. Serum was harvested after centrifugation and stored at 4°C until analyzed. Serum IgG concentration was determined by use of a commercially available radial immunodiffusion assay for sheep IgG,d according to the manufacturer's specifications. Briefly, 5 μL of serum was added to 1 well of a 48-well plate containing anti-sheep IgG antiserum dissolved in 1.5% agarose in tris-buffered saline solution and 0.1% sodium azide. Three reference standards (1.25, 5, and 10 mg/mL) included in the kit were tested concurrently with each sample. The plate was incubated at room temperature (23°C) for 24 hours, and the precipitin ring diameter was measured. The IgG concentration of test samples was determined by comparing precipitin ring diameter for test samples to a semilog plot generated from results for the reference standards. Serum samples with IgG concentration > 10 mg/mL were diluted 1:10 with sodium barbital buffer solutione and reanalyzed. For statistical analyses, all samples having a serum IgG concentration less than the assay's lowest detectable limit of 1.25 mg/mL were designated as having a concentration of 0 mg/mL.

Statistical analysis—Mean ± SD values for serum IgG concentration at 24 hours, birth weight, day 28 weight, and MDG from birth to day 28 were calculated. Least squares simple linear regression18,19 was used to evaluate the association between serum IgG concentration at 24 hours (continuous independent variable) and preweaning growth performance outcomes, including MDG and day 28 weight (continuous dependent variables). Serum IgG concentration at 24 hours and birth weight were also compared by means of simple linear regression analysis. Only variables with nonzero regression coefficients (P < 0.05) were permitted to enter the models. The goodness of fit of the models was established by R2, which was multiplied by 100 and expressed as a percentage to indicate the total variation in growth performance that was accounted for by variation in serum IgG concentration at 24 hours; the remaining percentage indicated the total variation in growth performance that was unexplained by variation in serum IgG concentration at 24 hours (residual variance). The quadratic form of the models was also screened by use of the F test (extra sum-ofsquared); differences between R2 values were tested by calculating F values to determine significance (P < 0.05) of the contribution of the quadratic models, compared with the simple linear models. Calculations were performed with the assistance of a statistical software package.f

Results

For the 20 lambs included in the study, serum IgG concentration 24 hours after birth ranged from 0 to 52.4 mg/mL (mean ± SD, 24.6 ± 17.5 mg/mL). Only 1 lamb had a serum IgG concentration lower than the detectable limit of 1.25 mg/mL. Birth weight ranged from 1,600 to 4,400 g (mean ± SD, 2,696 ± 937 g). Body weight 28 days after birth ranged from 5,200 to 12,500 g (mean ± SD, 9,253 ± 2,116 g). The MDG ranged from 125 to 323 g/d (mean ± SD, 234 ± 63 g/d).

No significant association was detected between serum IgG concentration 24 hours after birth and birth weight. Serum IgG concentration 24 hours after birth was significantly (P < 0.05) associated with MDG (R2 = 0.26) and day 28 weight (R2 = 0.25; Figure 1). Each 1 mg/mL increase in serum IgG concentration 24 hours after birth was associated with a 1.8 g/d increase in MDG and a 60.8-g increase in day 28 weight. The quadratic models were screened and rejected because these models did not result in R2 values significantly different from values obtained with the simple linear models.

Figure 1—
Figure 1—

Scatterplots of serum IgG concentration 24 hours after parturition in 20 healthy Sardinian dairy lambs versus MDG from birth to day 28 (A) and body weight at day 28 (B). In each graph, the solid line represents the best fit for the data, as determined by means of simple linear regression. Regression equations were as follows: MDG (g/d) = 189.1 + (1.81 × serum IgG concentration at 24 hours [mg/mL]); and day 28 weight (g) = 7,739 + (60.84 × serum IgG concentration at 24 hours [mg/mL]).

Citation: Journal of the American Veterinary Medical Association 229, 1; 10.2460/javma.229.1.111

For the 4 dead lambs, serum IgG concentration 24 hours after birth ranged from 0 to 50.2 mg/mL. The lamb that died at 1 week of age had a serum IgG concentration less than the detectable limit of 1.25 mg/mL. For the others 3 lambs, serum IgG concentrations 24 hours after birth were 50.2, 39.2, and 0 mg/mL.

Discussion

Results of the present study indicate that passive transfer status, determined as serum IgG concentration 24 hours after birth, was a significant source of variation in preweaning growth performance in dairy lambs. This is similar to results of other studies14,20 involving dairy and beef calves. Linear regression analysis revealed significant positive correlations between serum IgG concentration 24 hours after parturition and MDG and between serum IgG concentration 24 hours after parturition and body weight 28 days after birth in the present study. Coefficients of determination indicated that the variation attributable to serum IgG concentration 24 hours after parturition accounted on average for 26% and 25%, respectively, of the total variation in MDG and day 28 weight. These findings suggest improving passive transfer status in neonatal lambs within the first 24 hours after parturition may enhance their growth rate during the first month after birth. Proper neonatal management programs that enhance the likelihood that lambs receive a sufficient volume and concentration of colostrum within the first hours of life should be developed and used to meet this need.

In the present study, we did not detect a significant relationship between birth weight and serum IgG concentration 24 hours after birth; however, the reason for this was not apparent. Although male lambs may have higher serum IgG concentration than females, particularly with multiple litters,1,2 the influence of birth weight on passive transfer of IgG in neonatal ruminants has not yet been fully elucidated. In a study14 of 1,000 dairy heifer calves, Robison et al did not detect a significant relationship between birth weight and serum IgG concentration 24 hours after parturition. Conversely, a negative relationship between birth weight and immunoglobulin transfer in neonatal lambs has been reported.21,22 However, negative relationships between birth weight and duration of gestation and between birth weight and plasma thyroxine concentration have also been reported for lambs.22 Consequently, it appears that the negative relationship between birth weight and acquisition of passive immunity in newborn lambs could be an indirect link that reflects the effects of other important physiologic factors, such as duration of gestation and hormonal status at birth. However, the potential influences of these independent variables were not evaluated in the present study.

It is impossible to ascertain from the present study whether serum IgG concentration 24 hours after parturition was directly or indirectly related to growth through the first 28 days of life. A biological basis for this relationship was not apparent from our data; however, we have a few theories for this observation. First, the relationship between serum IgG concentration 24 hours after parturition and growth performance may be a direct cause-and-effect relationship. Thus, lambs with adequate passive transfer of antibodies against pathogens may develop more efficient metabolic systems that contribute to growth. In a study23 comparing vaccination schedules for ewes and the ability of their lambs to raise antibody concentrations against epsilontoxin of C perfringens, lambs from ewes vaccinated 3 weeks before parturition had higher titers of antibodies at birth than lambs from unvaccinated ewes. This suggests that vaccinating ewes before parturition might improve lamb growth by enhancing passive transfer of antibodies against specific pathogens. Second, lambs that receive and absorb colostral IgG at birth may also receive other nonimmunoglobulin factors in the colostrum that influence the growth. Colostrum is rich in antibodies, lymphocytes, cytokines, acute-phase proteins, hormones (growth factors), vitamins, minerals, and enzymes.24–27 The central role of cytokines in the immune regulation of the mammary gland is well accepted for ruminants.26,28 Colostral cytokines, along with other immune regulatory proteins such as complement and lactoferrin, are also believed to play an important role in the innate immunity of ruminant neonates.24–26,29 Considerable research effort has been directed in recent years at determining the relationships between development of neonatal calves and various growth factors, such as insulin-like growth factor-I and growth hormone.30,31 Many of these nonimmunoglobulin factors in colostrum might have interacted in conjunction with IgG concentration or acted directly to influence the growth response or to advance the immune and metabolic systems of the lambs. However, studies must be performed before definitive statements regarding passive transfer of cytokines and other immune regulatory proteins in neonatal lambs can be made. Critical studies in this area will likely involve comparing colostral and serum cytokine and hormone profiles with preand postweaning health and growth performance.

In the present study, a large proportion of the variation in MDG and day 28 weight (approx 75%) was unexplained by the variation in serum IgG concentration 24 hours after parturition and was attributable to some other factor. Clearly, there are many variance components for lamb growth through weaning32,33 that might explain the residual variance in MDG and day 28 weight. These include, but are not limited to, health status, management interventions, nutrition, environment, and other animal factors, such as dam age, lamb sex, litter number, behavior, absorptive ability, and inherent differences among individuals. We were able to remove health status as a potential source of variation in lamb growth, as all lambs in our study were apparently healthy. The proportion of variation attributable to farm management procedures was minimized because all lambs were from a single dairy farm. The weaning system used in the present study is a common management tool for dairy sheep farms, and lamb growth at 30 days with this system is reportedly not significantly different from lamb growth reported for mixed (lambs left with the dam during the day and separated during the evening) and traditional (lambs allowed to suckle the dam until approx 30 days of life) weaning systems.34 Consequently, dam and lamb factors likely accounted for the bulk of the residual variance observed in the present study.

Models created in the present study did not include adequacy or inadequacy of passive transfer (ie, a binary categorical independent variable) as a covariate because there is no serum IgG concentration that is universally accepted by the veterinary community as the cutoff below which FPT occurs in lambs. Thus, serum IgG concentration was incorporated in the models only as a continuous independent variable. However, serum IgG concentrations in this sample population covered a wide range.

Overall, results of our study suggest that passive transfer status is a significant source of variation for preweaning growth performance in dairy lambs. Optimizing passive transfer may improve lamb growth from birth to 28 days of age, and this effect may affect future management decisions. Passive transfer monitoring programs can identify lambs suffering from FPT, but because the causes of FPT are multifactorial (eg, inadequate concentration of IgG in colostrum fed, inadequate volume of colostrum ingested, retarded age of the lamb at first colostral feeding, and failure of the neonate to suckle or absorb ingested colostrum),1–5 programs designed simply to identify affected lambs will not replace comprehensive flock management programs. Colostrum and immunization management strategies should, therefore, receive appropriate attention by producers and veterinarians attempting to optimize passive transfer status and improve growth performance of dairy lambs raised in a production environment.

ABBREVIATIONS

FPT

Failure of passive transfer

MDG

Mean daily gain

a.

Covexin 8 vaccine, Schering-Plough Animal Health Co, Omaha, Neb.

b.

Volac Lamlac ewe milk replacer, Volac International Ltd, Orwell, Royston, Herts, UK.

c.

Petrini OC3 for weaning lambs, Petrini 1822 Co, Bastia Umbra, Perugia, Italy.

d.

Sheep IgG VET-RID kit, Bethyl Laboratories Inc, Montgomery, Tex.

e.

Barbital buffer, Sigma Chemical Co, St Louis, Mo.

f.

GraphPad Prism, version 4.01 for Windows, GraphPad Software Inc, San Diego, Calif.

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