Introduction
⌅Feeding practices during the neonatal period significantly impact the success of dairy calf rearing (Godden et al., 2019Godden SM, Lombard JE, Woolums AR, 2019. Colostrum management for dairy calves. Vet Clin North Am Food Anim Pract35: 535-556. 10.1016/j.cvfa.2019.07.005). Monitoring the quantity of colostral immunoglobulin absorbed following feeding of colostrum by neonatal calves is essential for enhancing the performance and health of preweaning dairy calves (Lopez & Heinrichs, 2022Lopez AJ, Heinrichs AJ, 2022. Invited review: The importance of colostrum in the newborn dairy calf. J Dairy Sci105, 2733-2749. 10.3168/jds.2020-20114), survival of preweaning calves (Urie et al., 2018Urie NJ, Lombard JE, Shivley CB, Kopral CA, Adams AE, Earleywine TJ, Olson JD, Garry FB, 2018. Preweaned heifer management on US dairy operations: Part V Factors associated with morbidity and mortality in preweaned dairy heifer calves. J Dairy Sci101: 9229-9244. 10.3168/jds.2017-14019) and better performance in later life (Abuelo et al., 2021Abuelo A, Cullens F, Brester JL, 2021. Effect of preweaning disease on the reproductive performance and first-lactation milk production of heifers in a large dairy herd. J Dairy Sci104: 7008-7017. 10.3168/jds.2020-19791). An adequate and immediate (within 2 to 3 hafter birth) colostrum supply is vital for establishing passive immunity in calves, and the amount of colostrum fed to newborn calves directly correlates with preventing illness and calf losses (Godden, 2019Godden SM, Lombard JE, Woolums AR, 2019. Colostrum management for dairy calves. Vet Clin North Am Food Anim Pract35: 535-556. 10.1016/j.cvfa.2019.07.005). Given that colostrum collection and storage practices influence the calf’s metabolism, endocrine system, and nutrition (Liermann et al., 2020Liermann W, Schäff CT, Gruse J, Derno M, Weitzel JM, Kanitz E, Otten W, Hoeflich A, Stefaniak, T, Sauerwein H, Bruckmaier RM, Gross JJ, Hammon HM, 2020. Effects of colostrum instead of formula feeding for the first 2 days postnatum on whole-body energy metabolism and its endocrine control in neonatal calves. J Dairy Sci103: 3577-3598. 10.3168/jds.2019-17708), it is vital to monitor the quantity, quality, and cleanliness of colostrum and to ensure that newborn calves receive colostrum on time (Fischer et al., 2019Fischer AJ, Villot C, Van Niekerk JK, Yohe TT, Renaud DL, Steele MA, 2019. Invited Review: Nutritional regulation of gut function in dairy calves: From colostrum to weaning. Appl Anim Sci355: 498-510. 10.15232/aas.2019-01887).
Because calf diarrhea is one of the most severe problems in dairy farming and a significant cause of economic losses in dairy operations due to high morbidity and mortality rates, high treatment costs, and low growth rate (Elsohaby et al., 2019Elsohaby I, Cameron M, Elmoslemany A, McClure JT, Keefe G, 2019. Effect of passive transfer of immunity on growth performance of preweaned dairy calves. Can J Vet Res83: 90-96.), the management of colostrum feeding is of particular importance for avoiding this disease (Carter et al., 2021Carter HSM, Renaud DL, Steele MA, Fischer-Tlustos AJ, Costa JHC, 2021. A narrative review on the unexplored potential of colostrum as a preventative treatment and therapy for diarrhea in neonatal dairy calves. Animals118: 2221. 10.3390/ani11082221). Likewise, respiratory tract infections resulting in pneumonia are a leading health concern in dairy calves worldwide because this disease has significant consequences for animal welfare, production, antimicrobial use (Jourquin et al., 2023Jourquin S, Lowie T, Debruyne F, Chantillon L, Vereecke N, Boyen F, Boone R, Bokma J, Pardon B, 2023. Dynamics of subclinical pneumonia in male dairy calves in relation to antimicrobial therapy and production outcomes. J Dairy Sci106: 676-689. 10.3168/jds.2022-22212), and lower preweaning weight gain (Cramer & Ollivett, 2019Cramer MC, Ollivett TL, 2019. Growth of preweaned, group-housed dairy calves diagnosed with respiratory disease using clinical respiratory scoring and thoracic ultrasound-A cohort study. J Dairy Sci102: 4322-4331. 10.3168/jds.2018-15420). The appropriate colostral feeding provides better growth and lower occurrence of pneumonia in neonatal calves (Zakian et al., 2023Zakian A, Rasooli A, Nouri M, Ghorbanpour M, Khosravi M, Constable P, Moazeni M, 2023. Effect of heating bovine colostrum at 60°C for 90′ on colostrum quality and the health and growth characteristics of Holstein dairy calves. Aust Vet J101: 175-186. 10.1111/avj.13231).
Neonatal calves suffering failed transfer of passive immunity (FPI) are more prone to enteric diseases caused by infectious pathogens and pneumonia (Lora et al., 2018Lora I, Gottardo F, Contiero B, Dall Ava B, Bonfanti L, Stefani A, Barberio A, 2018. Association between passive immunity and health status of dairy calves under 30 days of age. Prev Vet Med152: 12-15. 10.1016/j.prevetmed.2018.01.009). Thus, achieving an optimal transfer of passive immunity in newborn dairy calves is a crucial management goal in dairy farms. Mortality rate is an important indicator of animal welfare and the productivity of a dairy farm (Dawkins, 2017Dawkins MS, 2017. Animal welfare and efficient farming: Is conflict inevitable?Anim Prod Sci57(2): 201-208. 10.1071/AN15383).
Economic losses associated with high mortality include costs incurred by treating and controlling diseases before death, acquiring replacement heifers, and deferred economic loss due to potential genetic loss (Wathes et al., 2008Wathes DC, Brickell JS, Bourne NE, Swali A, Cheng Z, 2008. Factors influencing heifer survival and fertility on commercial dairy farms. Animal2: 1135-1143. 10.1017/S1751731108002322). Additionally, purchasing replacement heifers increases the risk of transmitting diseases in the herd (Torsein et al., 2011Torsein M, Lindberg A, Sandgren CH, Waller KP, Törnquist M, Svensson C, 2011. Risk factors for calf mortality in large Swedish dairy herds. Prev Vet Med99: 136-147. 10.1016/j.prevetmed.2010.12.001). Published data regarding the effect of serum immunoglobulin concentration in neonatal calves on health and mortality are scarce; some have been carried out in beef calves or conducted with limited observations, and some results from earlier studies have been contradictory. These previous findings complicate an accurate estimation of the impact of serum immunoglobulins on preweaning health in dairy calves. Therefore, we hypothesized that the traditional serum immunoglobulins G (IgG) concentration ≥10 g/L, indicative of adequate transfer of passive immunity of colostral immunoglobulins in dairy calves, reduces diarrhea and pneumonia and decreases preweaning mortality of Holstein calves in a high-input dairy operation. This study aimed to determine the effect of serum IgG concentration 24 h postpartum (estimated from serum %Brix) on the occurrence of diarrhea and pneumonia and the mortality of intensively raised Holstein calves.
Materials and Methods
⌅Animals and management
⌅This project was approved by the Autonomous Agrarian University Antonio Narro Animal Care and Use Committee (#03001-2243). The study was performed on a single large (~3500 milking cows) commercial dairy herd in northeastern Mexico (25°N, elevation 1155 m, mean annual rainfall 228 mm, mean annual temperature 23.8°C) from September 2021 to May 2023. A total of 4,349 female Holstein calves were enrolled in the study.
The farm had a calf-rearing facility with individual outdoor 2.4 m × 1.2 m portable pens with tube sides and plywood roofs with a covered area of 1.6 m2. Pens were clean and dry with no bedding (loose-packed soil) and good drainage. Each pen had two feeding pails with holders. Pens were about 0.5 m apart, which minimized microbial loads in the calf ambient. Disinfection of the pens using a high-pressure cleaner and disinfecting afterward was part of the farm routine in the present study. Immediately after birth, calves were separated from their dams, navel-dipped, weighed on a weighing digital scale (Coburn Company, Whitewater, Wisconsin, USA), and raised outdoors in all seasons. Calves were identified using traditional plastic ear tags. Two liters of high-quality colostrum (at least 50 mg/mL of IgG, based on specific gravity reading; JorVet Bovine Colostrometer, Jorgensen Laboratories, Loveland, CO) from freshly calved cows was fed to calves within one hour of birth. Two more liters were given within the next 8 hours of birth. Colostrum was given to all calves by staff members at the dairy herd via esophageal feeders (Nasco, Fort Atkinson, WI).
Calves were offered a milk replacer (MR; 28% crude protein and 20% fat, 4.87 megacalories of metabolizable energy/kg), mastitic milk, and antibiotic milk. MR was reconstituted to 14% solids with warm water and was offered at 0700 and 1430 h daily. The starter grain was a commercial starter containing 23% crude protein and 1.84 megacalories/kg and was offered free choice starting at day 4 of life. Water was offered free choice.
Calf health recordings
⌅Employees registered gender and birth weight. Preweaning average daily gain was calculated from birth and weaning weights (63.1 ± 1.9 days). After birth, the herd veterinarian in charge of calf-raising operations inspects the calves daily and records the occurrence of diarrhea, pneumonia, and calf mortality. Calf diarrhea was defined as loose feces that persisted for two or more days, accompanied by a decreased appetite, lethargy, dehydration (sunken eyes), and fever. Calf pneumonia was diagnosed when the following signs were observed: elevated respiratory rate, serous nasal discharge, coughing, fever, mild depression, and inappetence.
The herd veterinarians treated calves suffering from diarrhea or pneumonia following the standard procedures for these diseases. For pneumonia, treatment was initiated on recognition of inappetence, depression with undifferentiated fever (rectal temperature ≥ 39.4), ear droop, dry cough, and slightly increased respiratory rate. Treatment was based on tulatromycin, bromhexine, and metamizole sodium. Diarrhea was treated when feces were detected on the calf´s tail, decreased appetite, lethargy, dehydration, and fever. Treatment was based on marbofloxacin/gentamicin and oral electrolyte solutions. Mortality rate was defined as the number of events during the observation period/total calf days at risk (60). For calves that died, the cause of death was determined according to clinical signs of disease before demise. Calves that died before weaning were censored on the day of death.
Assessment of passive immunity
⌅The herd veterinarians collected blood samples (6 mL) 24 h post-calving for serum %Brix determination (serum IgG estimation). Blood samples were collected via jugular venipuncture using a 20-gauge, 1-inch hypodermic needle (BD Vacutainer Precision Glide, Becton Dickinson Co., Franklin Lakes, NJ) into a 10-mL Vacutainer® tube (no anticoagulant; Becton Dickinson, Franklin Lakes, NJ, USA). Blood was allowed to clot at room temperature for approximately one hour and centrifuged at 2,000 × g for 10 min, and sera was separated within 24 h of collection. Subsequently, the serum was harvested and assayed for %Brix using a digital Brix refractometer (PA202X-003-105, Misco, Cleveland, OH). Calves were categorized as having (serum Brix% < 8) or not having failure of passive immunity (FPI; serum Brix% ≥ 8; equivalent to 10.1 g/L serum IgG, the cut-off point for an FPI positive case, according to equations described by previous studies (Morril et al., 2013Morrill KM, Polo J, Lago A, Campbell J, Quigley J, Tyler H, 2013. Estimate of serum immunoglobulin G concentration using refractometry with or without caprylic acid fractionation. J Dairy Sci96: 4535-4541. 10.3168/jds.2012-5843; Deelen et al., 2014Deelen SM, Ollivett TL, Haines DM, Leslie KE, 2014. Evaluation of a Brix refractometer to estimate serum immunoglobulin G concentration in neonatal dairy calves. J Dairy Sci97: 3838-3844. 10.3168/jds.2014-7939; Elsohaby et al., 2015Elsohaby I, McClure JT, Keefe GP, 2015. Evaluation of digital and optical refractometers for assessing failure of transfer of passive immunity in dairy calves. J Vet Int Med29: 721-726. 10.1111/jvim.12560) and as having (Brix% ≤ 6.5; equivalent to 0 g/L serum IgG) or not having (Brix% > 6.5) agammaglobulinemia. In the present study, we defined successful passive transfer of antibodies in neonatal calves presenting serum Brix% ≥ 8. However, a detailed updated analysis by Buczinski et al. (2021Buczinski S, Lu Y, Chigerwe M, Fecteau G, Dendukuri N, 2021. Systematic review and meta-analysis of refractometry for diagnosis of inadequate transfer of passive immunity in dairy calves: Quantifying how accuracy varies with threshold using a Bayesian approach. Prev Vet Med189: 105306. 10.1016/j.prevetmed.2021.105306) shows that the Brix refractometry value for diagnosing adequate transfer of passive immunity in calves is ≥ 8.4. Lombard et al. (2020Lombard J, Uri N, Garry F, Godden S, Quigley J, Earleywine T, McGuirk S, Moore D, Branan M, Chamorro M, Smith G, Shivley C, Catherman D, Haines D, Heinrichs AJ., James R, Maas J, Sterner K, 2020. Consensus recommendations on calf- and herd-level passive immunity in dairy calves in the United States. J Dairy Sci103(8): 7611-7624. 10.3168/jds.2019-17955) indicate that the consensus target Brix measurement for sufficient transfer of passive immunity in calves in the United States is 8.1. To facilitate comparison across previous studies, we defined an adequate TPI status in calves with serum Brix% ≥ 8 because this value is the traditional dairy industry benchmark used in most previously published studies.
Statistical analyses
⌅Multivariable logistic regression models were employed to assess the effect of attainment of a BRIX refractometer reading ≥ 8 (serum IgG ≥ 10.1 g/L) 24 h after birth and the occurrence of agammaglobulinemia 24 h after birth on the incidence of preweaning diarrhea and pneumonia, as well as mortality of calves (response variables), using the maximum likelihood method of the LOGISTIC procedure of SAS (SAS Institute Inc., Cary, NC; version 9.4). The general equation of the logistic regression model was defined as follows:
Where π was the probability of diarrhea, pneumonia, and death; α was the intercept parameter; β1 to βn were the logistic regression coefficients (parameter estimates) for the explanatory effects (X1 to Xn) included in the statistical model. No elimination method was used to remove variables from the model because a standard view in epidemiology is that automated confounder selection methods, such as backward elimination, should be avoided as they can lead to biased effect estimates and underestimating their variance. The strength of the associations was estimated using adjusted odds ratios and the 95% confidence interval (95% CI).
Each multivariable model included potential confounders such as birth weight, season of birth, year of birth, dam parity, and gender. Birth weight was categorized as lower or greater than 37 kg. Parity was grouped into three categories: 1, 2-3, and >3. December, January, and February were grouped as winter; March, April, and May as spring; June, July, and August as summer; and September, October, and November as autumn. The Hosmer and Lemeshow chi-squared goodness-of-fit test was used to assess the whole fitness of the logistic regression model. A histogram for serum IgG based on BRIX refractometer reading was prepared with the Statgraphics Centurion XV software (Statpoint Technologies Inc., Warrenton, VA, USA). For the time of disease (pneumonia or diarrhea) occurrence postpartum, survival analyses were performed for calves with FPI or not FPI, using the Cox proportional hazard model (Statgraphics Centurion XV software). Interval from birth to disease occurrence was the dependent variable. Survival curves were generated at an exit time point of 60 days (weaning). For all the analyses, the significance was established at p<0.05.
Results
⌅Of the 4,349 calves born alive and included in the study, 22.8% had diarrhea (n = 991), and 15.0% had pneumonia (n = 653) in the preweaning period. The mean age of calves with diarrhea was 10.5 ± 6.6 d, while for calves with pneumonia, it was 39.1 ± 16.4 d. The overall calf mortality was 4.9 per 100-calf 60-days at risk. The majority of deaths occurred in calves less than 55 days of age, with an average age of 27 days. Serum IgG (estimated from equations of Morrill et al., 2013Morrill KM, Polo J, Lago A, Campbell J, Quigley J, Tyler H, 2013. Estimate of serum immunoglobulin G concentration using refractometry with or without caprylic acid fractionation. J Dairy Sci96: 4535-4541. 10.3168/jds.2012-5843; Deelen et al., 2014Deelen SM, Ollivett TL, Haines DM, Leslie KE, 2014. Evaluation of a Brix refractometer to estimate serum immunoglobulin G concentration in neonatal dairy calves. J Dairy Sci97: 3838-3844. 10.3168/jds.2014-7939; and Elsohaby et al., 2015Elsohaby I, McClure JT, Keefe GP, 2015. Evaluation of digital and optical refractometers for assessing failure of transfer of passive immunity in dairy calves. J Vet Int Med29: 721-726. 10.1111/jvim.12560) in calves 24 h postpartum ranged from 0.0 to 44.4 g/L. Calves with reduced absorption of maternal immunoglobulins (hypogammaglobulinemia; <10 g/L IgG) was 19.0%, whereas the percentage of calves with agammaglobulinemia (AG) 24 h after birth was 7.4%. The histogram describing the frequency of serum IgG concentrations in calves exhibited a positively skewed distribution with a mean (± SD) of 15.4 ± 8.5 (Fig. 1), which indicated that most IgG concentrations felt into the fair to excellent range (Lombard et al., 2020Lombard J, Uri N, Garry F, Godden S, Quigley J, Earleywine T, McGuirk S, Moore D, Branan M, Chamorro M, Smith G, Shivley C, Catherman D, Haines D, Heinrichs AJ., James R, Maas J, Sterner K, 2020. Consensus recommendations on calf- and herd-level passive immunity in dairy calves in the United States. J Dairy Sci103(8): 7611-7624. 10.3168/jds.2019-17955).
Calves that did not attain adequate serum IgG levels (≤ 10 g/L) had higher odds for diarrhea during the preweaning period than calves with FPI (Table 1). AG calves 24 h post-calving had higher odds for diarrhea than calves with no AG. Calves with FPI were more likely to suffer pneumonia than calves with adequate serum IgG concentration 24 h postpartum (Table 2). Compared to all calves not having AG, AG calves 24 h post-calving were 2.1 times more likely to have pneumonia.
| Variables | Prevalence, percentage | Odds ratio (OR)1 | 95% CI (OR) | p | |
|---|---|---|---|---|---|
| Serum IgG ≤ 10 mg/mL | 275/1010 (27.2) | 1.8 | 1.5-2.2 | <0.0001 | |
| Serum IgG > 10 mg/mL | 716/3339 (21.4) | ||||
| Agammaglobulinemia | 110/372 (29.6) | 1.9 | 1.4-2.5 | <0.0001 | |
| No agammaglobulinemia | 881/3977 (22.2) | ||||
| Variables | Prevalence, percentage | Odds ratio (OR)1 | 95% CI (OR) | p |
|---|---|---|---|---|
| Serum IgG ≤ 10 mg/mL | 169/1010 (16.3) | 1.4 | 1.1-1.7 | 0.0083 |
| Serum IgG > 10 mg/mL | 484/3339 (14.5) | |||
| Agammaglobulinemia | 85/372 (22.9) | 2.1 | 1.5-2.9 | <0.0001 |
| No agammaglobulinemia | 568/3977 (14.3) | |||
| Occurrence of diarrhea | ||||
| Yes | 397/991 (40.1) | 3.8 | 3.1-4.8 | <0.0001 |
| No | 256/3358 (7.6) |
Compared to calves with adequate serum IgG 24 h post-calving, calves with FPI were 1.9 times more likely to die before weaning (Table 3). Calves with AG 24 h post-calving had twice the risk of dying than those with no AG. The occurrence of diarrhea greatly affected the mortality rate of calves; likewise, the absence of pneumonia had a protective effect on mortality rate of calves. The odds of mortality were 2.3 times higher in calves with comorbidity of diarrhea and pneumonia compared with calves without these diseases (Table 3).
| Variables | Prevalence, percentage | Odds ratio (OR)1 | 95% CI (OR) | p |
|---|---|---|---|---|
| Serum IgG ≤ 10 mg/mL | 76/1010 (7.5) | 1.9 | 1.4-2.7 | 0.0002 |
| Serum IgG > 10 mg/mL | 137/3339 (4.1) | |||
| Agammaglobulinemia | 44/372 (11.9) | 2.6 | 1.6-4.0 | <0.0001 |
| No agammaglobulinemia | 169/3977 (4.3) | |||
| Preweaning mortality with occurrence of diarrhea | ||||
| Yes | 120/991 (12.1) | 2.4 | 1.7-3.4 | <0.0001 |
| No | 93/3358 (2.8) | |||
| Preweaning mortality with occurrence of pneumonia | ||||
| No | 119/3696 (3.2) | 0.4 | 0.4-0.5 | <0.0001 |
| Yes | 94/653 (14.4) | |||
| Preweaning comorbidity pneumonia and diarrhea | ||||
| Yes | 65/414 (15.7) | 2.3 | 1.6-3.6 | <0.0001 |
| No | 148/3935 (3.8) |
Kaplan-Meier survival curves for calves suffering diarrhea or pneumonia at 60 exit points by serum IgG concentration at 24 h of life are represented in Fig. 2 and Fig. 3, respectively. The survival curve for diarrhea illustrates that most reported clinical signs occurred at around 10 days postpartum and then tapered off for the rest of the preweaning period. In the case of the survival curve for pneumonia, most of the cases occurred at around 30 days with no tapering off for the rest of the preweaning period and with a clear difference for calves with FPI and adequate serum IgG in one-day-old calves.
Discussion
⌅Comparisons of the prevalence of FPI among studies in dairy calves are complicated due to variations in weather conditions, differences in rearing management, colostrum administration, and serum total proteins or IgG concentration used as the threshold for distinguishing calves with and without FPI. Even so, similar to previous studies (Staněk et al., 2019Staněk S, Nejedlá E, Fleischer P, Pechová A, Šlosárková S, 2019. Prevalence of failure of passive transfer of immunity in dairy calves in the Czech Republic. Acta Univ Agric Silvicult Mendel Brun67: 163-172. 10.11118/actaun201967010163), this study shows that the transfer of passive maternal immunity in intensively raised calves is a significant problem.
Similar to findings of Al-Alo et al. (2018Al-Alo KZK, Nikbakht Brujeni G, Lotfollahzadeh S, Moosakhani F, Gharabaghi A, 2018. Correlation between neonatal calf diarrhea and the level of maternally derived antibodies. Iranian J Vet Res19: 3-8.), where newborn calves with higher serum IgG levels had a reduced risk for diarrhea compared with calves with lower serum IgG, in the present study, calves with FPI or GA had a higher risk for the occurrence of this enteric disease. However, other studies have not found an association between passive immunity status and diarrhea (Raboisson et al., 2016Raboisson D, Trillat P, Cahuzac C, 2016. Failure of passive immune transfer in calves: A meta-analysis on the consequences and assessment of the economic impact. PLOS ONE113: e0150452. 10.1371/journal.pone.0150452; Schinwald et al., 2022Schinwald M, Creutzinger K, Keunen A, Winder CB, Haley D, Renaud DL, 2022. Predictors of diarrhea, mortality, and weight gain in male dairy calves. J Dairy Sci105: 5296-5309. 10.3168/jds.2021-21667). This discrepancy may arise from different methodologies to measure IgG, dissimilar populations, or environmental variations among studies.
Failed transfer of passive immunity seems responsible for a higher incidence of enteric diseases, increased use of antibiotics in calves, and, consequently, longer rearing periods, constituting a public health, economic, and animal welfare issue. Calves with passive immunity mount a protective immune response against pathogenic agents causing diarrhea in neonatal calves (Ridpath et al., 2003Ridpath JF, Neill JD, Endsley J, Roth JA, 2003. Effect of passive immunity on the development of a protective immune response against bovine viral diarrhea virus in calves. Am J Vet Res64(1): 65-69. 10.2460/ajvr.2003.64.65). Thus, these results reaffirm that to protect calves against enteric pathogens, newborn animals should absorb adequate amounts of immunoglobulins from colostrum (Gulliksen et al., 2009Gulliksen SM, Jor E, Lie KI, Hamnes IS, Løken T, Åkerstedt J, Østerås O, 2009. Enteropathogens and risk factors for diarrhea in Norwegian dairy calves, J Dairy Sci92: 5057-5066, 10.3168/jds.2009-2080).
Calves in the present study did not have an etiological work-up. At least ten primary enteric pathogens are involved in calf diarrhea (Cho & Yoon, 2014Cho Y, Yoon KJ, 2014. An overview of calf diarrhea-Infectious etiology, diagnosis, and intervention. J Vet Sci15: 1-17. 10.4142/jvs.2014.15.1.1). The only infectious agent previously identified in the studied site is Cryptosporidium parvum (Delgado-González et al., 2019Delgado-González RA, Meza-Herrera CA, González-Álvarez VH, Alvarado-Espino AS, Contreras-Villareal V, Gaytán-Alemán LR, Arellano-Rodríguez G, Véliz-Deras FG, 2019. Enteropathogens in Holstein calves with diarrhea during the first five weeks of age in Mexico. Indian J Anim Res53: 1085-1089. 10.18805/ijar.B-875). A negative correlation has been shown between the passive transfer of anti-C. parvum IgG antibody via colostrum during the first 24 h of life and the detection of cryptosporidiosis early in life in calves (Wang et al., 2003Wang HF, Swain JB, Besser TE, Jasmer D, Wyatt CR, 2003. Detection of antibodies to a recombinant Cryptosporidium parvum p23 in serum and feces from neonatal calves. J Parasitol89: 918-924. 10.1645/GE-3160; Lefkaditis et al., 2020Lefkaditis M, Mpairamoglou R, Sossidou A, Spanoudis K, Tsakiroglou M, Györke A, 2020. Importance of colostrum IgG antibodies level for prevention of infection with Cryptosporidium parvum in neonatal dairy calves. Prev Vet Med176: 104904. 10.1016/j.prevetmed.2020.104904). However, in the present study, other pathogens implicated in calf diarrhea and the sources of infections are unknown. These findings suggest that colostral antibodies partially protect newborn calves during their first day of life and highlight the importance of colostrum absorption in preventing neonatal diarrhea.
One of the main focuses of this study was to examine the association between post-colostral serum IgG levels of calves and preweaning pneumonia. In this study, inadequate serum IgG levels in calves increased the risk for clinician-diagnosed pneumonia, which is in line with previous studies where high blood levels of colostrum-derived IgG in calves are associated with reduced risks of this disease in dairy calves (Virtala et al., 1999Virtala AMK, Gröhn YT, Mechor GD, Erb HN, 1999. The effect of maternally derived immunoglobulin G on the risk of respiratory disease in heifers during the first 3 months of life. Prev Vet Med39: 25-37. 10.1016/S0167-5877(98)00140-8; Sutter et al., 2023Sutter F, Venjakob PL, Heuwieser W, Borchardt S, 2023. Association between transfer of passive immunity, health, and performance of female dairy calves from birth to weaning. J Dairy Sci106(10): 7043-7055. 10.3168/jds.2022-22448). However, other studies found a lack of association between serum IgG and the occurrence of pneumonia in dairy (Pithua and Aly, 2013Pithua P, Aly SS, 2013. A cohort study of the association between serum immunoglobulin G concentration and preweaning health, growth, and survival in Holstein calves. Int J Appl Res Vet Med11, 77-84.) and beef (Waldner & Rosengren, 2009Waldner CL, Rosengren LB, 2009. Factors associated with serum immunoglobulin levels in beef calves from Alberta and Saskatchewan and association between passive transfer and health outcomes. Can Vet J50: 275-281.) calves. This discrepancy could be due to various factors such as the quality of records kept by producers, stress, hygiene management, colostrum quality, quantity, and feeding time. IgG is effective in defense of the bovine respiratory tract against pathogenic microorganisms by opsonizing for enhanced recognition by macrophages and neutrophils, activating complement, blocking colonization sites, and neutralizing bacterial toxins (Caswell, 2014Caswell JL, 2014. Failure of respiratory defenses in the pathogenesis of bacterial pneumonia of cattle. Vet Pathol512: 393-409. 10.1177/0300985813502821). Thus, detecting hypogammaglobulinemia in 24-hour-old calves could hint at developing better management practices to diminish pneumonia in pre-weaned dairy calves.
In the present study, calves that survived diarrhea during the preweaning period were more susceptible to pneumonia before weaning, which agrees with previous reports that demonstrated the importance of diarrhea as a risk factor for the occurrence of pneumonia (Virtala et al., 1999Virtala AMK, Gröhn YT, Mechor GD, Erb HN, 1999. The effect of maternally derived immunoglobulin G on the risk of respiratory disease in heifers during the first 3 months of life. Prev Vet Med39: 25-37. 10.1016/S0167-5877(98)00140-8; Taylor et al., 2010Taylor JD, Fulton RW, Lehenbauer TW, Step DL, Confer AW, 2010. The epidemiology of bovine respiratory disease: what is the evidence for preventive measures?Can Vet J51: 1351-1359.; Gomes et al., 2021Gomes V, Pinheiro FA, Silva KN, Bosco KA, Morita LM, Minervino AHH, Madureira KM, 2021. Morbidity and mortality in Holstein calves from birth to 145 days of age on a large dairy farm in Brazil. Arq Bras Med Vet Zootec73: 1029-1038. 10.1590/1678-4162-12284). A calf’s susceptibility to pneumonia is influenced by the strength of its immune system and a previous occurrence of diarrhea (Ackermann et al., 2010Ackermann MR, Derscheid R, Roth JA, 2010. Innate immunology of bovine respiratory disease. Vet Clin North Am Food Anim Pract26: 215-228. 10.1016/j.cvfa.2010.03.001). The way diarrhea predisposes the occurrence of pneumonia could be due to nutritional setbacks that could deplete body fat, compromising the immune system and thus leaving the calf susceptible to subsequent respiratory infection (Moore et al., 2002Moore DA, Sischo WM, Festa DM, Reynolds JP , Robert Atwill E, Holmberg CA, 2002. Influence of arrival weight, season and calf supplier on survival in Holstein beef calves on a calf ranch in California, USA. Prev Vet Med53: 103-115. 10.1016/S0167-5877(01)00271-9). Also, diarrhea alters the gut microbiota, resulting in dysfunction of the gastrointestinal tract (Oultram et al., 2015Oultram J, Phipps E, Teixeira AGV, Foditsch C, Bicalho ML, Machado VS, Bicalho RC, Oikonomou G, 2015. Effects of antibiotics Oxytetracycline, florfenicol or tulathromycin on neonatal calves’ faecal microbial diversity. Vet Rec177: 598-598. 10.1136/vr.103320; Van Vleck Pereira et al., 2016Van Vleck Pereira R, Lima S, Siler JD, Foditsch C, Warnick LD, Bicalho RC, 2016. Ingestion of milk containing very low concentration of antimicrobials: Longitudinal effect on fecal microbiota composition in preweaned calves. PLOS ONE111: e0147525. 10.1371/journal.pone.0147525), which increases the risk for pneumonia. Another possibility could be that some pathogen agents, such as bovine coronaviruses, are associated with both neonatal calf diarrhea and pneumonia (Vlasova & Saif, 2021Vlasova AN, Saif LJ, 2021. Bovine coronavirus and the associated diseases. Front Vet Sci8: 643220. 10.3389/fvets.2021.643220); furthermore, in cases with severe debilitation, exists the possibility of complicating conditions such as bacterial pneumonia (Peek et al., 2018Peek SF, Mcguirk SM, Sweeney RW, Cummings KJ, 2018. Infectious diseases of the gastrointestinal tract. In: Rebhun’s Diseases of Dairy Cattle. Elsevier. pp. 249-356. 10.1016/B978-0-323-39055-2.00006-1).
The current study established that calves with FPI or suffering AG had greater odds of dying before weaning. These results align with other studies indicating that calves with serum total proteins <5.0 were 2.4 times more likely to experience mortality than those with serum total protein ranging between 5.0 and 6.0 g/dl (McCorquodale et al., 2013McCorquodale CE, Sewalem A, Miglior F, Kelton D, Robinson A, Koeck A, Leslie KE, 2013. Analysis of health and survival in a population of Ontario Holstein heifer calves. J Dairy Sci96: 1880-1885. 10.3168/jds.2012-5735). Stilwell & Carvalho (2011Stilwell G, Carvalho RC, 2011. Clinical outcome of calves with failure of passive transfer as diagnosed by a commercially available IgG quick test kit. Can Vet J525: 524-526.) showed that mortality due to infectious diseases was higher in the group with plasma IgG <10 mg/mL. Crannell & Abuelo (2023Crannell P, Abuelo A, 2023. Comparison of calf morbidity, mortality, and future performance across categories of passive immunity: A retrospective cohort study in a dairy herd. J Dairy Sci1064: 2729-2738. 10.3168/jds.2022-22567) found that preweaning mortality risk was higher in calves with poor passive immunity transfer than in excellent passive immunity. However, other studies have shown that serum IgG concentration has not resulted in a significant predictor of hazard for mortality (Chigerwe et al., 2015Chigerwe M, Hagey JV, Aly SS, 2015. Determination of neonatal serum immunoglobulin G concentrations associated with mortality during the first 4 months of life in dairy heifer calves. J Dairy Res824: 400-406. 10.1017/S0022029915000503). It is worth noting that some studies have only evaluated serum total protein concentrations and not serum IgG concentrations to assess passive immunity. Still, IgG determination is considered the reference method for determining passive transfer because the correlation between total proteins and serum IgG concentrations is inconsistent (Wilm et al., 2018Wilm J, Costa JHC, Neave HW, Weary DM, Von Keyserlingk MAG, 2018. Technical note: Serum total protein and immunoglobulin G concentrations in neonatal dairy calves over the first 10 days of age. J Dairy Sci101: 6430-6436. 10.3168/jds.2017-13553). Thus, the present study reaffirms that FPI in neonatal calves is responsible for reduced resistance to disease and increased mortality in calves early in life.
In line with other studies in different environments, despite the antimicrobial therapy, comorbidity of diarrhea and pneumonia markedly increased the risk of calf mortality (Gulliksen et al., 2009Gulliksen SM, Jor E, Lie KI, Hamnes IS, Løken T, Åkerstedt J, Østerås O, 2009. Enteropathogens and risk factors for diarrhea in Norwegian dairy calves, J Dairy Sci92: 5057-5066, 10.3168/jds.2009-2080; Alemu et al., 2022Alemu YF, Jemberu WT, Mekuriaw Z, Abdi RD, 2022. Incidence and predictors of calf morbidity and mortality from birth to 6 months of age in dairy farms of northwestern Ethiopia. Front Vet Sci9: 859401. 10.3389/fvets.2022.859401; Schinwald et al., 2022Schinwald M, Creutzinger K, Keunen A, Winder CB, Haley D, Renaud DL, 2022. Predictors of diarrhea, mortality, and weight gain in male dairy calves. J Dairy Sci105: 5296-5309. 10.3168/jds.2021-21667). These results are partly due to nutrient malabsorption, electrolyte loss, and respiratory tract lesions (Gaudino et al., 2022Gaudino M, Nagamine B, Ducatez MF, Meyer G, 2022. Understanding the mechanisms of viral and bacterial coinfections in bovine respiratory disease: A comprehensive literature review of experimental evidence. Vet Res53: 70. 10.1186/s13567-022-01086-1).
It was concluded that low post-colostral IgG levels and agammaglobulinemia were significant risk factors for pneumonia and diarrhea in the preweaning period. Also, calves with diarrhea faced an increased chance of pneumonia. Calves diagnosed either with diarrhea or pneumonia had a significantly increased risk of death. This study indicates that to reduce calf mortality in high-input dairy farms, attention should be focused on monitoring serum IgG 24 h postpartum in calves to ensure the attainment of adequate colostral-derived immunoglobulins. Also, the present study suggested that a digital Brix refractometer represents a valuable tool for estimating serum IgG in calves on time and for evaluating the success of the colostrum feeding program.