Introduction
⌅Respiratory system pathologies that lead to pneumonia constitute a chronic endemic disease in dairy calves in intensive systems worldwide (Buczinski et al., 2021Buczinski S, Achard D, Timsit E, 2021. Effects of calfhood respiratory disease on health and performance of dairy cattle: A systematic review and meta-analysis. J Dairy Sci104(7): 8214-8227. 10.3168/jds.2020-19941). This disease is one of the main causes of livestock losses in dairy farming when considering production performance (Windeyer et al., 2014Windeyer MC, Leslie KE, Godden SM, Hodgins DC, Lissemore KD, LeBlanc SJ, 2014. Factors associated with morbidity, mortality, and growth of dairy heifer calves up to 3 months of age. Prev Vet Med132: 231-240. 10.1016/j.prevetmed.2013.10.019; Jourquin et al., 2023Jourquin S, Lowie T, Debruyne F, Chantillon L, Vereecke N, Boye, 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(1): 676-689. 10.3168/jds.2022-22212), animal welfare (Barry et al., 2020Barry J, Bokkers EAM, De Boer IJM, Kennedy E, 2020. Pre-weaning management of calves on commercial dairy farms and its influence on calf welfare and mortality. Animal14: 2580-2587. 10.1017/S1751731120001615), the use of antimicrobials (Bokma et al., 2020Bokma J, Boone R, Deprez P, Pardon B, 2020. Short communication: Herd-level analysis of antimicrobial use and mortality in veal calves: Do herds with low usage face higher mortality?J Dairy Sci103: 909-914. 10.3168/jds.2019-16764) and consequently antimicrobial resistance (Zhang et al., 2022Zhang X, Yi X, Zhuang H, Deng Z, Ma C, 2022. Invited review: Antimicrobial use and antimicrobial resistance in pathogens associated with diarrhea and pneumonia in dairy calves. Animals12: 771. 10.3390/ani12060771). This disease is a significant problem in dairy operations where calves are raised artificially, as it causes high morbidity and mortality rates (Dubrovsky et al., 2019Dubrovsky SA, Van Eenennaam AL, Karle BM, Rossitto PV, Lehenbauer TW, Aly SS, 2019. Bovine respiratory disease (Brd) cause-specific and overall mortality in preweaned calves on California dairies: The BRD 10K study. J Dairy Sci102: 7320-7328. 10.3168/jds.2018-15463), increases farm costs related to treatment and prevention (Hyde et al., 2022Hyde RM, Green MJ, Hudson C, Down PM, 2022. Improving growth rates in preweaning calves on dairy farms: A randomized controlled trial. J Dairy Sci105: 782-792. 10.3168/jds.2021-20947), and potentially affects the future performance of animals (Dubrovsky et al., 2020; Buczinski et al., 2021Buczinski S, Achard D, Timsit E, 2021. Effects of calfhood respiratory disease on health and performance of dairy cattle: A systematic review and meta-analysis. J Dairy Sci104(7): 8214-8227. 10.3168/jds.2020-19941).
Likewise, gastrointestinal tract diseases manifested in diarrhea are frequent in preweaning dairy calves and are the main cause of death in the pre-weaning period (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). Diarrhea in the preweaning period is associated with adverse effects on subsequent reproductive performance (Aghakeshmiri et al., 2017Aghakeshmiri F, Azizzadeh M, Farzaneh N, Gorjidooz M, 2017. Effects of neonatal diarrhea and other conditions on subsequent productive and reproductive performance of heifer calves. Vet Res Commun41: 107-112. 10.1007/s11259-017-9678-9), increased antimicrobial use (Zhang et al., 2022Zhang X, Yi X, Zhuang H, Deng Z, Ma C, 2022. Invited review: Antimicrobial use and antimicrobial resistance in pathogens associated with diarrhea and pneumonia in dairy calves. Animals12: 771. 10.3390/ani12060771), and long-lasting economic impact, including a reduction in average daily gain (ADG) (Anderson et al., 2003Anderson DC, Kress DD, Bernardini TMM, Davis KC, Boss DL, Doornbos DE, 2003. The effect of scours on calf weaning. Prof Anim Sci19: 399-403. 10.15232/S1080-7446(15)31455-8), an increased services per conception, and a reduction of around 300 kg in milk production during the first lactation (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).
Previous research on calfhood bovine respiratory and enteric diseases has been linked to reduced ADG and future cow performance. These studies have been carried out in cooler environments with comfortable calf sheds. Diarrhea and pneumonia can vary by climatic conditions, herd size, and farm management practices (Cho & Yoon, 2014Cho Y, Yoon KJ, 2014. An overview of calf diarrhea—Infectious etiology, diagnosis, and intervention. J Vet Sci15(1): 1. 10.4142/jvs.2014.15.1.1; Maier et al., 2019Maier GU, Love WJ, Karle BM, Dubrovsky SA, Williams DR, Champagne JD, Anderson RJ, Rowe JD, Lehenbauer TW, Van Eenennaam AL, Aly SS, 2019. Management factors associated with bovine respiratory disease in preweaned calves on California dairies: The BRD 100 study. J Dairy Sci102(8): 7288-7305. 10.3168/jds.2018-14773). Therefore, it is pertinent to determine the impact of preweaning pneumonia and diarrhea on preweaning weight gain and subsequent fertility in heat-stressed calves because calves experiencing thermal stress during their development reduce their feed intake (López et al., 2018López E, Mellado M, Martínez AM, Véliz FG, García JE, De Santiago A, Carrillo E, 2018. Stress-related hormonal alterations, growth and pelleted starter intake in pre-weaning Holstein calves in response to thermal stress. Int J Biometeorol62(4): 493-500. 10.1007/s00484-017-1458-2), increase energy needs, weaken their immune function (Gupta et al., 2023) and increases their susceptibility to diseases (Bagath et al., 2019Bagath M, Krishnan G, Devaraj C, Rashamol VP, Pragna P, Lees AM, Sejian V, 2019. The impact of heat stress on the immune system in dairy cattle: A review. Res Vet Sci126: 94-102. 10.1016/j.rvsc.2019.08.011).
The present study investigates the null hypothesis that preweaning growth rate and reproductive metrics among artificially-reared Holstein calves do not differ between calves suffering diarrhea or pneumonia from healthy ones. This study aimed to determine the impacts of pneumonia and diarrhea from birth to weaning on preweaning ADG of Holstein calves raised in a commercial dairy farm in a hot environment. Additionally, the study examined the effects of birth weight on calf health and the occurrence of diarrhea and pneumonia from birth to weaning on the reproductive performance of Holstein heifers.
Material and methods
⌅Study design, animals, and housing
⌅The study protocol was approved by the Animal Experiment Committee of the Autonomous Agrarian University Antonio Narro (#03001-2198). The study was carried out on a single large (~3200 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 January 2020 to June 2023. The study included complete record data (preweaning growth and reproductive traits) of 7,809 heifers. The births were relatively well distributed across seasons: 29.9% (n = 1157), 25.2% (n = 1969), 36.0% (n = 2813), and 23.9% (n = 1870) of calves that were born in spring, summer, fall, and winter, respectively.
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, which prevented urine buildup. Each pen had two feeding pails with supporters. Pens were about 0.5 m apart, which minimized microbial loads in the calves´ ambient. Pens were moved to a different place and were washed and sanitized between calves.
Immediately after birth, calves were separated from their dams, navel-dipped, weighed on a digital scale (Coburn Company, Whitewater, Wisconsin, USA), and reared outdoors in all seasons. Calves were identified using traditional plastic ear tags. Two liters of high-quality colostrum (at least 50 mg/mL of immunoglobulins, based on specific gravity reading; JorVet Bovine Colostrometer, Jorgensen Laboratories, Loveland, CO, USA) from freshly calved cows was fed to calves within one hour of birth. Two more liters were given within the next 8 hours after birth. Dairy herd staff members administered colostrum to all calves via esophageal feeders (Nasco, Fort Atkinson, WI, USA).
Calf and heifer recordings
⌅Well-trained staff registered gender and birth weight. During the preweaning period, the herd veterinarians recorded the occurrence of diarrhea, pneumonia, and other health conditions such as lameness, infections, or injuries. The study did not include heifers presenting diseases other than diarrhea or pneumonia before weaning. 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. Pneumonia in calves was described as elevated respiratory rate, serous nasal discharge, coughing, fever, mild depression, and loss of appetite. treated Calves suffering from diarrhea or pneumonia were treated by the herd veterinarians following standard procedures for these diseases. Calves/heifers that died between birth and first calving were excluded from the study.
Outcomes of interest were preweaning growth rate, weaning weight at approximately 60 days, the occurrence of pneumonia and diarrhea, age at first breeding (AFB; defined as the age when a heifer was first recorded bred), age at conception, number of services per pregnancy, pregnancy rate at first service, and pregnancy rate to all services (only pregnant heifers). Weaning weight (WW) data, adjusted to 60 days of age, were calculated as follows: WW= (B-C/D × 60) + C, where WW= 60-day weight (kg), B= weaning weight (kg), C= birth weight (kg), D weaning age (days). Calving data were sorted by months and grouped into seasons: winter months, December to February; spring, March to May; summer, June to August; and fall, September to November. Birthweight was classified into <36, 36-38, 38-40, and >40 kg.
Statistical analysis
⌅Data were entered into a spreadsheet (Excel, Microsoft, Inc.) and transferred to SAS 9.4 (SAS Institute, Inc., Cary, NC, USA). Graphs were made using CurveExpert (version 9.1.1 for Mac, GraphPad Software, San Diego, California, USA; www.graphpad.com). The experimental units were individual calves.
To compare calves with and without diarrhea and pneumonia, based on birth weight (<36, 36-38, 38-40, and >40 kg), the GENMOD procedure of SAS was used. A logit link function was used, and a binomial distribution of the data was assumed. The following model was used:
Yijk = µ + Gi + β(Xij − X) + eijk, where: Yij = observed value of the dependent variable; µ = overall average; Gi = effect of group (n=4); β(Xij − X) = effect of season of calving (covariate; n=4), and eij= experimental error. Calves were the experimental units.
To analyze the effect of preweaning diseases contributing to overall pregnancy, percentage of pregnant heifers at 14 months, and first service pregnancy rate (binary outcome), the GENMOD procedure of SAS (SAS Institute Inc., Cary, North Carolina, USA) was employed using a model that included the fixed effects of group (preweaning diarrhea, pneumonia, co-occurrence of these diseases and healthy calves) with season of calving as a covariate. To compare means, the DIFF option was used.
The effect of the occurrence of diseases before weaning on the continuous variables was analyzed using the GLM procedure of SAS with the following model: Yijk = µ + Gi + β(Xij − X) + β(Wij − Y) + β(Zij − Z) + eijk, where Yijk = observed value of the dependent variable, μ= overall mean, Gi= the effect of group, eijk = random error, β = partial linear regression coefficient of Yijk on the continuous variables (possible confounders), Xij (birth weight; four classes),Wij [season of birth (four classes; winter: December to February, spring: March to May, summer: June to August, and autumn: September to November)] and Zij(year of birth), X, W, and Z = overall average of birth weight, season of birth, and year of birth, respectively. To compare the means the PDIFF option was used. Calves were the experimental units.
The bivariate Wilcoxon rank-sum test assessed the number of services per pregnancy (non-parametric; proc npar1way of SAS). The timing of diseases onset relative to parturition was analyzed using survival plots generated by Kaplan-Meier survival analysis performed with Statgraphics Centurion version XVII software (Statgraphics Technologies, Inc., The Plains, Virginia). For the time of postpartum disease onset, survival analyses were performed for calves with diarrhea or pneumonia using the Cox proportional hazard model (Statgraphics Centurion XV software). Survival curves were generated at an exit time point of 60 days (weaning). For all analyses, the significance was established at p<0.05.
Results
⌅Overall, 58.2% of the enrolled calves suffered from a disease, and 4.5% had concurrent diseases. Among the 7,809 calves in the present study, 1,680 (21.5%) had diarrhea, and 2,511 (32.2%) had pneumonia. Mean ± Standard Deviation birth weight was 37.6 ± 2.8 kg and ranged from 34.0 kg to 47.0 kg. The median (50th percentile for the set of values) time to diarrhea and pneumonia was 8.0 and 31.0 d, respectively.
The growing performance of calves from birth to weaning according to their health status is presented in Table 1. When evaluating the effects of diarrhea, pneumonia, or the concurrence of these conditions on preweaning ADG, it was found that calves suffering from these diseases had lower (p<0.01) preweaning weight gain than their healthy counterparts. Calves presenting both diseases before weaning had a lower ADG than calves that had only one disease. Likewise, weaning weight was greater (p<0.01) in healthy calves than in their peers with diarrhea, pneumonia, or both illnesses. Simultaneous presence of these medical conditions was associated with lower (p<0.01) weaning weight than calves suffering a single illness.
The reproductive performance of heifers based on diarrhea and pneumonia occurrence is presented in Table 2. Days to first insemination were eight days shorter (p<0.01) for healthy heifers than those with diarrhea. Likewise, days to first insemination were seven days shorter (p<0.01) for healthy heifers than for those with pneumonia. Heifers with co-morbidity of these diseases required 13 more (p<0.01) days for their first service.
| Reproductive variables | Diarrhea (D) | Pneumonia (P) | Comorbodity D-P | Healthy | |
|---|---|---|---|---|---|
| Days to first insemination | 389 ± 10b | 388 ± 10b | 394 ± 13a | 381 ± 10c | |
| Pregnant at 14 months of age1 | 1079/1337 (80.7)c | 1909/2157 (88.5)b | 246/350 (70.3)d | 3724/3965 (93.9)a | |
| Services per pregnancy | 1.5 ± 0.6b | 1.5 ± 0.6b | 1.7 ± 1.0a | 1.3 ± 0.5c | |
| Days to pregnancy | 401 ± 20b | 399 ± 16b | 414 ± 19a | 389 ± 19c | |
| Days to parturition | 681 ± 28b | 681 ± 16b | 696 ± 19a | 670 ± 19d | |
| First service pregnancy rate1 | 697/1337 (52.1)b | 1097/2157 (50.9)b | 103/350 (29.4)c | 2393/3965 (60.4)a. | |
| Pregnancy rate, all services1 | 1159/1337 (86.7)c | 1940/2157 (89.9)b | 305/350 (87.1)c | 3743/3965 (94.4)a. | |
Calves suffering from diarrhea, pneumonia, or the concurrence of these diseases had a greater (p<0.01) number of services per pregnancy than healthy calves before weaning. Days to pregnancy were lowest (p<0.01) in heifers without diarrhea or pneumonia and highest in those who suffered diarrhea comorbid with pneumonia. The occurrence of diarrhea or pneumonia in the preweaning period reduced (p<0.01) the pregnancy rate at first service by 10 percentage points compared to healthy heifers. Co-occurrences of diarrhea and pneumonia in the preweaning period decreased (p<0.01) pregnancy rate at first service by 22 percentage points compared to heifers suffering from single diseases.
The overall pregnancy rate was lower (p<0.01) in heifers having diarrhea, pneumonia, or comorbid conditions than in healthy heifers in the preweaning period. Days to calving were 9 days shorter (p<0.01) in healthy calves than heifers suffering diarrhea or pneumonia in the preweaning period. A comorbid condition was associated with 15 more (p<0.01) days to first freshening than heifers with only diarrhea or pneumonia.
Lighter calves at calving were more likely (p<0.05) to present diarrhea than heavier calves (Figure 1). However, birth weight did not affect the occurrence of pneumonia. The survival analysis for age when a calf was diagnosed with diarrhea or pneumonia (Figure 2) shows more reduced (p<0.01) time for calves suffering diarrhea (50th percentile = 8.0 days; SEM = 0.08) in the first 60 days of life, compared to pneumonia (50th percentile = 31.0 days; SEM = 0.68). After 25 days of age, the probability of diarrhea declined sharply, whereas pneumonia was more evenly distributed during the preweaning period.
Discussion
⌅The present study showed that the occurrence of diarrhea or pneumonia in the preweaning period resulted in lower daily weight gain, which is consistent with previous studies in dairy calves where abnormal fecal consistency (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(6): 5296-5309. 10.3168/jds.2021-21667), diarrhea (Pardon et al., 2013Pardon B, Hostens M, Duchateau L, Dewulf J, De Bleecker K, Deprez P, 2013. Impact of respiratory disease, diarrhea, otitis and arthritis on mortality and carcass traits in white veal calves. BMC Vet Res9(1): 79. 10.1186/1746-6148-9-79) or pneumonia (Bringhenti et al., 2021Bringhenti L, Pallu M, Silva JC, Tomazi T, Tomazi ACCH, Rodrigues MX, Cruzado-Bravo M, Bilby TR, Bicalho RC, 2021. Effect of treatment of pneumonia and otitis media with tildipirosin or florfenicol + flunixin meglumine on health and upper respiratory tract microbiota of preweaned Holstein dairy heifers. J Dairy Sci104(9): 10291-10309. 10.3168/jds.2020-19945; Tomazi et al., 2023Tomazi ACCH, Tomazi T, Bringhenti L, Vinhal APA, Rodrigues MX, Bilby TR, Huson HJ, Bicalho RC, 2023. Treatment with 2 commercial antibiotics reduced clinical and systemic signs of pneumonia and the abundance of pathogenic bacteria in the upper respiratory tract of preweaning dairy calves. J Dairy Sci106(4): 2750-2771. 10.3168/jds.2022-22451) decreased ADG. As expected, calves with co-occurrence enteric and respiratory disease events during the preweaning period gained less weight than calves with no disease events or a single infection. Still, results showed no association between underweight and comorbidity. Therefore, these data indicate that birth weight status is not a determinant of comorbidity of diarrhea and pneumonia.
Disease status is a significant factor influencing the growth rate of calves. Preweaning illness impacts the available nutrients in multiple ways. For instance, satisfactory nutrition is necessary for cells, including the innate response to an invading pathogen, to perform their functions optimally (Calder et al., 2020Calder P, Carr A, Gombart A, Eggersdorfer M, 2020. Optimal nutritional status for a well-functioning immune system is an important factor to protect against viral infections. Nutrients12(4): 1181. 10.3390/nu12041181; Venter et al., 2020Venter C, Eyerich S, Sarin T, Klatt KC, 2020. Nutrition and the immune system: A complicated tango. Nutrients12(3): 818. 10.3390/nu12030818). The nutritional requirement further increases during infection as immune cells use direct and indirect approaches to combat those pathogens (Lee et al., 2020). For example, consuming enough nutrients is essential for optimal antibody production (Hamidianshirazi et al., 2022Hamidianshirazi M, Ekramzadeh M, Hamidianshirazi AR, Zangene A, 2022. Association between nutrition and immune system: A review. Int J Nutr Sci7(2): 65-74. 10.30476/IJNS.2022.94619.1180). Additionally, diarrhea contributes to low calf weight gain by causing nutrient malabsorption or nutrient loss from the diet via diarrhea (Smith, 2009Smith GW, 2009. Treatment of calf diarrhea: oral fluid therapy. Vet Clin North Am Food Anim Pract25: 55-72. 10.1016/j.cvfa.2008.10.006), reduced feed intake (Morrison et al., 2019Morrison SY, LaPierre PA, Brost KN, Drackley JK, 2019. Intake and growth in transported Holstein calves classified as diarrheic or healthy within the first 21 days after arrival in a retrospective observational study. J Dairy Sci102(12): 10997-11008. 10.3168/jds.2019-16609), and decreased feed conversion efficiency (Hessman et al., 2009Hessman BE, Fulton RW, Sjeklocha DB, Murphy TA, Julia F, Payton ME, Elisa A, 2009. Evaluation of economic effects and the health and performance of the general cattle population after exposure to cattle persistently infected with bovine viral diarrhea virus in a starter feedlot. Am J Vet Res70: 73–85. 10.2460/ajvr.70.1.73; Khan et al., 2011Khan M, Weary D, Von Keyserlingk M, 2011. Effects of milk ration on solid feed intake, weaning, and performance in dairy heifers. J Dairy Sci94: 1071–1081. 10.3168/jds.2010-3733). Additionally, it could be that slow-growing calves are at higher risk of diarrhea or pneumonia before weaning.
The preweaning ADG in the present study was much lower than that reported by other researchers on Holstein calves (Rosenberger et al., 2017Rosenberger K, Costa JHC, Neave HW, Von Keyserlingk MAG, Weary DM, 2017. The effect of milk allowance on behavior and weight gains in dairy calves. J Dairy Sci100(1): 504-512. 10.3168/jds.2016-11195; Lucei et al., 2021). The prolonged heat stress during the year in the present study potentially could explain the lower ADG in the study population (López et al., 2018López E, Mellado M, Martínez AM, Véliz FG, García JE, De Santiago A, Carrillo E, 2018. Stress-related hormonal alterations, growth and pelleted starter intake in pre-weaning Holstein calves in response to thermal stress. Int J Biometeorol62(4): 493-500. 10.1007/s00484-017-1458-2). Low birth weight was associated with a higher incidence of diarrhea from birth to weaning. These results align with those of Fagundes et al. (2016Fagundes TF, Vidal LGP, Alves PAM, Tassinari WDS, Alves Alcântara de Menezes AD, Fonseca, AHD, Pereira MJS, 2016. Risk factors for diarrhea in a cohort of dairy heifer calves reared in individual outdoor hutches in Piraí, Rio de Janeiro, Brazil. Semina: Cienc Agr37(5): 3159. 10.5433/1679-0359.2016v37n5p3159), who observed that birth weight ≥ 40 kg in crossbred Holstein calves reduced the risk of diarrhea. Furthermore, it has been observed that higher weight in the first week of life is associated with less diarrhea (Windeyer et al., 2014Windeyer MC, Leslie KE, Godden SM, Hodgins DC, Lissemore KD, LeBlanc SJ, 2014. Factors associated with morbidity, mortality, and growth of dairy heifer calves up to 3 months of age. Prev Vet Med132: 231-240. 10.1016/j.prevetmed.2013.10.019). Low birth weight results from in-utero nutritional insufficiency, and such exposure early in life may have long-term implications for immunocompetence (Osorio et al., 2013Osorio JS, Trevisi E, Ballou MA, Bertoni G, Drackley JK, Loor JJ, 2013. Effect of the level of maternal energy intake prepartum on immunometabolic markers, polymorphonuclear leukocyte function, and neutrophil gene network expression in neonatal Holstein heifer calves. J Dairy Sci96: 3573-3587. 10.3168/jds.2012-5759). Therefore, this variable would help develop preventive measures and assess the prognosis of enteric infections for individual calves. Birth weight did not affect the occurrence of preweaning pneumonia, consistent with observations of Curtis et al. (2016Curtis GC, Argo C McG, Jones D, Grove‐White DH, 2016. Impact of feeding and housing systems on disease incidence in dairy calves. Vet Rec179: 512-512. 10.1136/vr.103895) and Glover et al. (2019Glover ID, Barrett DC, Reyher KK, 2019. Little association between birth weight and health of preweaned dairy calves. Vet Rec184(15): 477-477. 10.1136/vr.105062), who have reported negligible associations between birthweight and incidence of this respiratory disease.
The peak incidence of diarrhea in the present study was at eight days of age, which agrees with previous studies (Foster et al., 2009Foster DM, Smith GW, 2009. Pathophysiology of diarrhea in calves. Vet Clin North Am Food Anim Pract25(1): 13-36. 10.1016/j.cvfa.2008.10.013; Windeyer et al., 2014Windeyer MC, Leslie KE, Godden SM, Hodgins DC, Lissemore KD, LeBlanc SJ, 2014. Factors associated with morbidity, mortality, and growth of dairy heifer calves up to 3 months of age. Prev Vet Med132: 231-240. 10.1016/j.prevetmed.2013.10.019; Berber et al., 2021Berber E, Çanakoğlu N, Sözdutmaz İ, Simsek E, Sursal N, Ekinci G, Kökkaya S, Arıkan E, Ambarcıoğlu P, Göksu A, Keleş I, 2021. Seasonal and age-associated pathogen distribution in newborn calves with diarrhea admitted to ICU. Vet Sci8(7): 128. 10.3390/vetsci8070128). Peak incidence of pneumonia in the present study was at 33 days, which is in line with previous studies where this respiratory tract disease becomes a critical health problem in replacement heifers older than 30 days of age (McGuirk, 2008McGuirk SM, 2008. Disease management of dairy calves and heifers. Vet Clin North Am Food Anim Pract24:139-153. 10.1016/j.cvfa.2007.10.003).
In the present study, the age at first breeding was shorter in healthy heifers than heifers diagnosed with diarrhea, pneumonia, and co-occurrence of these diseases before weaning. The decision on at what age to start breeding heifers is based chiefly on the puberal weight of heifers. Healthy heifers in the present study grew faster than sick counterparts and, therefore, the association between diarrhea and pneumonia occurrence is probably because the absence of diseases from birth to weaning enhanced growth rate of heifers from weaning to puberty, which allowed heifers to attain earlier the appropriate weight for first service. The adverse effects of respiratory infection on ADG following movement to group housing can be observed up to approximately nine months of age. Average daily gain results in a 14.3 kg decrease in body weight (BW) for calves with respiratory infections at one year of life (Stanton et al., 2012Stanton AL, Kelton DF, LeBlanc SJ, Wormuth J, Leslie KE, 2012. The effect of respiratory disease and a preventative antibiotic treatment on growth, survival, age at first calving, and milk production of dairy heifers. J Dairy Sci95(9): 4950-4960. 10.3168/jds.2011-5067). Although a calf's life returns to normal after pneumonia recovery, lung damage often remains (Hermeyer et al., 2012Hermeyer K, Buchenau I, Thomasmeyer A, Baum B, Spergser J, Rosengarten R, Hewicker-Trautwein M, 2012. Chronic pneumonia in calves after experimental infection with Mycoplasma bovis strain 1067: Characterization of lung pathology, persistence of variable surface protein antigens and local immune response. Acta Vet Scand54(1): 9. 10.1186/1751-0147-54-9), indicating how critical healthy lungs are to an animal’s subsequent fertility. In the case of diarrhea, the long-lasting effect of this disease is less clear because when multiple pathogens damage the intestines, the damaged lining tissue grows back, and the intestines’ function returns to normal fairly quickly when the appropriate antimicrobials are used (Constable, 2009Constable PD, 2009. Treatment of calf diarrhea: Antimicrobial and ancillary treatments. Vet Clin North Am Food Anim Pract25(1): 101-120. 10.1016/j.cvfa.2008.10.012).
It has long been suggested that heifers be inseminated to calve between 23 and 24 months (Ettema and Santos, 2004Ettema JF, Santos JEP, 2004. Impact of age at calving on lactation, reproduction, health, and income in first-parity Holsteins on commercial farms. J Dairy Sci87: 2730-2742. 10.3168/jds.S0022-0302(04)73400-1; Boulton et al., 2015Boulton AC, Rushton J, Wathes DC, 2015. A study of dairy heifer rearing practices from birth to weaning and their associated costs on UK dairy farms. Open J Anim Sci5: 185–197. 10.4236/ojas.2015.52021) because decreasing the age at first calving (AFC) reduces rearing costs and extends the herd life. In the current study, the mean AFC for healthy heifers was shorter than in heifers diagnosed with diarrhea, pneumonia, or comorbidity of these diseases during calfhood, which is in line with observations of Teixeira et al. (2017Teixeira AGV, McArt JAA, Bicalho RC, 2017. Thoracic ultrasound assessment of lung consolidation at weaning in Holstein dairy heifers: Reproductive performance and survival. J Dairy Sci100(4): 2985-2991. 10.3168/jds.2016-12016) where heifers suffering lung consolidation at 60 d of life had a higher AFC. This response could result from a greater weight gain in healthy heifers, as AFC is linked to ADG before puberty (Raeth-Knight et al., 2009Raeth-Knight M, Chester-Jones H, Hayes S, Linn J, Larson R, Ziegler D, Ziegler B, Broadwater N, 2009. Impact of conventional or intensive milk replacer programs on Holstein heifer performance through six months of age and during first lactation. J Dairy Sci92: 799-809. 10.3168/jds.2008-1470; Stefańska et al., 2021Stefańska B, Gąsiorek M, Nowak W, 2021. Short- and long-term effects of initial serum total protein, average starter feed intake during the last week of the preweaning period, and rearing body gain on primiparous dairy heifers’ performance. J Dairy Sci104: 1645-1659. 10.3168/jds.2020-18833). Healthy calves could have shown a better ADG not only because they did not suffer any disease but also because they were born with a higher birth weight, and this fact could condition that they reach a greater weight at weaning and consequently improve the fertility indexes.
Furthermore, early episodes of pneumonia or diarrhea could cause carry-over effects on reproductive outcome, as reported by Heinrichs et al. (2005Heinrichs A J, Heinrichs B S, Harel O, Rogers GW, Place NT, 2005. A prospective study of calf factors affecting age, body size, and body condition score at first calving of Holstein dairy heifers. J Dairy Sci88(8): 2828-2835. 10.3168/jds.S0022-0302(05)72963-5), who showed that AFC was not only affected by ADG but also health problems during the first two months of life. Likewise, Warnick et al. (1994Warnick L, Erb H, White M, 1994. The association of calfhood morbidity with first-lactation calving age and dystocia in New York Holstein herds. Kenya Vet18: 177–179.) found that heifers with respiratory tract infections in the first three months of life calved three months later than their healthy herd mates. Age at first calving is a crucial factor for dairy farmers because it significantly affects the lifetime productivity of heifers (Le Cozler et al., 2008Le Cozler Y, Lollivier V, Lacasse P, Disenhaus C, 2008. Rearing strategy and optimizing first-calving targets in dairy heifers: A review. Animal2: 1393–1404. 10.1017/S1751731108002498). Therefore, avoiding diseases before weaning is a good start to life in heifers because it paves the way for increased productivity in the future.
It is worth mentioning that previous economic analyses indicate that calving at 24 months is more advantageous than calving at older ages because of reduced replacement heifer costs and earlier heifer productivity (Boulton et al., 2017Boulton AC, Rushton J, Wathes DC, 2017. An empirical analysis of the cost of rearing dairy heifers from birth to first calving and the time taken to repay these costs. Animal11(8): 1372-1380. 10.1017/S1751731117000064). The median age at calving observed in heifers suffering from pneumonia in our study (22.6 months) indicates that this goal was achieved regardless of pneumonia history.
In agreement with 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), services per pregnancy were increased in heifers with a history of preweaning diarrhea. This response can be explained by the reduced weight gain of the diseased calves, as poorly grown calves require more services to conceive (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). Furthermore, the pregnancy rate was higher in healthy heifers early in life, which is in line with previous studies in which the likelihood of pregnancy decreased in heifers with a history of diarrhea (Aghakeshmiri et al., 2017Aghakeshmiri F, Azizzadeh M, Farzaneh N, Gorjidooz M, 2017. Effects of neonatal diarrhea and other conditions on subsequent productive and reproductive performance of heifer calves. Vet Res Commun41: 107-112. 10.1007/s11259-017-9678-9; 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). Furthermore, the results of the present study are in line with previous studies in which heifers with a history of calfhood diseases have lower reproductive efficiency, particularly in the key reproductive metric of pregnancy rate (Teixeira et al., 2017Teixeira AGV, McArt JAA, Bicalho RC, 2017. Thoracic ultrasound assessment of lung consolidation at weaning in Holstein dairy heifers: Reproductive performance and survival. J Dairy Sci100(4): 2985-2991. 10.3168/jds.2016-12016; 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). These data suggest that the health problems early in life had a long-term carryover effect on heifers’ fertility, and periods of calfhood disease compromise development with long-term adverse consequences on reproductive outcomes. Therefore, some of the economic losses attributed to preweaning episodes of pneumonia or diarrhea are due to suboptimal fertility.
Conclusion
⌅This study provides evidence that Holstein calves in a hot environment that suffer from diarrhea, pneumonia, or co-occurrence of both diseases before weaning presented lower preweaning weight gain, which was reflected in decelerating the occurrence of the first service and increasing the age at pregnancy and calving. Furthermore, episodes of these diseases early in life were detrimental to pregnancy rate. Since initial low birth weight affected the occurrence of diarrhea, the need to selectively treat these light calves to prevent this condition should be emphasized. Furthermore, strategies to prevent diarrhea and pneumonia before weaning might be required to improve the reproductive performance of Holstein heifers in intensive production systems in warm environments.