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Static and Dynamic Components of Right Ventricular Afterload Are Negatively Associated with Calf Survival at High Altitude1

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Static and Dynamic Components of Right Ventricular Afterload Are Negatively Associated with Calf Survival at High Altitude1 Published September 29, 2016 Static and dynamic components of right ventricular afterload are negatively associated with calf survival at high altitude1 J. M. Neary,*2 R. D. Brown,† T. N. Holt,‡ K. R. Stenmark,† R. M. Enns,§ M. G. Thomas,§ and F. B. Garry‡ *Department of Animal and Food Sciences, College of Agricultural Sciences and Natural Resources, Texas Tech University, Lubbock 79409-2141; †Division of Pediatric Critical Care, School of Medicine, University of Colorado Denver, Aurora 80045; ‡Integrated Livestock Management, Department of Clinical Sciences, College of Veterinary Medicine and Biomedical Sciences, Colorado State University, 1678 Campus Delivery, Fort Collins 80523-1678; and, §Department of Animal Sciences, The College of Agricultural Sciences, Colorado State University, Fort Collins 80523-1171. ABSTRACT: The purposes of this study were to pulse pressures (P = 0.03) at 3 mo of age than calves evaluate mean, systolic, and diastolic pulmonary that survived to 7 mo. Calves presumed to have died arterial pressures; pulmonary arterial pulse pres- tended to have greater systemic oxygen extraction sures; and systemic oxygen extraction fraction as fractions at 3 mo of age than calves that survived (P risk factors for the survival of suckling calves on one = 0.13). Diastolic pressure was not associated with ranch located at an altitude of 2,730 m in Colorado, survival (P = 0.27). Mean pulmonary arterial pres- USA. A prospective cohort study of 58 calves was sure is predominantly determined by static resistance performed. Pulmonary arterial pressures and sys- attributable to distal pulmonary arterial remodeling. temic oxygen extraction were measured when calves Pulse pressure and systolic pulmonary arterial pres- were approximately 3 mo (86 ± 7 d) and 7 mo (197 sure represents the dynamic or oscillatory resistance ± 6 d) of age. Seven of the 58 calves (12%), 4 steers and is determined by the characteristics of ventricu- and 3 heifers, were unaccounted for and presumed lar ejection and proximal arterial stiffness. These dead between 3 and 7 mo of age. Calves presumed findings indicate that it may be beneficial to include to have died between 3 and 7 mo of age had sig- pressure measurements indicative of both static and nificantly greater mean (P = 0.005) and systolic (P dynamic pulmonary arterial resistance in the selec- = 0.001) pulmonary arterial pressures and greater tion of breeding stock at high altitude. © 2016 American Society of Animal Science. All rights reserved. J. Anim. Sci. 2016.94 doi:10.2527/jas2016-0652 INTRODUCTION is a leading cause of suckling calf death loss among ranches at altitudes over 2,400 m (Neary et al., 2013). Right-sided congestive heart failure (RHF) sec- The susceptibility of cattle (Bos taurus) to hypoxia- ondary to pulmonary hypertension, or cor pulmonale, induced pulmonary hypertension has been attributed to their highly muscular small pulmonary arteries that vasoconstrict and remodel in response to hypoxia (Al- 1Funding for the study was provided by producer donations to exander and Jensen, 1963a,b; Tucker et al., 1975). the Integrated Livestock. Management program of the College of Because mean pulmonary arterial pressure Veterinary and Biomedical Sciences, Colorado State University; (mPAP) is moderately heritable (Shirley et al., 2008; the Department of Animal Science’s John E. Rouse Endowment, Newman et al., 2015), producers at high altitudes Colorado State University; and, the National Institutes of Health (> 2000 m) commonly screen their breeding stock (HL-014985, to KRS). The content is solely the responsibility of to identify individuals with high mPAP—typically the authors. The authors have no conflicts of interest to declare. 45 mmHg—and remove them from the herd (Holt 2Corresponding author: [email protected] and Callan, 2007). This strategy is thought to reduce Received May 20, 2016. Accepted July 15, 2016. the incidence of RHF because cattle with mPAP ◊ ◊ Neary et al. 45 mmHg are considered to be at increased risk of at an altitude of 2,410 m. At 2 mo of age, they were RHF (Holt and Callan, 2007). Although the prognos- moved to new pastures at an altitude of 2,730m. From tic value of PAP measurement has been validated in 4 to 7 mo of age, calves had access to pastures ranging other species (Ghio et al., 2001), it has not been deter- in altitude from 2,730 m to approximately 3,500 m. mined in cattle. Further, to our knowledge, there has Calves were sampled twice at approximately 3 mo (86 been no scientific validation that the identification and ± 7 d) and 7 mo (197 ± 6 d) of age. Every second calf removal of individuals with mPAP 45 mmHg from into the chute was sampled. Fifty-one of the 58 calves the breeding stock will reduce the incidence of RHF sampled at 3 mo of age survived to 7 mo of age and in the calf crop. Therefore, it is important to define the were resampled. utility of mPAP to predict calf survival. The dams were given prebreeding and precalving To date, selection strategies to reduce calf death vaccinations offering protection against viral agents loss from RHF have focused on mPAP, reflecting the of respiratory disease. Calves were vaccinated against static resistance to ventricular afterload attributable to the same respiratory pathogens at 4 to 8 wk of age and distal pulmonary arterial remodeling (Alexander and 2 to 4 wk before weaning. All calves were sired by Jensen, 1963a,b; Holt and Callan, 2007). By contrast, bulls with a mPAP < 42 mmHg at 2,440 m. A hormonal the dynamic, pulsatile component of pulmonary ar- growth promotant (Synovex C; Zoetis, Madison, NJ) terial blood flow has largely been ignored; however, containing 100 mg progesterone and 10 mg estradiol more recent evidence from human studies suggests benzoate was administered to all calves in the herd that disturbed flow pulsatility arising from pulmonary at 2,730 m when approximately 8 wk old. All calves arterial stiffening may contribute to the development were clinically healthy when sampled at 3 mo of age. of RHF (Schäfer et al., 2016). If so, indirect measures The Colorado State University Animal Care and Use of pulmonary arterial stiffening, such as systolic pul- Committee approved the study before any animals monary arterial pressure (sPAP) and pulmonary arte- were sampled (protocol 09–1524A). rial pulse pressure, may also serve as valuable indica- tors of RHF susceptibility in cattle. Pulmonary Arterial Pressure (PAP) Testing It has also been suggested that the small cardio- pulmonary system of domestic cattle relative to body Holt and Callan (2007) provide a full description of size and oxygen requirements is a risk factor for RHF the equipment, materials, and facilities required for PAP (Veit and Farrell, 1978). A reduction in the rate of testing. In brief, saline-filled, polyethylene catheter tub- oxygen delivery relative to metabolic demand would ing (external and internal diameter of 17 and 12 mm, re- manifest physiologically as an increased systemic spectively) was fed through a 12-gauge, 8.9-cm needle oxygen extraction fraction (sOEF), that is, the propor- that was inserted into the jugular vein. The position of tion of oxygen within arterial blood that is extracted the catheter tip within the vascular system was deter- by the peripheral tissues (McLellan and Walsh, 2004). mined from the pressure waveform on the oscilloscope If the rate of oxygen delivery is reduced, sOEF must (BM5Vet; Bionet America, Inc., Tustin, CA). The jugu- increase to maintain aerobic metabolism at steady lar vein, right atrium, right ventricle, and pulmonary ar- state. Consequently, calves that have a high sOEF (> tery have distinct pressure waveforms (Holt and Callan, 0.30) may be at greater risk of decompensated heart 2007). Once inside the pulmonary artery, mean, systolic, failure and death because they have less physiological and diastolic pressures were recorded after the pressure reserve to respond to the increased cardiac workload waveforms stabilized. Pulse pressure was calculated as associated with increasing mPAP. the absolute difference between systolic and diastolic The purposes of this study were to evaluate mean, pressures. Calves were moved to a small pen enclosure systolic, diastolic pulmonary arterial pressures, pulmo- for at least 20 min before sampling. nary arterial pulse pressures, and sOEF as risk factors for the survival of suckling calves to 7 mo of age on 1 ranch Blood-Gas Analyses located at an altitude of 2,730 m in Colorado, USA. Approximately, 2.5 mL of blood aliquots of arte- MATERIALS AND METHODS rial and mixed venous blood were collected in 3-mL syringes. Arterial blood was collected from the coc- Study Site and Cattle cygeal artery using a 22-gauge, 2.54-cm (1”) hypoder- The 58 calves (30 heifers and 28 steers) included mic needle. The bovine coccygeal artery is a suitable in the study were a composite of Red Angus, Hereford, source for blood-gas analysis (Collie, 1991; Nagy et Gelbvieh, and Simmental breeds. Calves were born to al., 2002). Mixed venous blood was collected via the primiparous heifers on a commercial cow-calf ranch catheter used for pulmonary arterial pressure mea- Pulmonary arterial pressure and calf survival ◊ surement. Syringes used for arterial blood gas collec- version 12; Stata Corporation, College Station, TX). tion were heparinized with approximately 0.25 mL of Only 7 of the 58 calves in the cohort were presumed to sodium heparin (1,000 IU/ml). The plunger of each have died; consequently, median values are provided syringe was pulled back to the 3-mL mark coating the as measures of central tendency. Further, Mann–Whit- inner chamber surface with heparin. Heparin was then ney U tests were used to determine if the pulmonary expelled so that only the needle hub contained heparin. arterial pressures or sOEF of the 3 mo old calves dif- The sample was discarded if during collection the flow fered according to 7 mo survival status.
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