Assessment of energy expenditure by daily heart rate measurement—validation with energy accretion in sheep

Livestock Production Science 78 (2002) 99–105 www.elsevier.com / locate / livprodsci

Assessment of energy expenditure by daily heart rate measurement—validation with energy accretion in sheep a, b c c A. Arieli *, A. Kalouti , Y. Aharoni , A. Brosh a

Department of Animal Science, Faculty of Agriculture, Hebrew University of Jerusalem, P.O. Box 12, Rehovot 76100, Israel b Wageningen Agricultural University, Wageningen, The Netherlands c Agricultural Research Organization, Ramat Yishay, Israel Received 10 July 2001; received in revised form 2 April 2002; accepted 3 May 2002

Abstract An experiment was conducted in sheep to test the validity of the heart rate method as a tool for determining energy expenditure. A comparison was made between assessments of energy expenditure by this method and the comparative slaughter technique. Animals were kept individually in metabolic cages and were fed ad libitum. One group was fed a high-energy diet, comprised of 75% concentrates and 25% alfalfa hay cubes (C diet) for 84 d. A second group was fed 25% concentrates and 75% of alfalfa hay cubes (R diet) for a 42 d, and then switched to the C diet for 42 d. The third group received the R diet cubes for 84 d. Body composition was determined in four animals at the start of the experiment, and in 12 animals at its termination. The entire experimental period was divided into four sub-periods. For each diet, metabolizability and average heart rate were determined for 3 consecutive days. Individual oxygen consumption was determined by the mask technique and the ratio of oxygen consumption to heart rate, the O2 pulse (O2P), was established for each sub-period. The average ratio of energy expenditure values computed from the product of daily heart rate times O2P to those obtained from the difference between metabolizable energy intake and energy accretion derived from the comparative slaughter technique, was 1.067. We concluded that the monitoring of heart rate combined with a repeatable calibration of individual O2P is a reliable and useful method for determining energy expenditure in ruminants.  2002 Elsevier Science B.V. All rights reserved. Keywords: Energy expenditure; Sheep physiology; Heart-rate monitoring; Oxygen pulse

1. Introduction Energy expenditure (EE) is a major element in overall energy budget of growing animals. It can be *Corresponding author. Tel.: 1972-8-948-9203; fax: 1972-8948-9867. E-mail address: [email protected] (A. Arieli).

assessed by indirect calorimetry, generally measured from respiration balance, or by difference calculations based on the combined balance of metabolizable energy intake (MEI) and bodily energy accretion (Blaxter, 1989). Due to the limitations to using data obtained in chambers to describe the energy budget of free-ranging animals (Close, 1990), other techniques need to be explored. The finding of a high

0301-6226 / 02 / $ – see front matter  2002 Elsevier Science B.V. All rights reserved. PII: S0301-6226( 02 )00094-5

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correlation between EE and heart rate (HR) in man (Andrews, 1971) and animals (Webster, 1967), and the relative simplicity of the latter monitoring method, make continuous monitoring of HR a potential technique for determining EE under free-range conditions. The method involves a calibration step in which HR and EE (usually be the mask method) are monitored simultaneously, and a daily measurement of HR is taken, to be ultimately translated into EE values. This technique has been used in exercising and resting humans (Ceesay et al., 1989; Livingstone, 1997) and livestock (Richards and Lawrence, 1984; Purwanto et al., 1990; Zerbini et al., 1992; Rometsch et al., 1997; Brosh et al., 1998). From experience gathered with the HR method, it has been recommended that each individual be calibrated against its own respiratory parameters. Some researchers have recommended using a regression equation to describe the relationships between EE and HR (Ceesay et al., 1989; Livingstone, 1997; Rometsch et al., 1997). On the other hand for resting livestock, Brosh et al. (1998) found that, for individuals, the O 2 pulse (O2P), i.e., the ratio of oxygen consumption to HR is a quite constant factor, indicating that the O2P can be used as a parameter for calculating the daily EE in free-ranging animals. To date, a direct comparison of HR-based EE values in resting animals with EE values obtained by other methods has not been conducted. The present trial is the first part in a series of larger experimental setup in which environmental effects of EE of free range cattle and dairy cattle are evaluated. In the present experiment, the EE in sheep kept indoor and consuming high and low energy density diets was determined. In these animals the assessment of EE by the HR method was compared with EE estimated by the difference of ME intake and energy accretion. Three different feeding methods were imposed in order to increase the variability of the results and consequently the range of validity of the method.

2. Materials and methods The experiment was conducted from June to August 2000. Sixteen Assaff cross-bred lambs (initial body weight 5063.7 kg) were used. Four of the

animals were slaughtered at the beginning of the experiment and their body composition analyzed. The remaining 12 sheep were housed for 84 d in a ventilated barn. The ranges of air temperature, relative humidity and thermal humidity index (THI) during the experiment were, respectively, 24 to 31 8C, 62 to 77%, and 74 to 81. Light was turned on from 06.00 to 19.00 h. Lambs were kept in metabolic cages. Feed was provided ad libitum, allowing 7% refusals, and presented in two meals: 70% of the daily allowance was provided at 08.00 h and the rest was given at 16.00 h. Refusals were weighed daily before the morning meal, and sub-samples were stored at 2 20 8C for analysis. Water was always available. The lambs were divided according to body weight into three groups. Dietary treatments differed in energy concentration: group H was fed a high-energy diet, comprised of 75% concentrates and 25% alfalfa hay cubes (diet C) during the entire experiment (84 d). Group M was fed 25% concentrates and 75% alfalfa hay cubes (diet R) for a period of 42 d, and then switched to diet C for the rest of the experimental period. Group L received the R diet during the entire experimental period. The ME concentrations were 11.7 and 8.7 MJ / kg of DM for the concentrates and hay, respectively. The experimental period was comprised of four equal sub-periods of 21 d. Intake was measured daily. On days 8 to 14 of each sub-period, daily feces output was measured. Feces were collected, weighed, and kept at 2 20 8C for later analysis. On days 15 to 17 of each sub-period HR was monitored continuously with data loggers (DL, Dansoft, Rehovot, Israel, www.dansoft.net) fastened to a harness attached to the thorax behind the fore legs. This device was programmed to record mean HR (mean of three 10-s measurements) at 15-min intervals, from which 12 means for every 2 h interval were taken to represent the diurnal HR pattern. Oxygen consumption (VO 2 ) was measured on day 17, simultaneously with HR monitoring. The simultaneous measurements were conducted for approximately 15 min, in the morning, between 10.00 and 13.00 h. Data were monitored continuously and recorded at a rate of eight measurements per minute. An open-circuit mask system for measuring VO 2 (Taylor et al., 1982) was used for the respiratory gas

A. Arieli et al. / Livestock Production Science 78 (2002) 99–105

measurements. To reduce stressed related reading, the recording of HR and VO 2 has started when animal’s HR has returned to the normal level obtained previously (on days 15 to 17). For each measuring day, the N 2 recovery of the system was assessed gravimetrically by injecting 40 g nitrogen into the mask (McLean and Tobin, 1990). Reduction of O 2 in mask air was similar to that obtained by sheep respiration (i.e., about 1% oxygen). The amount of N 2 consumed was calculated as the reduction in O 2 multiplied by air flow (about 60 l / min) and time, and standardized to STP. The calculated amount was compared to the weighted N 2 consumption, to produce a correction factor. Usually the S.E. of the two correction replications (performed at the start and end of monitoring animals respiration) was in the range of 0.5% or less. The variability of O2P was tested in seven of the 12 lambs in this experiment. Six measurements were performed at mean hours 02.15; 07.21; 10.53; 13.43; 19.10; 22.47 during a 24-h period. Mean HR values in the correspondent times were 95.4; 88.3; 101.4; 99.5; 107.8; 97.8, S.E.D. 5 3.81 (P , 0.001). Mean O2P values in the correspondent times were 0.255; 0.255; 0.266; 0.243; 0.241; 0.262, S.E.D. 5 0.015 (P 5 0.51), indicating constant relation of VO2 to HR during the day. Animals were slaughtered in an abattoir and carcasses were separated into two equal halves. One half was dissected entirely into the following sections: intestine, stomach, liver, heart, lungs, legs and rib muscles, ribs and leg bones, skin and blood. Each section was weighed, and representative samples were stored at 2 20 8C for later analysis. Each of the bodily sections were analyzed for DM, ash, crude protein and ether extract. Feeds and feces samples were dried at 55 o C for 48 h, than ground to pass through a 2-mm screen. The DM and OM contents were determined following drying at 105 8C overnight or ashing at 600 8C for 3.5 h. Content of CP was determined by the Kjeldahl method in a Tecator Kjeltec auto 1030 analyzer. Ether extract was determined according to the Association of Official Analytical Chemists (AOAC) (1990). Neutral detergent fiber (NDF) in feed samples was determined according to van Soest et al. (1991)). Gross energy (GE) was determined with a Parr semi-adiabatic calorimeter, Model 1261.

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The metabolizable energy in feedstuffs was calculated from digestible energy (DE) using the National Research Council (NRC) (2001) equation: ME (kJ / kg of DM) 5 DE*1.01 2 1.883 (kJ / kg of DM) For each lamb in each sub-period, the oxygen consumed per heartbeat was calculated from the simultaneous measurements of HR and VO 2 , according to Brosh et al. (1998), and the O2P was computed. Animal EE (kJ / kg 0.75 per day) was calculated by multiplying the O2P by the total number of heartbeats per day, assuming 20.47 kJ / l of O 2 consumed (McLean and Tobin, 1990). Energy retention (ER) was calculated from the difference between initial and final body energy content. Initial content was calculated as the product of initial live body weight and initial mean body energy density, determined in the four lambs that were slaughtered at the beginning of the experiment. Final body energy content was calculated from the product of the final live body weight by body energy density, determined in animals slaughtered at the end of the experiment. These respective carcass sections were composited into total live weight, and energy content was calculated assuming an energy density of 23.5 kJ / g of protein and 39.3 kJ / g of fat (Webster, 1983). Results are presented as means and their respective S.E.s. Means were compared by contrast t-tests. Significance was declared at P,0.05 unless otherwise indicated.

3. Results and discussion The mean ad libitum intakes of DM, DE and ME were 89 g / kg 0.75 per day (S.E. 2.3), 989 kJ / kg 0.75 per day (S.E. 26.4), and 839 kJ / kg 0.75 per day (S.E. 21.1). The range of ME intake was 770 to 960 kJ / kg 0.75 per day (see Table 1), in accord with our goal of inducing a large range of ME intake in order to facilitate variation in energy expenditure. To determine the dietary energy metabolizability and the animal’s MEI, we used the NRC (2001) equation, which relates ME to DE concentration. According to that equation the resultant ME:DE

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Table 1 ME intake (MEI, kJ / kg 0.75 per day), energy retention (ER, kJ / kg 0.75 per day), estimated energy expenditure by the comparative slaughter technique (EECST, kJ / kg 0.75 per day), or estimated by the HR method (EEHR, kJ / kg 0.75 per day), and EE predictability Sheep

Treatment a

MEI

ERb

EECST c

EEHRd

EE predictability e

1 2 3 4 5 6 7 8 9 10 11 12

High High High High Medium Medium Medium Medium Low Low Low Low

855 786 944 847 770 837 851 959 853 884 793 693

173 142 221 242 303 172 234 224 116 199 151 100

682 644 723 604 467 665 616 735 737 685 643 593

651 801 814 619 493 801 633 759 631 710 747 644

0.954 1.244 1.126 1.024 1.056 1.205 1.026 1.033 0.856 1.036 1.163 1.086

839 21.1

190 16.9

650 21.8

692 27.9

1.067 0.031

Mean S.E. a

Dietary treatments: concentrate to roughage ratio of 75:25, 50:50 and 25:75 in high, medium, and low, respectively. Energy retention determined by the comparative slaughter technique. c Calculated as MEI2ER. d Calculated by the HR technique. e Calculated as the ratio of EEHR / EECST. b

ratios for the C and R diets were 0.858 and 0.834, respectively. Those values were slightly higher than that of 0.81 proposed by the Ministry of Agriculture, Fisheries and Food (MAFF) (1984). Thus, some bias could be associated with the lamb’s predicted MEI. However, such errors appear to be small, and did not substantially affect the predictions of EE. Means (S.E.) of live weight, protein, fat and energy in sheep slaughtered at the beginning of the experiment were 47.8 (2.75) kg, 8.4 (0.3) kg, 3.9 (0.6) kg, and 350 (30.5) MJ, respectively. The average energy concentration in these sheep, 7.32 MJ / kg of live weight, was assumed to represent the initial energy density of each of the other sheep that took part in the metabolic experiment. Mean (S.E.) of final weight, and accretion of protein and fat during the 84-d study were 64.0 (1.2), 3.4 (0.44) and 6.6 (0.83) kg, respectively. When expressed per metabolic body weight, mean energy accretion was 190 kJ / kg 0.75 per day (S.E. 16.9). As depicted in Table 1, the mean predicted EE, from the difference between ME intake and energy accretion was 650 kJ / kg 0.75 per day (S.E. 21.8). The HR data showed a diurnal pattern: values

varied between 78 beats / min at night to 102 beats / min during the day in R-fed, and between 95 and 105 beats / min in their C-fed counterparts (Fig. 1a). At midnight, when the HR of C-diet sheep was higher by about 15%, than that of compared to R-diet sheep. The daily HR curves of the two diets tended to coincide during the day. Similar trends in daily HR pattern have been observed by Purwanto et al. (1990), who compared metabolic responses in dry and lactating cows kept indoors. Much larger diet induced differences in HR have been found in growing heifers kept in an open shed (Brosh et al., 1998). In those animals, HR with R and C diets varied between 40 and 60 beats / min, and 80 and 110 beats / min, respectively, while MEI was 600 and 1200 kJ / kg 0.75 per day, respectively. It can thus be concluded that the level of dietary energy intake and the animals’ rearing (indoor vs. outdoor) conditions can have a profound effect on the HR response to dietary energy intake modifications. The O2P averaged 0.250 ml O 2 / beat kg 0.75 and was not affected by the diet (data not shown). The average O2P level found in this study, is similar to that reported for heifers (Brosh et al., 1998), where similar to our study the O2P was not affected by

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Fig. 1. (a) Daily pattern of heart rate in lambs fed concentrates (circles) and roughage (triangles) diets. (b) Daily pattern of energy expenditure in lambs fed concentrates (circles) and roughage (triangles) diets.

dietary treatment. Higher O2P values of about 0.4 ml O 2 / beat kg 0.75 have been reported for dry dairy cows kept at 2400 m in Ethiopia (Zerbini et al., 1992), and in heat-stressed lactating Israeli dairy cows (Aharoni et al., unpublished). According to Purwanto et al. (1990) the O2P is 0.44 and 0.35 ml O 2 / beat kg 0.75 for lactating and dry dairy cows, respectively. The described variation in O2P appears to reflect its

dynamics in resting animals, as affected by the balance between the physiological needs for oxygen delivery and heat dissipation. The relative significance of these two circulatory system functions may vary according to the animal’s production level and its thermoregulatory demands. The accuracy of the HR recording method relies mainly on the individual calibration of the EE:HR

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relationship (Morio et al., 1997). Based on regression analysis of this relationship in humans it has been suggested (Blackburn and Calloway, 1985) that the prediction of EE from HR is unreliable at low HR where resting and exercising HR values may overlap. In cattle like humans, during exercise EE increases more than HR (Richards and Lawrence, 1984; Rometsch et al., 1997). This apparent increase in O2P results from increased oxygen extraction in body tissues, and from the arterio–venous oxygen difference (Eckert et al., 1988). Nevertheless, in resting heifers the O2P has been found to be relatively constant for individual animals and diets and to be an appropriate parameter for estimating EE from HR of non-exercising animals (Brosh et al., 1998). The constancy of the O2P during the 24-h cycle was further studied in growing sheep and calves (Aharoni et al., unpublished). The O2P of growing animals did not change during the 24-h cycle or in response to increased THI up to 85. It can thus be concluded that excluding the prediction of EE in exercising subjects, where regressing EE vs. HR can provide an accurate calibrating procedure, for resting and growing animals the O2P ratio may be a reasonable parameter for predicting EE for long-term energy budget calculations. Based on HR and O2P data, a clear diurnal pattern of EE with both diets was observed (Fig. 1b). The EE varied between 600 kJ / kg 0.75 per day during the night to 770 kJ / kg 0.75 per day during the day in R-fed lambs, and between 670 kJ / kg 0.75 per day and 770 kJ / kg 0.75 per day in C-fed lambs. Using similar approach in heifers, a diurnal EE pattern has been found by Purwanto et al. (1990) and Brosh et al. (1998). Likewise, Shinde et al. (1998) described, in stall-fed rams, an increase in EE between 06.00 and 14.00 h. These diurnal changes in EE apparently reflect the animal’s feeding activity and assimilation of dietary energy intake. The main aim of the current study was to evaluate the precision of the HR technique as a tool for predicting EE in resting ruminants. The appraisal was based on comparing the EE-based HR data with energy accretion EE-based calculations. When the ratio of EE estimate by the HR method to the EE estimated from the difference between MEI and ER was computed for each animal, the average coeffi-

cient was 1.067 (S.E. 0.031, see Table 1). The 6.7% difference in EE between the two methods may reflect the overall experimental errors in the evaluation of energy metabolizability, in the comparative slaughter method, and in the EE prediction by the HR method (errors in HR and in O2P). Our finding is in agreement with Mundia and Yamamoto (1997) who reported that in heifers, the average daily estimate of EE based on HR readings is similar to direct measurements of EE. Referring to various methods of evaluating of energy expenditure, Blaxter (1989) concluded that when a comparison is made between ER measured by the respiration method and that estimated by the comparative slaughter method, one should expect a discrepancy on the order of 1% of the MEI. According to Close (1990) the degree of agreement in the estimate of heat production measured by calorimetry and the comparative slaughter procedure ranges between 22 and 10%. The EE /(MEI2ER) ratio in the present study fit into the range described by Close (1990), suggesting that the daily monitoring of HR combined with a repeatable calibration of individual O2P is a reliable and useful method for determining EE in ruminants.

Acknowledgements This research was supported by the US–Israel Binational Agricultural Research and Development Fund, project No. IS-2887-97R.

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