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Alteration of metabolic profiles in young and adult Murrah buffaloes exposed

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 International Journal of Applied Animal Sciences, Volume 1(1):23-29 ISSN 1925-3869 (online)
©International Network for Scientific & Industrial Information

Research Article
Alteration of metabolic profiles in young and adult
Murrah buffaloes exposed to acute heat stress
N. Haque1*, A. Ludri1, S. A. Hossain2 and M. Ashutosh1
1
Dairy Cattle Physiology Division, 2Dairy Cattle Nutrition Division, National Dairy Research Institute
Karnal, Haryana- 132001, India
*Corresponding author: [email protected]

ABSTRACT
To ascertain the comparative effect of acute heat stress on metabolic profiles, twelve young and adult Murrah
buffaloes (n=6) were exposed to 22°, 40°, 42° and 45°C for 4 h duration in a climatic chamber. Physiological
parameters like rectal temperature (RT) and respiratory rate (RR) were monitored to assess magnitude of stress in
the animals due to thermal exposure. A significant increase (P<0.001) of the RT and RR in both young and adult
buffaloes was observed after exposure to 40°, 42° and 45°C for 4 h as compared to thermoneutral temperature
(22°C). Blood samples were drawn in sterile vacutainer tubes containing ethylene diamine tetra acetic acid
(EDTA -1mg/ml) anticoagulant from jugular vein puncture. Plasma was separated immediately and stored
at – 20°C for biochemical assays. Acute heat exposure suppressed the thyroid hormone activity. Cortisol
concentration in blood plasma showed increasing trend with enhancement of temperature. Plasma insulin decreased
while plasma NEFA (non esterified fatty acid) concentration increased (P<0.001) with exposure to elevated
temperature. The intensity of changes in metabolic hormones was more pronounced in youngs compared to adults
indicating youngs’ more susceptibility to heat stress. This study concludes that, acute heat stress evokes a series of
drastic changes in the animal's biological functions including enzymatic reactions, hormonal secretions and blood
metabolites.

Key words: Murrah buffaloes, heat stress, physiological responses, metabolic hormones
Int. J. Appl. Anim. Sci. 1(1):23-29

INTRODUCTION animal is greater than its capacity to lose heat

The current range of the buffalo extends as (Wagner, 2001), a portion of the metabolizable
far as latitude 45°N in to 40°S line latitude (Marai energy typically used for production must be diverted
and Habbeb, 2010). Buffaloes are found only in to assure thermal balance. Therefore, selection for
certain regions in the world; principally Asia, some tolerance to environmental stress has traditionally
Mediterranean countries, some countries in eastern resulted in reduced productivity (Smith et al., 2000).
Europe and in many countries in Latin America. The primary factors that cause heat stress in dairy
Although such regions are widely different in the animals are high environmental temperatures and
geographical conditions, no other domestic animal relative humidity (West, 2003). In addition, radiant
can thrive and be similarly useful and economical. energy from the sun contributes to stress if animals
India has about 102.4 million buffaloes which are not properly shaded.
represents 56.5 percent of the world buffalo Thermal stress is a unique and complex
population. India is the first country in the world for phenomenon that brings about numerous challenges
number of buffaloes and milk production (about 55 beyond the animals baseline homeostatic mechanism
million tons) and possesses the best milch breeds causing alterations of the normal physiological
(FAO, 2010). Among these, Indian Murrah is the mechanisms thus elicits a stressful response. Thermal
most important and well-known buffalo breed in the stress is a concern for all livestock production
world. Like all other mammals buffaloes are systems and its effects have been studied because of
homeotherms i.e. they maintain a constant body the profound and readily apparent negative impact on
temperature by constantly regulating peripheral and production, health and it causes even mortality.
internal body temperature with assistance of Exposure to high ambient temperature is the major
cutaneous sensors and internal temperature sensors constraint on buffalo productivity in hot climatic
(located in the hypothalamus) along with integration areas. An increase in body temperature of around
of the endocrine system. When the heat load of an 1.0°C may result in detectable, deleterious effects on

23
 Int. J. Appl. Anim. Sci. 1(1):23-29

metabolism, tissue integrity and a significant 42°C and Twb = 36°C) inside the climatic chamber.
depression in production (McDowell et al., 1976; After exposure of animals for 4 hours (h) at the above
Shebaita and El-Banna, 1982). mentioned temperature, blood was collected for
When animals are exposed to stress for long biochemical assay. The rectal temperature (RT) was
duration (chronic stress), they try to acclimatize in recorded with a mercury in glass clinical
the adverse condition. Acclimation involves thermometer, inserted 3 inches in the rectum for at
phenotypic responses to environmental changes, least 2 minutes and the rectal mucosa was in contact
which are reflected in hormonal signals and also in with the bulb of the thermometer. Respiration rate
alterations in target tissue responsiveness to hormonal (RR) of animals was recorded by observing flank
stimuli (Collier et al., 2006). The time required for movement and one inward and outward movement
acclimation varies according to tissue types, and was counted as one respiration and recorded/min.
ranges from a few days to several weeks; for Three-day interval was maintained for the exposed
example, changes in metabolism in response to heat animals in between two temperature treatments to
stress occur over a few days (Collier et al., 2008). nullify the effect of earlier acute heat stress. Blood
However, this picture does not cover all situations; samples were also collected from animals in the
some external environmental stresses, such as month of March when the average environmental
dehydration (Silanikove, 1994) and acute heat stress temperature was 22°C, which is considered to be the
(Silanikove, 2000), may very quickly (within 24 to 48 temperature of thermoneutral environment for
h) take animals beyond their current acclimatized- tropical animals and used as control group. Blood
adaptive range, which necessitates the induction of samples were drawn in sterile vacutainer tubes
emergency physiological responses in order to avoid containing ethylene diamine tetra acetic acid (EDTA
sudden death. Such changes result in impairment of -1mg/ml) anticoagulant from jugular vein puncture
productive and reproductive performance of animals posing minimum disturbances. Immediately the tubes
and buffaloes in particular (Habeeb et al., 1997). were brought to the laboratory for further processing
Therefore, present study was undertaken to measure for plasma separation by centrifugation of the blood
the comparative influence of heat stress on sample at 210 g for 30 minutes. Separated plasma
biochemical parameters at different temperatures in was stored at – 20°C till use.
young and adult buffaloes. This information is likely
to further help to minimize heat stress in Murrah Estimation of biochemical parameters
buffaloes. Estimation of plasma cortisol was done by
DEMEDITEC Cortisol Enzyme Immunoassay Kit
MATERIALS AND METHODS (Kiel, Germany) by ELISA method. Plasma levels of
thyroxine (T4), triiodothyronine (T3) andinsulin were
Selection, Feeding and Maintenance of Animals estimated by radioimmunoassay methodusing RIA kits
Two groups of healthy Murrah buffaloes, as per the standard procedure specified along with kits
young (1-2 yrs) and adult (3-4 yrs) were selected for (supplied by Board of Radiation and Isotope
the experiment comprising six animals in each group. Technology, Mumbai, India).Samples were analyzed
The experimental animals were maintained as per for NEFA semi-automatically using commercial
standard feeding and management practices followed photometric assays.
at National Dairy Research Institute, Karnal, India.
This consists of feeding ad libitum roughages and Statistical analysis
water; concentrates mixture as per Kearl (1982) All the data generated were statistically
feeding standard. Concentrate mixture consisted of analyzed by two way ANOVA using SigmaStat (11.0
mustard cake, maize, wheat bran, rice bran, mineral software package) Statistical Analysis System (Jandel
mixture and salt. The crude protein (CP) and total Scientific, San Rafael, CA, USA), according to
digestible nutrients (TDN) of diet was 12% and 60%, Snedecor and Cochran (1994). Data from different
respectively. experiments are presented as mean ± SE. Differences
with probabilities P <0.05 were considered
Climatic chamber experiment and sample significant. After testing for normality and equal
collection variance, two-way ANOVA followed by all pair wise
A climatic chamber (22'26" x 10'10" x 8') multiple comparison procedures (Holm-Sidak
insulated with thermostatically fitted heat convector method) for variable were employed to determine the
was used for exposing animals. The temperature of difference in the different treatment temperature
chamber was maintained at 40.0 ± 1.0°C, 42.0 ± (22°C, 40°C, 42°C and 45°C) and two age groups
1.0°C and 45.0 ± 1.0°C prior to experiment. The viz., young and adult buffaloes as well as temperature
average relative humidity was 50% (average Tdb = x age interaction.

24
 Int. J. Appl. Anim. Sci. 1(1):23-29

RESULTS AND DISCUSSION dissipation of heat from the skin surface.

Consequently, the internal heat gradient between the
Physiological responses rectal and skin temperature is narrowed, and the
Effect of acute heat stress on rectal temperature: external heat gradient between the skin and the
The rectal temperatures of experimental animals are surrounding air is widened, thus promoting body-heat
depicted graphically in Fig 1. There was significant dissipation from the skin surface.
increase (P<0.05) in rectal temperature at 40°, 42°
and 45°C groups as compared to 22°C in both young Effect of acute heat stress on respiration rate
and adult buffaloes. On comparison of two age (counts/ minute): The respiration rate was
groups, it was found that only at 22°C, rectal statistically different (P<0.05) with each other at all
temperature was significantly higher (P<0.05) in the temperatures in both young and adult (Fig 2). But
young buffaloes whereas at other temperatures, it was in adult animals, at 42°C and 45°C, the respiration
statistically similar in both groups. rate was statistically similar. In different age group, it
was found that there was no significant difference
(P<0.05) in respiration rate at the above temperatures
except in case of 45°C, significant higher (P<0.05)
40.5
respiration rate was observed in young animals than
39.5 adults. The increase in respiration rate with the
Rectal temp.(ºC)

38.5
increasing temperature may be due to the more
demand of oxygen by the tissues in stressful
37.5
condition. The results of physiological responses are
36.5 in agreement with the observations of Koga et al.
35.5 (2004), Sevegnani et al. (2007), Thanh and Chang
(2007), Gudev et al. (2007) and Lallawmkimi (2009).
34.5
22ᴼC 40ᴼC 42ᴼC 45ᴼC
Temperature Metabolic profiles
Young Adult Effect of acute heat stress on plasma cortisol
concentration: The plasma cortisol concentration
Figure 1. Rectal temperature (°C) in young and adult Murrah was statistically higher (P<0.05) at 40°, 42° and 45°C
buffaloes exposed to different temperatures as compared to 22°C temperature in young as well as
Bars indicate ±SE (Standard Error). Significance of effects for age, adult animals (Table 1). The results showed an
temp, age x temp. interaction P<0.001 increasing trend with increase in temperature,
however, the concentrations did not differed at 40°,
42° and 45°C. The cortisol concentrations were also
100 statistically similar in both age groups which
indicated that age has no effect on plasma cortisol
level. The present findings are similar to those
Respiration rate (counts/min)

80

reported by Zia-Ur-Rahman et al. (1997), Nessim

60
(2004), Dhami et al. (2006), Habeeb et al. (2007) and
40 Meghad et al. (2008).
Activation of the hypothalamic–pituitary–
20 adrenal axis and the consequent increase in plasma
glucocorticoid concentrations are perhaps two of the
0
22ᴼC 40ᴼC 42ᴼC 45ᴼC most important responses of the animals to climatic
Temperature stressful conditions. Adrenal corticoids, mainly
Young Adult cortisol, elicit physiological adjustments which
enable animals to tolerate stressful conditions
Figure 2. Respiration rate (counts/min) in young and adult Murrah (Christison and Johnson, 1972). Concentration of
buffaloes exposed to different temperatures cortisol is altered by acute and chronic heat exposure
Bars indicate ±SE (Standard Error). Significance of effects for age
P = 0.042; Significance of effects for temp, age x temp. interaction and by changes in photoperiod (Alvarez and Johnson,
P<0.001 1973). Acute and chronic thermal stress shows
differing responses on glucocorticoid concentrations,
being elevated in former but not in later (Collier et
The great changes in RT are induced in al., 1982). The initial rise in plasma glucocorticoids is
buffaloes by a marked increase in blood flow from due to activation of the adrenocorticotropin (ACTH)
the body core to the surface, which accelerates releasing mechanism in the hypothalamus by

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 International Journal of Applied Animal Sciences, Volume 1(1):23-29 ISSN 1925-3869 (online)
©International Network for Scientific & Industrial Information

Table 1. Comparison of metabolic profiles in young and adult Murrah buffaloes exposed to different temperatures

Temperature (°C)
Parameters Young Adult
22°C 40°C 42°C 45°C 22°C 40°C 42°C 45°C
ax bx bx bx ax bx bx
Cortisol (ng/ml) 7.77 12.96 12.99 16.12 7.55 12.29 13.75 14.87bx
±0.84 ±0.99 ±0.98 ±1.65 ±0.97 ±0.84 ±1.44 ±1.69
Insulin 9.63by 7.02ay 6.47ay 6.42ay 7.92bx 4.84ax 5.13ax 4.91ax
(µU/ ml) ±0.19 ±0.29 ±0.37 ±0.31 ±0.28 ±0.34 ±0.31 ±0.24
T3 1.45ay 1.26ax 1.18ax 1.12ax 1.10ax 0.99ax 0.96ax 0.91ax
(ng/ml) ±0.14 ±0.11 ±0.12 ±0.10 ±0.08 ±0.08 ±0.05 ±0.10
T4 5.78by 5.16ay 4.99ay 4.93ay 4.96bx 3.81ax 3.78ax 3.35ax
(ng/ml) ±0.23 ±0.18 ±0.15 ±0.19 ±0.11 ±0.15 ±0.11 ±0.13

NEFA (mmol/l) 0.21ax 0.35abx 0.32abx 0.43bx 0.16ax 0.27abx 0.29abx 0.35bx
±0.03 ±0.06 ±0.03 ±0.05 ±0.02 ±0.04 ±0.03 ±0.06
Means (±SE) with different superscripts in rows for a parameter differ significantly (P<0.05)
a, b
indicate significant difference between temperature; x,y indicate significant difference between age group

thermo receptors of the skin (Chowers et al., 1966), did not detect significant difference between the
whereas the later decline to normal, inspite of stressed and unstressed animals in plasma insulin
continuing heat stimulus, indicates a negative concentration or reported an increase in insulin levels
glucocorticoid feedback and a decrease in the during exposure to elevated temperature (Chaiyabuter
glucocorticoid binding transortin (Lindner, 1964). et al., 1987).
The increase of plasma cortisol level during acute Decrease of insulin level with increasing
heat stress is attributed to the fact that glucocorticoid temperature may be due to the decrease in heat
hormones have hyperglycemic action through the production. One classic response during heat stress is
gluconeogenesis process, thus enhancing glucose a reduction in circulating insulin coupled with a
formation in heat stressed animals. This indicates the reduction in systemic insulin sensitivity. Elevated
role of the adrenal cortex gland in adaptation to blood NEFA levels as a result of lipolysis during heat
stress. The glucocorticoids also work as vasodilators stress reduce insulin sensitivity and thus decrease
to help heat loss and have stimulatory effect on muscle glucose uptake, glucose oxidation, and
proteolysis and lipolysis, hence, providing energy to hepatic gluconeogenesis, which are classically
the animal to help offset the reduction of intake referred to as the Randle effect (Randle, 1998).
(Cunningham, 2007).On the other hand,
corticotrophin-releasing hormone is known to Effect of acute heat stress on plasma thyroid
stimulate somatostatin release from the hypothalamus hormone (T3 and T4) concentration: These
which in its turn inhibits growth hormone and thyroid hormones are the primary determinants of basal
stimulating hormone secretion from the pituitary metabolic rate and play a permissive role in weight
(Riedel et al., 1998).This putative hormonal pattern gain or tissue production (Magdub et al., 1982).Acute
will help the animals to dissipate the heat, obtained heat exposure suppressed the thyroid hormone
from the environment. activity in the present study (Table 1). Plasma T3
level was comparable with each other for all the
Effect of acute heat stress on plasma insulin exposed temperature. In comparison to age group, it
concentration: In present study, plasma insulin was observed higher plasma T3 concentration in
decreased with exposure to elevated temperature in youngs only at thermoneutral temperature (22°C).A
both young and adult animals (Table 1). The plasma decrease in plasma T4 concentration (from 5.78 to
insulin concentrations were significantly decreased 4.93 in young and from 4.96 to 3.35 ng/ml in 22° and
(P<0.001) at 40°, 42° and 45°C as compared to 22°C 45°C, respectively) was found with increase in
in both young and adult animals. At 40°, 42° and temperature and it was significantly lower (P<0.05)
45°C, no difference (P<0.05) was found for insulin in both young and adult animals at 40°, 42° and 45°C
concentrations in young and adult. The insulin levels as compared to 22°C. Young Murrah buffaloes were
were higher (P<0.05) in young animals under all the found to have higher (P<0.05) T4 level if compared
temperature conditions as compared to adult. These to adults under all temperatures. Previous study also
findings are consistent with those of Sejrsen et al., indicates acute heat exposure induced decrease in
1980; Herbein et al., 1985; Habeeb, 1987; Abdel- plasma T3 and T4 in young and old buffalo calves
Samee et al., 1989. However, other researchers either (Nessim, 2004). In male Friesian calves, plasma

26
 Int. J. Appl. Anim. Sci. 1(1):23-29

concentration of T3 decreased significantly when 2002; Macrae et al., 2006).Acute stress responses
ambient temperature increased from 24 to 38 °C result in activation of the sympathetic-adrenal
during 9 h, in the climatic chamber (Habeeb et al., medullary axis and the hypothalamic–pituitary–
2001). Plasma T3 concentration decreased from 151 adrenal cortex axis. Activation of the former leads to
to 126 ng/dl when Friesian calves were exposed to an immediate rise in catecholamine concentrations,
direct solar radiation of hot summer (Yousef et al., whereas activation of the latter results in a more
1997). In lactating buffaloes, plasma T3 gradual rise in ACTH and cortisol concentrations that
concentration decreased significantly (P<0.001) by peak by 10–20 min (Lay et al., 1992). This enhances
17.2% with the increase of ambient temperature from metabolic fuel availability due to NEFA mobilisation
17.5 to 37.1 °C (Habeeb et al., 2000). due to the activation of lipase by both hormones
T3 and T4 hormones influence different (Cunningham and Klein, 2007). The reduction in
cellular processes in the body such as its calorigenic insulin action during heat stress also allows for
(heat-producing) activity that accounts for about 50% adipose lipolysis and mobilization of non-esterified
of the basal metabolic rate of normal animals. fatty acids (Bauman and Currie, 1980).Post
Decreased thyroid hormone levels during heat stress absorptive carbohydrate metabolism is also altered by
are an adaptive response and also might be an attempt the reduced insulin action with the net effect of
to reduce metabolic rate and heat production (West et reduced glucose uptake by systemic tissues (i.e.
al., 2003). Appropriate thyroid gland function and muscle and adipose). The reduced nutrient uptake
activity of thyroid hormones are considered crucial to coupled with the net release of nutrients (i.e. amino
sustain the productive performance in domestic acids and NEFA) by systemic tissues are key
animals (growth, milk, hair fiber production) and homeorhetic (an acclimated response vs. an
circulating thyroid hormones can be considered as acute/homeostatic response) mechanisms
indicators of the metabolic and nutritional status of implemented by heat stressed animals (Bauman and
the animals (Todini et al., 2007). Changes of blood Currie, 1980).
thyroid hormones concentrations are an indirect
measure of the changes in thyroid gland activity. A CONCLUSIONS
major exogenous regulator of thyroid gland activity is Exposure to elevated ambient temperature
the environmental temperature (Dickson, 1993), so an evokes a series of drastic changes in animal
inverse relationship between ambient temperature biological functions, which include disturbances in
and blood TH concentrations has been found enzymatic reactions, hormonal secretions and blood
(Starling et al., 2005). The decrease in thyroid metabolites. Improved knowledge of the functional
hormone levels during summer may be attributed to relationship between animals and their environment,
the decrease in thyroid stimulating hormone and/or understanding the mechanisms by which
the increase in glucocorticoid hormone. On the other environmentally induced hyperthermia causes
hand, long days in summer suppress the expression of decreased production and jeopardizes animal health
monodeiodinase gene in the hypothalamus of goats, and the physiological mechanisms of acclimation to
thus limiting the local bioavailability of thyroid environmental stresses will provide insight for
hormones (Yokus et al., 2006).Decline of thyroid developing new strategies to ameliorate the economic
hormones' in response to heat stress is probably an impact of heat stress and will improve the welfare
attempt to reduce metabolic heat production. and efficiency of production.

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