Influences of summer season on some biochemical andhormonal changes in crossbred cows during suckling

period

Teama F. E. I., Gad A. E.Biological Applications Department, Radioisotopes Applications Division, Nuclear Research Center, Atomic Energy

Authority, Inshas, Cairo, Egypt, P. O. 13759.Key words: suckling, urea, total protein, T4, P4, Leptin, crossbred cows.

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AbstractSeasonal variation in environmental conditions in postpartum cows may lead to

some biochemical and physiological changes which affect the productive efficiency of

farm animals. This study was conducted in the bovine farm of "Experimental farms

project" of Nuclear Research Center, Atomic Energy Authority of Egypt-Inshas to evaluate

some blood biochemical and some hormonal changes during the suckling period in

crossbred cows under winter and summer conditions. Alterations in metabolites and

metabolic hormones during the first 10 weeks postpartum in both winter and summer

during a period of suckling were analyzed on a total of 13 crossbred (Brown Swiss X

Ballade) cows (winter, n=7; summer, n=6). The blood samples were taken at 2 weeks

intervals, 5 times in each season to determine the concentrations and changes in

Glucose, urea, total cholesterol, total proteins and some hormones including leptin, T4

and progesterone (P4) under winter and summer conditions. The data indicated that:

total protein (P < 0.01), glucose (P < 0.05), leptin (p<0. 01), total cholesterol (P < 0. 01),

and T4 (P < 0. 01) concentrations had significant seasonal differences between the two

calving groups. A positive correlation coefficient was observed between leptin levels with

T4 hormone.

From the data obtained in this study, we conclude that in summer

season, calving cows, certain biochemical and hormonal levels may

2

enhance but not enough to dramatically affect circulating levels of

urea and progesterone. The positive correlation between leptin and T4

may indicate association in the rate of metabolism.

IntroductionMost long-lived species, including ruminants, exhibit

seasonal cycles of physiological functions in order to cope with

seasonal fluctuations in climate and food availability (Patkowski

et al., 2006; Duarte et al., 2010). These seasonal rhythms are

reflected on the ability of the endogenous adaptive mechanism to

react in advance to regular environmental changes associated with

the seasons (Piccione et al., 2009).

The anabolic processes during postpartum are being converted

into catabolic ones giving the priority to mammary gland over

other tissue so, that the period of early lactation is followed by

negative energy balance (Algers and Uvnäs-Moberg, 2007).

Parturition and postpartum period are followed by significant

changes in biochemical and endocrine parameters (Jain, 1993).

However, cows quickly adapt themselves to the changes of these

important parameters by means of different physiological

mechanisms. During pregnancy, maternal tissues are involved in

providing energy for reproduction processes, which may affect

blood biochemical variables besides the effect of other factors

such as breed, age, malnutrition, fetal growth, or season (Swanson

et al. 2004, Yokus et al. 2006). In the course of lactation period

blood biochemical parameters including total protein and urea are

3

important indicators of the metabolic activity in lactating

animals (Karapehlivan et al. 2007).

The drastic reproductive changes that occur at

parturition as well as the high metabolic demands required to

initiate lactation impose great stress on these animals.

Biochemical determination of serum constituents can provide

valuable information relating to nutrition, sex, age and

physiological status of the animal (Osman et al., 2003). Moreover,

it seems that these biochemical measurements are often influenced

by a change in physiological status, environmental conditions, as

also observed in goats and sheep (Piccione et al., 2009 and

Piccione et al., 2012). The same outher seems that there is a

close relationship between blood constitunts and the season.

Different biochemical and haematological changes have been

established during lactation period in dairy cows (Quiroz-Rocha et

al., 2009), sheep (Vihan and Rai, 1987), and sows (Dhabhar and

McEven, 2001) during lactation in concomitance with heat stress

exposure. On the basis of these considerations, the aim of the

present study was to assess the trends in seasonal variations in

different biochemical parameters in postpartum crossbred suckling

cows.

Materials and MethodsAnimals and Nutritional Practice:

Thirteen crossbred pregnant cows (Brown Swiss X Balady) at

the fourth parity were used in this study, they are belong to the

4

bovine farm of "Experimental farms project" of Nuclear Research

Center, Atomic Energy Authority of Egypt which is located in the

desert area of Inshas. The average body weight was 389 ± 14.2 Kg.

The cows were monitored from the second week after calving to 10

week postpartum during the suckling period. The lactating cows

suckled their calves for all the observation time.

The cows were divided into two groups according to calving

season, seven in winter time (January, February and March) and six

in summer time (July, August and September). The cows were housed

in a free-stall barn with rain force shade during day and night.

The cows were daily offered a concentrate basal diet as 2 % of the

average body weight. The concentrate consisted of 27%

undecorticated cotton seed meal, 35% wheat bran, 30% yellow corn,

5% soybean meal, 1.5% lime stone and 1.5% sodium chloride. Rice

straw was available at all time. Minerals and vitamin blocks

(Tithebarn limited, Winsford, Cheshire CW7 3PG.U.K.) were

available for all cows during all times. The animals were watered

freely ad libitum.

Blood samples and biochemical components and hormonal analysis:

Fasting blood samples were taken every 2 weeks interval,

5 times in each season. The blood from each cow was collected

directly from the jugular vein into three separate test tubes

contain heparin, sodium fluoride or without anticoagulant. The

tubes were placed in an ice box at 4°C, transferred to the

laboratory and then centrifuged for 10 min at 3000 rpm at 4°C.

Serum and plasma were separated in vials and kept at -20°C until

5

analyzed. Plasma glucose, urea, total protein and total

cholesterol were determined spectrophotometrically by using

commercial kits (Biodiagnostic, Egypt). Thyroxin (T4) level was

estimated by the radioimmunoassay (RIA) technique using solid

phase coated tubes kits provided with (I125) and progesterone (P4)

(Diagnostic Systems Laboratories, Inc. Webster, Texas, USA). The

quantitative measurement of leptin hormone in serum was performed

using ELISA kit for multispecies (DRG Diagnostics, Marburg,

Germany) according to the manufacturer’s instruction.

Table (1) showed the fortnightly changes in ambienttemperature, relative humidity (RH)% and temperature humidityindex (THI) values at mid-day in winter (January, February andMarch) and in summer months (July, August and September).

Table 1: Air temperature, Relative humidity and TemperatureHumidity Index (THI) during experiment period.

Season Week Air temp.(C°) (RH) % (THI)Winter 2

46810

2123242630

6764606149

---7578

Overallmean

24.8 60.2 76.5

Summer 246810

4038383231

4853555958

9184898281

Overallmean

35.8 54.6 85.4

Air temperature (C°) and relative humidity (%) were

measured under shade weekly during mid day using thermo-hygrometer

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(table 1). The temperature-humidity index (THI) was calculated

according to (Armstrong, 1994).

Statistical analysis: Analysis of variance was carried out by two way analysis of

variance detected using GLM procedure by SPSS (SPSS version 8 for

Windows; SPSS Inc., Chicago, IL, USA). The differences between

means were detected using Duncan's Test (1955). Results are

expressed as arithmetic mean ± standard error of mean (S.E.M.) and

significance was set up at (p≤0.05 or 0.01), respectively.

Correlation coefficients were calculated between all variables

estimated herein and each other.

Results and DiscussionA. Biochemical changes in postpartum lactating cows during

seasonal variation:

Seasonal variation including heat stress may affect on some

biochemical and physiological parameters in postpartum cows which

reflect on the reproductive performance of those animals.

One of the main biochemical parameters measured was plasma

proteins between postpartum cows calved in winter and summer

during suckling period over 10-week trial. In our data a highly

significant effect of fortnight intervals on the level of total

protein (p<0.01) was recorded. Both suckling groups had increased

7

plasma protein following parturition until week 6. After week 6,

the level was almost similar among both groups (figure 1a) and

Table (2). Our results are in agreement with what have been

observed by other authors in different studies (El Sherif and

Assad, 2001; Karapehlivan et al, 2007) and the low levels of

plasma proteins observed during the first weeks after calving

could be due to the decrease of protein level in the last

pregnancy period caused by the speed fetus muscular development.

Also, the significant increase of plasma proteins could be due to

a decrease of globulin after parturition. The higher level of

protein in winter group compared to summer one maybe due to the

high energy needed for milk synthesis in the mammary glands during

early lactation (Bremmer et al, 2000; Yokus et al, 2006).

(a) (b)

(c) (d)

Figure 1: Mean fortnightly total protein (a), Glucose (b), plasma urea level (c) and total cholesterol level (d) between winter and summer calving groups during suckling period in cows.

8

Significant changes were recorded in the level of glucose as a

result of seasonal variation and time intervals is shown in figure

(1b) and table (2) but a non significant effect was observed for

both seasonal and time interaction on glucose level following

parturition and during suckling. Due to the high demands of

energy for the process of lactation and maintenance, glucose has

shown to be depressed in the early postpartum period afterwards

levels began to increase (Vazquez-Anon et al., 1994). The higher

level of glucose observed in summer group compared to winter may

imply that it took longer for animals to recover from negative

energy balance than the winter group (Ciccioli et al, 2003).

A non significant change was observed in the level of

plasma urea nitrogen during the time between week 4 and week 6

then significant elevations were observed at week 8 and 10 for

both seasonal suckling groups as shown in figure (1c). Table (2)

shows an increased level of urea in winter (21.65 mg/dl) than in

summer (19.67 mg/dl). This increment maybe attributed to different

proteinic metabolism during lactation which was reported in

previous study in sheep and cattle (Karapehlivan et al, 2007). Our

data was indicated a significant effect of week of sampling as

indicated by a progressive increase in plasma urea nitrogen

following parturition.

Highly significant changes were recorded sue to the effect

of time and season as well as their interaction (S x T) for serum

total cholesterol level following postpartum between groups

(P<0.01). Figure (1d) shows the mean weekly values of serum total

9

cholesterol in two different seasons. No seasonal variation was

noted at the early postpartum suckling period (2, 4, and 6 weeks).

The level of cholesterol increased as lactation or suckling

advanced to reach significant values at weeks 8 and 10 (P<0.01)

especially for the winter period (Table 2). Previous studies have

shown that postpartum serum cholesterol was at its lowest

concentration in the first month of lactation, reaching its

maximum concentration at about 5 months and thereafter decreased

up to late lactation (Arave et al.,1975). Both the increased

nutrient demands of the rapidly growing fetus from the previous

pregnancy and the utilization of cholesterol for steroidogenesis

could be contributing factors to its low level in early lactation

(Arave et al., 1975). The author also reported that summer

calving cows had higher levels of total cholesterol compared to

winter calving cows. Our findings are discordant with the seasonal

differences reported by this author. Both seasonal groups had

their lowest levels of total cholesterol following parturition.

This study proved a significant effect of both time and season.

Total cholesterol levels for both suckling groups gradually

increased with the progress of time in the winter group with

greater weekly averages compared to the summer group. Reist et al

(2003) proposed that cholesterol and glucose are closely related

metabolites. Glucose has been shown to promote the uptake of

cholesterol for steroidogenesis. Although levels of glucosein the

current study were not significantly different between summer and

winter groups for season versus time interaction.

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Table 2: Mean (±SE) of serum and plasma biochemical parameters of crossbred cows (Brown Swiss X Ballady) in winter and summer duringsuckling period. Items Blood biochemical parameters

Proteing/dl

Glucosemg/dl

Urea mg/dl Cholesterolmg/dl

Season (S)Winter (overall X)

6.73± 0.07A

70.88 ±0.54B 21.65±0.59 152.20±2.24A

Summer (overall X)

6.42±0.08 B 73.21 ±0.59A 19.67±0.65 131.72±2.42B

Significance (p≤)

0.01 0.05 0.135 0.01Time of sampling (T) (weeks after calving)2nd 5.64±0.117D 67.89±0.89B 15.91±0.97D 68.79±3.69E

4th 6.15±0.116C 71.82±0.86A 18.82±0.98C 90.13±3.64D

6 6.48±0.113C 72.52±0.84A 21.0±0.91BC 144.63±3.68C

8 7.01±0.118B 74.34±0.89A 24.33±0.95AB 195.49±3.67B

10 7.44±0.115A 73.65±0.85A 25.07±0.96A 210.752±3.69A

Significance (p≤) 0.01 0.01 0.01 0.01

Interactions (S x T)Winter2nd 6.08±0.159e

f 66.77 1.45± 16.09 1.32±69.52±5.01f

4th 6.51±0.157d

e 70.05 0.86± 19.05 1.32±87.76±4.98e

6 6.66±0.155a

d 71.15 1.33± 21.37 1.33±151.80±4.96d

8 7.03±0.161a

bc73.81±1.08 24.84 1.30±

213.53±5.01b

10 7.36±0.163a

b72.62±0.78 26.91 1.31±

238.37±4.99a

Summer 2nd 5.20±0.172g 69.02 1.42±

15.72±1.43 68.06±5.41f

4th 5.78±0.171f

g73.59±1.55 18.59 1.44±

92.50±5.38g

6 6.29±0.170d

ef 73.89 1.36± 20.63 1.43±137.46±5.42d

11

8 6.99±0.172b

c 74.88 1.35± 20.16 1.42±177.47±5.41c

10 7.52±0.169a 74.69 0.72± 23.26 1.41±183.14±5.40c

Significance (p≤)

0.05 0.905 0.366 0.01Means bearing different letters (A, B and C or a, b and c) in the same column within each classification differ significantly (P≤.01 and 0.05), respectively.

B. Hormonal changes in postpartum lactating cows during seasonal

variation:

T4 and progesterone levels were estimated in the present

study to detect their changes during seasonal variation. Our data

showed that serum T4 gradually increased following parturition

after week 4 and continued to do so as suckling progressed. T4 was

highly significant for summer group than the winter group. Effect

of season, time of sampling and interaction were highly

significant (P <0.01) Table (2). The significance difference was

found between the two seasonal groups during 10-week period.

Figure (2a) depicts mean fortnight values of serum T4 between

postpartum summer and winter calving groups over the 10-week

trial. At week 10 for the summer group, there was a sharp increase

in serum T4 which was determined to be as an outline guife showing

what has happened during early lactation. During gestation,

thyroid hormones may play a role in maintenance of pregnancy and

during lactogenesis. Thyroid hormones synthesis has been shown to

increase steadily as early lactation progresses. It may be an

important hormone for normal ductal development of the mammary

glands (Vonderhaar and Greco, 1979). Additionally, higher levels

of thyroid hormones may act as a metabolic signal to the cow to

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begin resumption of ovarian activity (Reist et al., 2003). A major

exogenous regulator of thyroid gland activity is the environmental

temperature (Dickson, 1993). Being metabolic regulators as well as

calorigenic hormones, several heat stress studies have shown that

under both acute and chronic heat stress conditions, T3 and T4

synthesis were reduced and subsequently, less value were found in

milk or plasma (Johnson and Vanjonack, 1976; Magdub et al., 1982).

The dairy cow compensates for the additional environmental heat

load by reducing synthesis and secretion of these calorigenic

hormones. Other studies showed some conflicting results with no

differences found in the amount of thyroid hormone synthesis with

control versus acutely heat stressed cows (McGuire et al., 1991).

A highly significant rise of thyroid hormones was observed at the

onset of the humid warm season (June, July, and August) (Assane

and Sere, 1990). It can be supposed that an enhanced thyroid

activity during the humid warm season in such environments is

functional reaction for the animals facing the increased

availability of food, following the seasons characterized by food

shortage (quantity and quality) which is consistent with the

present study.

( a( )b( )c)

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Figure 2: mean fortnightly T4 (a), P4 (b) and Leptin (c) between winterand summer calving groups during suckling period in cows.

Although previous studies have reported conflicting

results concerning the secretion rate of progesterone (P4) under

heat stress conditions, our present data indicate a significant

effect of time (P < 0.01), but not season. Progesterone level

increased through the time of postpartum as more cows became

cyclic. Effects of season and week x season interaction were not

significant. For both groups' summer and winter calving, serum

progesterone level was at nadir levels for the first 6 weeks

postpartum. The winter group had an earlier rise in mean serum

progesterone than the summer group. This is an indication of an

earlier ovulation. Table 2 and Figure (2b) showed mean postpartum

fortnightly of serum P4 in winter and summer calving groups over

10-week trial. Postpartum changes in serum P4 are evident over

time as the cow prepares itself for another estrous cycle. By

measuring serum P4 levels, time of first ovulation can be

determined. Serum progesterone levels are nearly undetectable

until about day 30 postpartum (Taylor et al., 2003). Levels

exceeding 1 ng/mL are considered an indication for resumption of

ovulation, which is not being uncommon for the first estrous cycle

which seems to be shorter in length than normal. The present

results show a significant effect of week, indicating a secretary

pattern that changes accordingly with resumption of ovarian

cyclicity and subsequent estrous cycles, especially cow number

1and 7 in winter group, 5 and 6 in summer group. Between the two

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seasonal groups, the summer calving group had an earlier rise in

serum P4 (0.892±0.04 ng/ml) compared to the winter calving group

(0.963±0.03 ng/ml). Previous heat stress studies have reported

inconsistent results on the pattern of progesterone secretion.

Wise et al., (1988) found that lactating dairy cows subjected to

either shade or without had similar P4 concentrations. Howell et

al., (1994) reported that lactating dairy cows exposed to chronic

heat stress which would be typical of a long summer had decreased

P4 concentrations. The THI values for the end of August and

September (summer) of the current study were considered mild and

within borderline heat stress values. Although our results show no

overall significant effect of season, there was a significant

difference between the two groups at week 8 and they tended to be

a different by the end of week 6. The effects of a chronic heat

stress from several previous months of summer may lead to a

prolonged interval to first ovulation in this group of cows.

There was a highly significant effect of season (P <

0.01) between the two calving groups for leptin hormone, with

levels in summer calving cows being higher. There was no

significant effect of time or time x season interaction. Table 3

and Figure (2c). During early postpartum period, cows that are in

a more severe negative energy balance have a greater mobilization

rate of non esterfied fatty acids (NEF) from adipose tissue (the

main site of synthsis). As a result, adipocytes are depleted and

leptin synthesis is reduced (Block et al., 2001). Furthermore, it

has also been found that leptin secretion was altered by

15

photoperiod. In sheep studies, longer daylength was found to

increase leptin mRNA in adipose tissue as well as plasma leptin.

As daylength increases, the availability of food is also increased

in a grazing environment. Therefore, a longer photoperiod could

aid the animal in adapting to its environment through interactions

between leptin, insulin, glucocorticoids and brain hormones

(Chilliard et al., 2001). In another photoperiod study, Garcia et

al., (2002) found that in ovariectomized, estradiol-implanted

cows, plasma leptin was increased from January onwards until the

summer solstice. It has been reported that slight changes in cow

body weight or body condition does not significantly alter

circulating plasma leptin (Chilliard et al., 2001). For the

current study, there was a significant seasonal effect. The summer

group on average tended to have a greater amount of leptin for the

entire 10-week trial compared to the winter group. After calving,

the summer group averaged about 4.45ng/mL and the winter group

averaged about 3.656ng/mL. The winter group increased to an

average of about 3.769ng/mL by week 6 and the levels remained

fairly constant for the remainder of the 10 weeks. Likewise, the

summer group’s leptin concentrations did not deviate significantly

over time, although by week 8, levels had risen to an average of

about 4.95ng/mL. Our results suggest that the summer calving group

did not sxhibit a significant drop in body condition, enough to

deplete their adipose reserves and circulating leptin. Longer

daylength during the late summer compared to the winter could

16

therefore explain the summer group’s tendency to have greater

concentrations of serum leptin at postpartum.

Table 3: Mean (±SE) of serum hormonal parameters of crossbred cows (Brown Swiss X Ballady) in winter, summer and interaction during suckling period. Items Hormonal levels

T4(µg/dl) P4(ng/ml) Lipten (ng/ml)Season (S)Winter (overallX)

6.62 ±0.08B 0.591±0.021 3.728±0.074B

Summer (overall X)

12.03±0.09A 0.557±0.020 4.700±0.080A

Significance (p≤) 0.01 0.256 0.01Time of sampling (T) (weeks after calving)2nd 9.45 ± 0.14 B 0.02±0.032E 4.052±0.124

17

4th 6.76 ±1.101 D 0.08 ±0.027D 3.945±0.119

6 10.24±0.138 A B 0.477 ±0.028C 4.294±0.123

8 9.41 ±0.129 B 0.927 ± 0.032B 4.392±0.121

10 10.75±0.141 A 1.348 ±0.030A 4.391±0.123

Significance (p≤) 01.0 0.01 0.036

Interactions(S x T)Winter2nd 6.92±0.11a 0.022 0.038±

3.656±0.168

4th 5.66±0.112d 0.147±0.01 3.521 0.161±

6 6.87±0.121ab 0..464±0.04 3.769 0.164±

8 6.92±0.17a 0.963±0.03 3.833 0.167±

10 6.71±0.19b 1.357±0.044 3.864 0.159±Summer 2nd 11.98±0.20c 0.02±0.006 4.45±0.1654th 7.87±0.21d 0.02±0.005 4.37±0.126

6 13.6±0.26b 0.49 0.047± 4.82 0.141±

8 11.9±0.17c 0.892 0.040± 4.95 0.108±

10 14.78±0.38a 1.338 0.043±4.92±0.070

Significance (p≤) 0.01 0.459 0.855 Means bearing different letters (A, B and C or a,b and c) in the same column within each classification differ significantly (P≤.01 and .05), respectively.

Correlation coefficients for levels of protein, glucose,

urea, cholesterol, T4, progesterone and leptin were illustrated in

table (4). Concentration of protein was positively correlated

with concentrations of urea, cholesterol, and progesterone. Level

of urea was also positively correlated with concentrations of

cholesterol and progesterone. Concentration of cholesterol was

18

positively correlated with progesterone and finally, T4 level was

positively correlated with leptin.

Concentration of T4 hormone and leptin in serum were positively correlated during summer season of lactating cows which is in agreement with previous study (Ciccioli et al, 2003). It was shown that leptin administration increased pro-TSH gene expression(Legradi et al, 1997) and concentration of thyroxin (Ahima et al, 1996) in fasted rodents. Because basal metabolic rate and energy expenditure are directly regulated by thyroxin, the results of thecurrent study indicate that concentrations of leptin in serum may be associated with the rate of metabolism, increased secretion of anabolic hormones and tissue accretion.

Table 4: Correlation coefficients between levels oftotal protein, glucose, urea, total cholesterol, T4,progesterone and leptin

Item Correlation Coeffients

T.

protein

Glucos

e

urea T.

cholestero

l

T4 P4 Lepti

n

T. protein - .268 .625

**

.775** - .810

**

-

Glucose - .286 .375** .292 .385

*

-

urea - .- - .714** - .663

**

-

T.

cholestero

l

- - - - .919

**

-

T4 - - - .748*

*P4 - - - - - - -

19

Leptin - - - - - - -

Conclusion: From the present study it could be concluded that summer calving

cows may have an increase some biochemical and hormonal levels but not

enough to dramatically reduce the circulating levels of glucose, urea

and progesterone. The positive correlation between leptin with T4 may

indicate there associated implication in regulation in the rate of

metabolism.

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