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Effects of Heat Stress on Reproduction
and Fertility of Dairy Cows
David Wolfenson
Department of Animal Sciences
Faculty of Agriculture, Food and Environment
The Hebrew University
Rehovot, Israel
Introduction
• About 60% of the world cattle population is located in
hot zones, 35° north and south of the equator.
• The problem of heat stress is on the rise because
increases in milk yield are resulting in greater metabolic
heat production and because of anticipated changes in
the global climate.
• The problem is multifactorial in nature.
10 15 20 25 30 35
Air temperature
38
39
40
41 B
od
y t
em
pera
ture
(Berman et al 1985)
Sweating rate in cattle is relatively low
Cow Man Horse 0
300
600
900
1200
1500 g/h
x m
2
In the holding area
Along the feeding line
Cooling system: sprinkling & ventilation
(Berman, Wolfenson & Flamenbaum)
Fans in the resting area
Farm C
38.5
39.0
39.5
40.0
40.5
07:00 14:00 21:00
Hour of day
Farm A
38.5
39.0 39.5
40.0
40.5
09:00 14:00 18:00
Farm B
38.5
39.0
39.5
40.0
40.5
07:00 14:00 21:00
9 cooling periods/day
Bo
dy t
em
pera
ture
(°C
)
5 cooling periods/day
3 cooling periods/day
9 cooling periods/day
(Wolfenson & Thatcher, 2013)
Milk production*
Cooling minimal intensive
Winter (kg/d) 39 41
Summer (kg/d) 35 40
Diff. (W-S; kg) 4 1
Ratio (S/W) 90% 98%
Cooling minimal intensive
Winter (%) 43.5 46.6
Summer (%) 16.7 33.8
Difference (W-S) 26.8 12.8
Conception rates*
*mature cows
(Flamenbaum et al ; Israel Herd Book)
TH
I
50
60
70
80
90
THI
Conception rate and THI
20
30
40
1 2 3 4 5 6 7 8 9 10 11 12
Month
CR
(Israel Herd Book)
Hyperthermia
Follicles
Ovary
Embryo
Oocyte
Uterus Hypothalamus
Hypophysis
Corpus luteum
Steroidogenesis Growth
Follicular dynamics during the estrous cycle
Dominant follicle
Medium follicles
FSH
surge FSH
surge
Preovulatry follicle
Inhibin concentration in plasma is lowered by heat stress
Day of cycle
Inh
ibin
(n
g/m
l)
4 9 14 19
0.1
0.2
0.3
0.4
0.5
heat stressed
cooled
Medium-size
follicles N
um
be
r o
f fo
llic
les
1
2
3
4
5 Heat stress
Control
Day of cycle 1 4 7 10 13 16 19 22
FS
H (n
g/m
l)
0.5
0.3
0.1
FSH in plasma Heat stress
Control
(Roth et al)
Early emergence of the preovulatory follicle
Day of Cycle
Fo
llic
ula
r d
iam
ete
r (m
m)
Heat stressed Cooled
(Wolfenson et al)
Long duration of dominance is associated with low conception rate
Austin et al., 1999
0
20
40
60
80
100
0 2 4 6 8 10 12 14
Co
ncep
tio
n r
ate
Duration of dominance
13 14 15 16 17 18 19 20
Day of cycle
0
1
2
Larg
e f
oll
icle
s (
#)
Heat stress increases number of large follicles
Heat stress
Cooled
Twining rate in mature lactating cows
September - April May - August 0
3
6
9
12
15
(%)
(Ryan & Boland (1991), and Israel Herd Book)
Calving Months
Theca cells Granulosa cells
Follicular Steroidogenic Capacity
Steroid production by the preovulatory follicle
during different seasons
autumn winter summer
Granulosa - Estradiol
summer autumn winter
Theca - Androstenedione
ng
/10
5 c
ell
s
ng
/10
5 c
ell
s
a
b
ab
a
a
b
(Wolfenson et al)
Preovulatory follicle
(12-18 mm)
Medium follicle
(5-8 mm)
Small antral follicle
(0.5 -1.0 mm)
Primordial follicle
Follicular growth is a quite long process
Carryover effect: Estradiol & Androgen production 26 days after induction of acute heat stress (5 days)
0
3
6
9
12
Androstenedione
Theca cells
0
20
40
Estradiol
Granulosa cells
ng
/10
5 c
ells
Preovulatory follicles
(Roth et al)
Heat stress
Control
The corpus luteum
Plasma progesterone is lower during the summer
Day of cycle
0 3 6 9 12 15 18 21
5
1
2
3
4
6
7
ng
/ml
Winter
Summer
1 3 5 7 9
Day of culture
0
200
400
600
800
1000
Winter
Summer
luteinized thecal cells
1 3 5 7 9
Day of culture
0
200
400
600
800
1000
Winter
Summer
luteinized granulosa cells
Progesterone production during winter and summer by
luteinized granulosa and theca cells n
g/1
05 c
ell
s
ng
/10
5 c
ell
s
(Sonego et al)
The formation of a sub-optimal corpus luteum
in summer is determined to a great extent by
the ‘quality’ of the ovulatory follicle from
which it originated.
Heat stress lowers the preovulatory LH surge
Heat stressed
Control
(Gilad et al)
0
1
3
5
7
6 12 18 21
Days in cycle
pro
geste
ron
e (
ng
/ml)
P<0.03
Normal LH
Low LH
Low LH surge is associated with low progesterone
(Bloch et al)
junction
Fimbria
Oviduct Utero - tubal
Co
ncep
tus
po
sit
ion
IFN t production
by trophoblast
Shedding of zona pellucida
Implantation
150µ 170µ 205µ 340µ
250 mm
3
mm 425µ
develo
pm
en
t
Days after mating
Progesterone Estradiol
8 4 0
5
10
16 12 20
3
6
Estr
ad
iol
(pg
/ml)
Pro
ge
ste
ron
e
( ng
/ml)
Bovine peri-implantation events
Co
ncep
tus
(W. Thatcher)
Association between progesterone level and
embryonic development
0 2 4 6 8 10 12 14 16
(Adopted from Mann et al., 1999)
0
3
6
9
12
0
5000
10000
15000
20000
0
5000
10000
15000
20000
Day in cycle 16-day embryo
Pro
geste
ron
e (
ng
/ml)
Inte
rfe
ron
t
-(u
nit
s p
er
ute
rus)
Big Small
OOCYTE QUALITY
Effect of heat stress on OOCYTE COMPETENCE
(adapted from:
P.J. Hansen, 2013)
The process of oocyte and follicle formation is quite long and therefore, impairment early in the process can lead to reduced fertility many days later.
Bla
sto
cys
t (%
)
10
20
30
40
50
60 Summer
October
10
20
30
40
50
60
70
Gra
de
I (
%)
December
Autumn
Quality of oocytes and % blastocysts aspirated during
the autumn following summer heat stress
Hypothesis:
Enhanced removal of the pool of impaired
follicles, that had been damaged during
the preceding summer, could induce an
earlier emergence of healthy follicles in
the autumn.
Summer
A u t u m n
heat stress Cycle 2 Cycle 3 Cycle 4 Cycle 1
Day of cycle
ovulation
OPU
PG GnRH
0 4 11 20 18
Control
(n = 8)
heat stress
Summer X4
15 7 0 4 11 20 18
OPU
Treatment
(n = 8)
heat stress
Frequent aspiration to enhance follicular
turnover
Roth et al.
Autumn
In vitro culture
2-cell stage 4-cell stage 8-cell stage
8-day blastocyst
100
20
40
60
80
% Grade I
Cycle 1 Cycle 2 Cycle 3 Cycle 4
T C
Treat x cycle P < 0.05
10
20
30
40
50
60
8-Cells stage
Cycle 1 Cycle 2 Cycle 3 Cycle 4
T C
%
* P < 0.05 *
*
% 10
20
30
40 Blastocysts
Cycle 1 Cycle 2 Cycle 3 Cycle 4
T C
* P < 0.05
*
*
Results
%
10
20
30
40
50
60
70
80 4-Cells stage
Cycle 1 Cycle 2 Cycle 3 Cycle 4
T C
*
*
* P < 0.05
*
• In both groups, low oocyte quality and low embryonic
development were noted in the early autumn.
• However, significant improvement in developmental
competence was evident earlier in the treated group.
Roth et al.
20
30
40
50
60
Multiparous First-calving
27% 29%
53%
37%
* P<0.06
n=111 n=76 n=75 n=120
Three induced 9-day cycles with GnRH + PGF2α
improves conception rate in first-calving cows
Control
Treatment
Co
nce
pti
on
ra
te (
%)
Friedman et al., 2011
*
Fertility study (1)
Treatment with GnRH + PGF2α improves conception
rate in cows with low milk production
Control
Treatment
Friedman et al., 2011
20
30
40
50
60
< 40 kg
Co
ncep
tio
n r
ate
(%
)
> 40 kg
51%
36%
30%
*
* P<0.05
Day in cycle
0
2
4
6
8
10
0 5 10 15 20
Pro
geste
ron
e (
ng
/ml)
CONTROL
CIDR
CIDR in
CIDR out
CIDR device increases plasma progesterone
Friedman et al., 2011
Fertility study (2): exogenous progesterone
CIDR
Control
20
30
40
50
60
BCS < 2.25
27%
49%
n=64 n=71
*
*P<0.05
Co
nc
ep
tio
n r
ate
36%
32%
n=110 n=132
BCS > 2.25
Progesterone improves conception rate in cows
with low body condition
CIDR Control
20
30
40
50 46%
Postpartum
disorders
25%
Healthy
36% 38%
*
Co
nc
ep
tio
n r
ate
Progesterone improves conception rate in cows
with postpartum disorders
*P<0.09 Friedman et al., 2011
Control
GnRH
Summer 0
10
20
30
40
50
60
70 C
on
cep
tio
n r
ate
(%
)
n=157 n=157
P<0.01
Winter
n=75 n=81
NS
Kaim et al., 2003
Fertility study (3): GnRH injection at onset of estrus*
(Friedman, Wolfenson & Roth, In Press, JDS 2015)
AI
Fertility study (4): Combined Treatment
Monty and Wolff, 1974
Winter Summer
Estr
us d
ura
tio
n (
h)
Duration and intensity of estrus
Fertility study (5): Timed AI
TAI CONTROL 50
60
70
80
90
100 P
reg
na
ncy r
ate
(1
35
d P
P)
Summer
Winter
Pregnancy rate increased by Ovsynch - TAI
in the summer
(de Rensis et al 2002)
P<0.05
Conception rate per timed AI by month
(57)
(83)
(89)
(96)
(84)
(65)
(89)
(83) (117)
(93)(72)
(76)
(74)
0
10
20
30
40
50
60
May
'01
Jun
'01
Jul
'01
Aug
'01
Sep
'01
Oct
'01
Nov
'01
Dec
'01
Jan
'02
Feb
'02
Mar
'02
Apr
'02
May
'02
Pre
gn
an
cy
ra
te/A
I (%
)
-5
0
5
10
15
20
25
30
Te
mp
era
ture
(oC
)
Pregnancy rate/AI Temperature
Fricke et al., 2003
CONCLUSIONS
• Hyperthermia impairs several ovarian functions in lactating dairy cows.
• The knowledge gained enables to examine hormonal strategies to optimize reproductive function and to improve fertility of heat-stressed cattle.
• Efficient cooling management is a prerequisite for other strategies to improve fertility.
• Specific treatments for specific designated subpopulations of cows are suggested.
Collaboration
Z. Roth, R. Braw-Tal, R. Meidan, W.W. Thatcher, I. Flamenbaum, A. Arav, A. Bor, Y. Folman, M. Kaim, H. Sonego, B. Lew, A. Bloch, E. Friedman, Y. Lavon, Y. Graber, M. Maman
Thank you