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