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Theriogenology 74 (2010) 327344


www.theriojournal.com
Review

When is a cow in estrus? Clinical and practical aspects


J. Roelofsa,b,*, F. Lpez-Gatiusc, R.H.F. Hunterd, F.J.C.M. van Eerdenburge,
Ch. Hanzenf
a
Adaptation Physiology Group, Wageningen University, The Netherlands
b
Animal Husbandry and Animal Health, HAS Den Bosch, The Netherlands
c
Department of Animal Production, University of Lleida, Spain
d
Institute of Reproductive Medicine, Hannover Veterinary University, Germany
e
Department of Farm Animal Health, Utrecht University, The Netherlands
f
Department of Ruminants Theriogenology, University of Lige, Belgium
Received 1 October 2009; received in revised form 12 February 2010; accepted 12 February 2010

Abstract
Good detection of estrus is critically important in dairy husbandry. Incorrect detection of estrus is related to loss of profit due to
extended calving intervals, milk loss, veterinary costs, etc. Detection of estrus remains a major problem despites enormous progress in
the knowledge of reproductive physiology of the cow and in development of estrus detection aids. To achieve good estrus detection,
many factors have to be taken into account. On one hand a cow has to express estrus and on the other hand the farmer has to detect it.
Combined action of several hormones causes physiological changes that lead to ovulation and an environment in the uterus that allows
sperm to fertilize the egg. Besides these internal actions, a number of external changes can be observed. When using visual observations,
time of the day and time spend on observation have a great impact on detection rates. Many devices are available to aid in estrus
detection, such as pedometers, mount devices, temperature, and hormone measurements.
Expression of estrus can be influenced by many factors. Heritability, number of days postpartum, lactation number, milk production,
and health are known to influence estrus expression. Environmental factors like nutrition, season, housing, herd size, etc. also play a role
in estrus expression. To evaluate estrus detection, record keeping is very important; a number of formulas can be used to assess detection
efficiency. Besides the farmer, the veterinarian and inseminator can play an important role in estrus confirmation and good insemination
strategy. In the end, the time of ovulation and the age of the egg at sperm penetration is critical for conception. Therefore, emphasis in
research needs to be on the timing of insemination relative to ovulation, and thus on the detection of ovulation.
2010 Elsevier Inc. All rights reserved.

Keywords: Dairy cattle; Estrus; Physiology; Detection; Efficiency

Contents

1. Introduction ............................................................................................................................. 328


2. Underlying physiology ................................................................................................................ 329
3. Behavioral changes .................................................................................................................... 330
4. Why is it important to detect estrus? ............................................................................................... 330
5. Factors of influence of estrus detection ............................................................................................ 331

* Corresponding author: Tel.: 31 73 6923893; fax: 31 73 6923699.


E-mail address: j.roelofs@hasdb.nl.

0093-691X/$ see front matter 2010 Elsevier Inc. All rights reserved.
doi:10.1016/j.theriogenology.2010.02.016
328 J. Roelofs et al. / Theriogenology 74 (2010) 327344

5.1. Cow factors ..................................................................................................................... 331


5.1.1. Heritability ........................................................................................................... 331
5.1.2. Postpartum ........................................................................................................... 332
5.1.3. Number of lactation ................................................................................................ 332
5.1.4. Milk production ..................................................................................................... 332
5.1.5. Lameness ............................................................................................................. 332
5.1.6. Hormonal treatments ............................................................................................... 333
5.2. Environmental factors ......................................................................................................... 333
5.2.1. Bull .................................................................................................................... 333
5.2.2. Nutrition .............................................................................................................. 333
5.2.3. Season ................................................................................................................ 333
5.2.4. Circadian variation .................................................................................................. 334
5.2.5. Housing ............................................................................................................... 334
5.2.6. The herd size ........................................................................................................ 334
6. Detection of estrus ..................................................................................................................... 334
6.1. Detection of estrus by the farmer ........................................................................................... 334
6.1.1. Visual detection ..................................................................................................... 335
6.1.2. Estrus detection aids ................................................................................................ 335
6.2. The inseminator and estrus confirmation .................................................................................. 336
7. Estrus detection rates at herd level .................................................................................................. 337
7.1. Evaluation of heat detection accuracy ..................................................................................... 337
7.2. Evaluation of heat detection efficiency (HDE) ........................................................................... 337
8. Conclusion .............................................................................................................................. 338
References ............................................................................................................................... 339

1. Introduction cattle, man is no match for a bull at detecting estrus in


the cow even in the XXI century. Enormous progress in
In mammals, estrus is a behavioral symptom and the knowledge of the reproductive physiology of the
strategy to ensure that the female is mated close to the cow and in development of estrus detection aids during
time of ovulation. Estrus is an external and visible sign the last decades have not been sufficient for practice.
of ovulation, an internal and invisible event. The word Detection of estrus remains a major problem and its
estrus is derived from observations by Ancient people incorrect detection has been related to an annual cost
in herds of cattle, but not precisely related to mating. It greater than US$ 300 million by the USA dairy industry
comes from the Greek word oo (oistros), meaning [3]. Estrus signs in pregnant cows make the situation
a gatfly, member of the Family Oestridae, whose buzz- even more difficult. Pregnant cows will sometimes
ing during summer caused cows to become hyperac- even show standing behavior when mounted [4]. More
tive, usually showing frenzied behavior [1]. It is natural than 40% of cows were inseminated at a time of high
that the Greek would use the word oistros to describe
the behavior of a cow in heat. Such interest in estrus
behavior was not new. We can observe a cow in estrus
as perhaps the first representation of a reproductive
event more than 10,000 yr ago, in Teyjat (Dordogne,
France). An aurochs bull (Bos primigenius) is sniffing
the vulva with a clear representation of movement for
mounting (Fig. 1). Of course, Paleolithic cave paintings
and engravings show that knowledge of bovine behav-
ior was not rudimentary for prehistoric people; rather, it
just reflected the first human abstraction following sev-
eral hundred thousand years of social relationships be-
Fig. 1. Wild aurochs bull sniffing the vulva of a cow. Illustration from
tween man and animals, as a prelude to the domestica- the Magdalenian engraving in the Grotte the la Mairie, Teyjat,
tion process and especially intense in the case of cattle Dordogne, France. Circa 10000 B.C. Note sniffing has been expanded
[2]. Despite this long time of contact between man and and over-drawn on the original composition.
J. Roelofs et al. / Theriogenology 74 (2010) 327344 329

milk progesterone levels [5]. In a more recent study [6], minates in release of an oocyte into the oviduct at
about 19% of the inseminations were performed in ovulation.
pregnant cows. In the Netherlands, 4% of the calves It is useful to appreciate that because it is the ma-
born are from an insemination before the last one, turity of a Graafian follicle that regulates the amount of
0.16% is from 2 inseminations before the last one [4]. estradiol synthesized, so it is the maturity of the follicle
Progress in synchronizing estrus has not substantially that regulates its own time of ovulation and coincident
improved the reproductive performance of dairy cows, maturation of the oocyte, due to the positive feedback
although some protocols do allow fixed time insemina- of estradiol triggering the surge of gonadotropin release
tion [7]. Furthermore, milk production per cow is in- [14].
creasing year after year and the metabolic clearance of As a classical gonadal steroid hormone, estradiol is
steroid hormones related to high milk production [8] also exerting influences on the genital tract, rendering it
probably reduces behavioral manifestation of estrus. edematous, tonic, and highly secretory, especially in
However, as reported by Van Eerdenburg [9], there is the cervical glands, leading to a characteristic outpour-
no correlation between estrus expression and milk ing of mucus. In species in which semen is deposited
yield; yet high milk production can be correlated with into the anterior vagina at the time of mating, such as
high fertility [10]. The influence of seasonal and acute ruminants, rabbits, cats, and primates, including Man,
heat stress on steroid production by dominant follicles the cervix and its complement of mucus play a critical
may, moreover, have dramatic consequences in warm role in reproduction. Vaginal/cervical fluid is the first
countries [11]. Finally, the most accurate external sign of physiological medium that sperm cells encounter in the
estrus, standing to be mounted, was only registered around female genital tract and must overcome on their journey
60% of estrus periods in recent studies [12,13]. This paper to the site of fertilization. Macromolecular glycopro-
deals with views on estrus signs in order to propose a set teins, also known as mucins, constitute a three-dimen-
of criteria to improve the efficiency and accuracy of sional filamentous network throughout the mucus se-
estrus detection in the dairy herd. Automatic identifi- cretion mass which determines the physical properties
cation of a cow in estrus and factors affecting estrus of the mucus [15]. Cervical mucus becomes more plen-
behavior are reviewed. Confirmation of estrus at insem- tiful, watery, translucent, less viscous and easier to
ination is also suggested as a critical step. traverse by spermatozoa in the follicular phase of the
ovarian cycle. By contrast, in the luteal phase of the
cycle this mucus becomes scanty and viscous and,
2. Underlying physiology
consequently, unfavorable to sperm penetration [15].
The phenomenon of estrus occurs due to a specific Vaginal/cervical fluid dramatically reduces its mechan-
influence of ovarian steroid hormones on behavioral ical barrier effect during the course of estrus so that at
centers in the mammalian brain. As a Graafian follicle the middle of estrus (8 12 h after first manifestation of
matures under the stimulation of pituitary gonadotro- estrus) it is mechanically less hostile for the movement
phic hormones during the last three or four days of an of sperm [16,17].
estrus cycle, it synthesizes and secretes increasing Changes in temperature in the ovarian structures at
quantities of estradiol. In due course, the concentration estrus have been evaluated [18,19], whereas changes in
of estradiol circulating in the systemic blood reaches an temperature in deeper portions of the genital tract ur-
arbitrary levela thresholdwhich triggers two closely- gently require specific study using modern technology.
linked events due to positive feedback on particular They may not reflect temperatures as measured in the
areas of the brain. First, the threshold concentration of vagina or rectum, and may be prompting diverse mo-
estradiol causes the behavioral response, already dis- lecular changes in epithelial tissues of the genital tract
cussed, termed estrus. A second and closely-linked in- and in developing embryos [20].
fluence of estradiol positive feedback is to trigger a Accumulation of white blood cells in sub-epithelial
surge of release of pituitary gonadotrophic hormones, layers of the congested uterine mucosa is also a feature
especially LH. This results in a peak of gonadotrophins, of impending estrus, and again is regulated primarily by
detectable in the peripheral circulation that prompts the ovarian steroid hormones. Such white cells, especially
process of ovulation at a related time, commonly some polymorphonuclear leucocytes, are mobilized into the
20 30 h later in western breeds of cows. LH can be uterine lumen of estrus animals where they actively
demonstrated to bind to tissues of a pre-ovulatory fol- phagocytose dead or dying sperm cells, bacteria, and
licle, thereby causing a cascade of processes that ter- cellular debris. In the absence of pathological condi-
330 J. Roelofs et al. / Theriogenology 74 (2010) 327344

tions, white cells are not normally infiltrated into the also licking, rubbing, and aggressive behavior like head
lumen of the oviducts in estrus animals. This difference butting [33]. The above mentioned changes in behavior
between uterus and oviduct is important because the can be observed by the herdsman. Another behavioral
caudal (distal) isthmus of the bovine oviduct acts as a change during estrus, which is more difficult to detect
functional sperm storage site or reservoir for at least without technical aids but which is pronounced in many
24 30 h after mating at the onset of estrus [2123]. estrus cows, is the increase in activity as seen in an
Despite the above classical description, a new theory increase in the number of steps taken by a cow during
has been proposed by one of the authors highlighting estrus [e.g., 34 36]. Another change that is found in
the role of GnRH in the regulation of estrus behavior some cases during estrus which is not really related to
[9]. Probably, estradiol is not the only hormonal factor behavior is a decrease in milk production. In a study by
regulating estrus signs. In spontaneously cycling cows, Schofield et al. [37], milk yield was significantly re-
estradiol is sometimes elevated for a day before the duced on the day of estrus in a proportion of cows. This
onset of estrus behavior [24] and the alpha type recep- was manifested as a reduction in milk yield at the first
tors for estradiol in the hypothalamus disappear com- milking after the onset of estrus followed by a com-
pletely during estrus [25]. Therefore, GnRH is also pensatory increase at the subsequent milking. On the
proposed as a key factor in the regulation of estrus other hand, Rajamahendran et al. [38] did not find a
behavior. significant drop in milk production associated with es-
trus.
3. Behavioral changes
4. Why is it important to detect estrus?
As already mentioned, a cows behavior changes
due to hormonal changes preceding ovulation. The Management of reproduction is an important eco-
most pronounced sign of estrus is standing immobile nomic component in the success of a dairy enterprise.
when being mounted. Although it is difficult to com- The calving interval is primarily a function of the num-
pare studies because of many different estrus detection ber of days from calving to the initiation of the next
strategies, it is clear that many cows do not display pregnancy (days open) and the fixed effect of preg-
standing heat at all during estrus [12,26,27]. In dairy nancy length. The days open depend on the days from
cattle, the range of standing mounts is between 3140 calving to the first insemination or mating (WP: waiting
and 3225, respectively, in cows [28] and heifers [29]. period) and on the length of reproduction period (RP)
Standing heat is not the only behavioral sign cows i.e., on the number of days between the first and the last
display during estrus. The so called secondary signs of insemination followed or not by a pregnancy.
estrus, or, as Esslemont et al. [30] referred to it, a Impact of WP on calving interval is rather high
period of intensified behavior (PIB), are important to because a 1 d reduction in WP decreased calving in-
detect cows in estrus [12,27,31]. Many authors have terval by 0.86 d [39].
classified estrus behavior according to different defini- Pregnancy or conception rate depend on fertilization
tions. Beach [32] introduced the terms sexual attractiv- rate and on the quality of the embryo. These two last
ity, proceptivity, and receptivity. He stated that attrac- parameters are influenced by the estrus detection rate.
tivity refers to the females stimulus value in evoking The influence of the timing of artificial insemination
sexual responses by the male, proceptivity refers to (AI) relative to the stage of estrus was investigated long
various reactions by the female toward the male in ago. Early studies [40,41] were based on very frequent
establishing or maintaining sexual interaction, and re- (4 12 times per day) estrus detection of cows and
ceptivity refers to the female responses necessary for inseminations done on standing heat, not secondary
the success of the male to mate her. Although these signs. These studies indicated that maximum pregnancy
definitions all involve the male and are not solely based rates were obtained from midestrus until a few hours
on behavior, they are useful in observing estrus in dairy after the end of standing behavior. The a.m.p.m. rule
cows even when the bull is replaced by artificial insem- was developed as a guide for farmers. Cows first seen
ination. Behaviors that are displayed more (intense) in standing heat in the morning (a.m.) would be insem-
during estrus compared to non-estrus are restlessness, inated in the afternoon (p.m.) and those observed stand-
sniffing the vulva of another cow, flehmen, resting with ing in the evening would be bred the next morning.
the chin on the back of another cow, (disorientated) Other reports emphasized the importance of inseminat-
mounting and being mounted but not standing [27], but ing heifers or cows 12 to 18 h after the detection of
J. Roelofs et al. / Theriogenology 74 (2010) 327344 331

estrus to obtain optimal pregnancy or conception rates optimal when using a precise method for determining
[12,42 45]. On the contrary, two studies with twice estrus onset [48,50,53].
daily heat checks, using several thousands (44,707) of Among the numerous different factors associated
fresh or frozen semen, did not observe any differences with variation in the sex ratio of mammals, time of
in non return rates for cows that received AI at the same insemination and therefore estrus detection rate could
a.m. or during the p.m. following a.m. detection [46], or have an influence. In many species, early insemination
for cows inseminated once daily compared to the or mating appears to favor female offspring whereas
a.m.p.m. guideline [47]. Collectively, these results late mating appears to favor male offspring (for review
emphasized the importance of adapting the timing of see [54]). Most of the earlier studies based on infre-
insemination to farm conditions. If the management quent observations of estrus do not find any differences
permits precise determination of when a heat began, the in the sex ratio [46,55]. The opposite observation has
a.m. p.m. system should be used. If the pregnancy been reported as well. Using an Ovatec probe to mon-
rate is unsatisfactory or heat is not routinely detected, itor changes in electrical resistance of vaginal secre-
tions in beef cows, Wehner et al. [56] observed that
cows should be inseminated soon after they are first
early inseminations (estimated as 20 h before ovula-
detected in standing heat. If the beginning of estrus is
tion) resulted in 93% heifer calves while late insemi-
more precisely detected using an electronic estrus de-
nations (estimated to be 10 h before ovulation) resulted
tection system, it would be better to inseminate within
in 92% of bull calves. Martinez [57] showed, from data
4 12 h of observation of estrus [48]. In the same obtained on 716 cows inseminated at different times
context, it seems that the pedometer is a promising tool 8 44 h from the visual detection of estrus, that the
for prediction of ovulation and so can contribute to percentage of calved females (73.1%) is significantly
improving fertilization rate by better timing of insem- higher for early inseminations (8 18 h), and it de-
ination. It was found that highest pregnancy or concep- creases 1.9% per hour from the onset of estrus. Delayed
tion rates were obtained when insemination was per- AI (30 h) produced a significant deviation of the sex
formed between 517 h after increase of activity ratio towards the males (72.1%); nevertheless, fertility
[49,50]. (percentage of successful pregnancies) diminishes sig-
Insemination time can influence fertilization rate and nificantly, from 66.2% (8 18 h) to 45.4% (30 h).
embryo quality through the numbers of accessory Conversely, another study, using the Heat watch elec-
sperm [45]. Accessory sperm are sperm trapped in the tronic estrus detection system, to compare influence of
zona pellucida. Their numbers represent the number early (0 8 h or 8 10h), middle (8 16 h), or late
and quality of sperm competing for fertilization of the (20 25 h or 16 24 h) insemination time on sex ratio
ovulated ovum. On average, nearly 10 sperm cells per was unable to detect any effect of this parameter [54].
embryo were necessary to reach the maximum quality A more recent study using pedometers, frequent visual
of embryo [51]. This number is clearly favored by observations of heat signs, and ultrasonographic detec-
breeding later rather than earlier. Fertilization rate is tion of ovulation, did not find any difference in sex ratio
correlated with the increasing accessory sperm number. when inseminations were performed early (from 36
Early insemination resulted in lower fertilization rates 20h before ovulation), intermediate (from 20 8h be-
but good embryo quality, whereas late insemination (24 fore ovulation), or late (from 8h before to 12h after
h after the onset of estrus) reduced embryo quality but ovulation, [58]).
the fertilization rate was good [45]. Assessing ovulation
by ultrasonography and recovering 122 ova/embryos in 5. Factors of influence of estrus detection
80 lactating Holstein-Friesian cows, Roelofs et al. [52]
also showed that fertilization rates were significantly 5.1. Cow factors
higher when insemination was performed 36 12 h be- 5.1.1. Heritability
fore ovulation than after ovulation. Moreover, cows The degree of estrus expression has a low heritabil-
inseminated 24 12 h before ovulation, which corre- ity (0.21) and varies individually between cows and
sponds with insemination 0 12 h after first detection of even for the same cow from one estrus period to an-
standing heat, yielded highest percentages of viable and other [59,60]. Differences between genetic lines and
good embryos compared to cows inseminated after breeds have been reported [61]. For example, the du-
ovulation. Thus, the intermediate time of approxi- ration of sexual receptivity and estrus intensity (mounts
mately 12 h (6 16 h) after the onset of estrus was per hour) are higher for Bos taurus than for Bos indicus
332 J. Roelofs et al. / Theriogenology 74 (2010) 327344

cows, whereas, in general, dark-colored breeds show increased standing-still, the primary and most reliable
more intense estrus behavior than cows with white or sign of estrus [72].
red hair coloration [62]. Some further cow-related fac-
tors that influence estrus behavior include postpartum 5.1.4. Milk production
anestrus, age (lactation number), milk production, and Although there is no correlation between estrus ex-
the number of cows in estrus at the same time [63]. pression and milk yield [9], the metabolic clearance of
steroid hormones related to high milk production [8]
5.1.2. Postpartum probably reduces behavioral manifestation of estrus. In
Silent estrus (or more correctly: silent ovulation), is effect, in a study on 267 lactating dairy cows, Lopez et
common at the first postpartum ovulation in lactating al. [74] reported that higher milk producers ( 39.5
dairy cows. The physiologic mechanisms related to the kg/day) had a lower serum estradiol concentration on
postpartum ovulation without estrus signs have not the day of estrus, and duration of estrus was greatly
been resolved. Probably, high concentrations of estro- reduced compared with lower producers ( 39.5 kg/
gens during late gestation and parturition determine a day). In the same sense, in a study on 5,883 estrus
refractory effect to the estrogens present at the first events [72], each 1 kg increase in milk yield was
postpartum ovulation. However, progesterone released associated with a 1.6% decrease in walking activity at
from the corpus luteum formed after the silent ovula- estrus. Walking, however, is not the same as behavioral
tion seems to favor estrus expression during the next estrus score. Some behaviors are correlated with walk-
ovulatory cycle [64]. Postpartum return to regular cy- ing activity, but others are not [63]. Cows that produce
more milk may have a deeper NEB and a deeper NEB
clicity is critical for efficient reproduction. Subsequent
will increase the NEFA level, which is correlated with
reproductive performance may be influenced by the
lower walking activity [75].
characteristics of normal estrus cycles during the post-
partum period, the number of estruses [65,66], early 5.1.5. Lameness
ovulation [67], and follicular dynamics [68]. Moreover, The effect of lameness on ovarian postpartum activ-
a delayed return to regular cyclicity [66,69], and an ity is contradictory. For some, clinical lameness post-
increased incidence of abnormal ovarian cycles during pones by up to 18 d the beginning of ovarian cyclicity
the postpartum period [70] have been reported to ad- and by 24 d the onset to estrus compared to non-lame
versely affect the reproductive efficiency of high-pro- cows [76,77]. Such effects have been observed in cases
ducing dairy cows. of subclinical lameness [78]. Lameness has also been
associated with a higher risk of ovarian cysts due to a
5.1.3. Number of lactation delay or inhibition of the LH surge [79 83]. Such
By quantifying behavioral signs of estrus using a effect seems to be increased by the presence of a high
score system [12,27] and walking activity at estrus somatic cell counts (SCC) [83]. Recently, it has been
[66,71,72], higher behavioral scores and activity values shown that in lame cows the dominant follicle grew at
were registered in primiparous cows, compared to mul- the same rate to the same maximum diameter and
tiparous cows. For example, each additional lactation ovulated at the same time as in healthy animals [83].
number was associated with a 21.4% decrease in walk- Lameness is classically associated with a reduction
ing activity at estrus [72]. In contrast, the number of of estrus intensity in dairy cows [31,84]. This reduced
standing-to-be-mounted events at estrus, a main indi- estrus expression may be caused by physical limitations
cator that a cow is in estrus, increases with parity of the lameness itself inducing a reduced frequency of
[62,63]. The lack of a relationship between standing- primary and secondary estrus behaviors. It is, therefore
to-be-mounted and pedometer readings was demon- interesting to note that subclinical claw disorders have
strated by van Vliet and van Eerdenburg [63]. The no influence on the intensity of estrus expression [85].
explanation for this could be related to the fact that Some differences between lame and normal cows have
the walking activity increase can occur 16 h before the been recently determined. Lame cows spent more time
onset of estrus [73], a period in which cows are often lying and less time standing and walking during estrus.
observed as mounters [62]. Consequently, a direct re- They have a lower BCS and a lower bite rate while
lationship between mounting other cows and increased grazing [31]. Using a weighted scoring system to quan-
pedometer readings has, in fact, been described [63], tify estrus behavior, it has been determined that lame-
reinforcing the idea that secondary signs such as ness can induce an overall reduction of approximately
mounting-other-cows decrease with parity alongside 37% in estrus intensity [86]. In lame cows, factors
J. Roelofs et al. / Theriogenology 74 (2010) 327344 333

involved in the reduction of first postpartum estrus of steps recorded by a pedometer is greater and estrus
behavior more than in incidence of estrus are not yet detection improved. In absence of tactile stimulation by
well understood. Several possibilities have been pro- a bull, expression of estrus is not modified [26]. Oth-
posed [78]. erwise, the presence of a bull in the herd can inhibit
Lameness could reduce estrus intensity by reducing cow-cow mounting [101] or has no effect on the dura-
progesterone concentrations (see below) before estrus tion of estrus [102]. The presence of an estrus cow, a
without affecting estradiol or cortisol milk profiles [78]. nymphomaniac cow, or a teaser bull increases the prob-
The lower progesterone concentrations observed in ability of observing a mount [4,103]. Such effects of the
chronically stressed lame cows could result from an presence of a bull have been observed after synch-
alteration of pulsatile patterns of luteinizing hormone ronization of animals with prostaglandins [104,105].
(LH) as shown by injection of adrenocorticotrophic Mounting activity of teaser bulls seems to depend on
hormone (ACTH) [79]. cows [101]. Estrus would be shortened if the cow were
Lame cows sniff other cows less [78]. The purpose naturally mated or artificially inseminated [106,107].
of sniffing is to detect chemical signals or pheromones
The interval between calving and the onset of estrus
between estrus herd mates. So they increase self attrac-
behavior can be shortened by the presence of a bull
tion but also induce sexual behaviors in others [87].
[108,109].
Receiving less positive feedback motivation from other
cows, severely lame cows express a less intense estrus
[78]. Conversely, standing likely less long, a lame cow 5.2.2. Nutrition
is also less pheromonally attractive for other cows [78]. Poor nutrition or the loss of body reserves (negative
energy balance) can negatively affect estrus expression
5.1.6. Hormonal treatments [62,110,111]. Dietary phosphorus treatment (adequate
The importance of progesterone priming in the effi- or in excess) did not have a significant effect on dura-
ciency of estrus expression has been observed after use tion or intensity of estrus [112,113]. A recent study
of synchronization programs [88,89]. Progesterone in- shows that the odds of estrus being detected by slight
creases the number of hypothalamic estradiol receptors signs instead of standing heat was multiplied by 7.8 for
during the luteal phase and, consequently, the sensitiv- a group of multiparous Holstein cows fed a high diet
ity to estradiol [90]. This can result in a positive effect (allowing high milk yield while limiting body condition
on expression of specific estrus signs (mounts, chin loss) in winter indoor and at grazing compared to a low
resting, and sniffing) compared to only estradiol treat-
diet (aiming at limiting milk yield while mobilizing
ment in ovariectomized cows [89].
adipose tissue reserves). The major factor to explain the
Usually, no differences in duration of estrus have
less intense estrus behavior in the high diet group was
been observed between estrus induced by PGF2alpha
the milk yield which was higher in the high diet group
and estrus occurring spontaneously [12,91]. Neverthe-
[13].
less, some authors observed a decrease of the accuracy
of estrus detection after use of prostaglandins [92].
According to some publications, duration of natural 5.2.3. Season
estrus seems to be longer than estrus induced by pros- Most of the studies report a seasonal effect on estrus
taglandins (15,3 vs. 13,3 h [93]; 21,7 vs. 19,8h [94]). behavior [72,114 122]. Conversely, some authors found
Estrus seems to be more often detected after use of that increased temperature did not influence the dura-
progestagenes than after use of prostaglandins [95]. tion of estrus in dairy cows [91]. Such differences can
Some studies have shown that use of bST can induce a be due to the maximal considered temperature i.e., 24,4
reduction of estrus behavior [96 98]. C in the study of Walker [91], 34,6 C in the study of
White [122] and 33,9 C in the study of Pennington
5.2. Environmental factors [119]. An extended period of high temperature shortens
5.2.1. Bull the duration of estrus and reduces the intensity of be-
The presence of a male can positively affect expres- havior [123,124]. Conversely, beef cows were mounted
sion of estrus in sows [99] or onset of estrus in sheep more frequently during estrus in winter and duration of
and goats [100]. Number and duration of interactions estrus was longer during summer with longer intervals
with a fenceline-housed bull are higher during than between mounts [122]. Heavy rain, strong wind,
between estrus. The reasons (olfactory, visual . . .) are or high humidity reduce or suppress estrus behavior
not very well known. The relative increase in number [101,125,126].
334 J. Roelofs et al. / Theriogenology 74 (2010) 327344

5.2.4. Circadian variation truses, each additional cow in estrus at the same time
Some studies suggest no variation in estrus during was associated with a 6.1% increase in walking activity
the day [28,30,127129]. According to others studies, [66]. So the number of mounting activities is multiplied
estrus behavior seems to be more frequent during the by 5 if the number of cows in heat at the same time is
evening or nocturnal period [104,130,131] or early multiplied by 4 or more (49.8 vs. 11.2) [125].
morning and daylight hours [63,121,125,132]. Some
observed variations can be related to usual management
6. Detection of estrus
activities like feeding, cleaning, or milking [133].
The ability to detect a cow in estrus mainly depends
5.2.5. Housing on the experience of the farmer and the time invested in
According to King et al. [134], approximately half estrus detection. It is important that the farmer can
of the estrus periods in lactating cows were not detected recognize and interpret several behaviors that indicate a
by casual observation under tie stall barn conditions cow is in estrus. Timing of observation on the day, time
compared with cows observed continuously and housed spent on estrus detection, and frequency have a large
under free stall barn conditions. Barn-housed cattle effect on estrus detection rates [e.g., 12,143]. Besides
exhibited more mounts per hour during estrus than visual observation of estrus, many devices can aid in
cattle housed on pasture [128] mainly because cows on improving estrus detection. Of course, record keeping
pasture spend more time grazing than animals confined of animals in estrus in a structured and organized way
in barns [135]. On the other hand, Cutullic et al. [13] is also very important.
found no effect of pasture access on the intensity of
estrus behavior (estrus detected by slight signs versus 6.1. Detection of estrus by the farmer
standing heat). The substrate of the floor on which Different methods can be used to detect estrus. Their
cattle are housed affects estrus behavior. Mounting comparison can be made using different parameters
activity is less frequent on slatted floors than in straw [144]. During an estrus period, normal estrus behavior
yards [136], slippery surfaces [119], or dirty floors can be correctly detected and considered as truly pos-
[137]. Duration of estrus and number of mounts are itive (a). If such estrus has not been detected, it will be
longer (13.8 vs. 9.4 h) and greater (7 vs. 3.2 times) on considered as a false negative (c). During diestrus,
dirt than concrete surfaces [138]. Covering a concrete estrus behavior is usually not detected and such behav-
slatted floor with perforated rubber mats improved the ior can be considered as a true negative (d). Otherwise,
ability of cows to express normal behavior of estrus the diagnostic can be considered as a false positive (b).
[139].
Estrus Diestrus
5.2.6. The herd size Diagnostic (a) (b)
When the herd is larger, the number of social inter- Diagnostic (c) (d)
actions between the animals will be greater. Most of the The sensitivity (efficiency, detection rate, diagnosis rate) of estrus
time (60%), mounting activity is initiated by heavier detection is (a/(ac))*100
cows [140]. Dominant cows may inhibit the mounting The specificity of estrus detection is (d/bd))*100
activity of subdominant cows [126]. Other authors have The error rate is (b/ab))*100
not found any correlation between dominance, rank, The positive predictive value (accuracy) is (a/(ab))*100
The negative predicting value is (d/(cd))*100
and the frequency of given or received mounts [141].
The possibility to form sexually active groups (SAG) is Many researchers have studied one or more of the
higher when the size of the herd is increased. The above mentioned variables to evaluate different estrus
degree of estrus expression and, therefore, the possibil- detection aids [e.g., 36,73,145149]. When comparing
ity to detect an estrus can be dramatically favored by these variables between studies, it is important to know
the number of cows in estrus at the same time what was used as golden standard, because this can
[9,12,13,63,125,142]. The simultaneous presence of influence the results. True or false positives can be
other animals in estrus allows the cow the opportunity determined by repeated ultrasonography for ovulation
to share estrus behavior so that estrus expression may [150] or progesterone measurement around detection of
also be result of sexual stimulation by other animals in estrus [27,145,146]. True and false negatives can be
estrus [12]. More animals in estrus were detected, with determined by progesterone measurements throughout
increasing numbers of animals simultaneously in estrus the estrus cycle [27,146] or in comparison with other
[36] and, by analyzing activity increases for 995 es- estrus indicators [36,151,152].
J. Roelofs et al. / Theriogenology 74 (2010) 327344 335

6.1.1. Visual detection 6.1.2. Estrus detection aids


Many studies have investigated estrus detection by Many reviews are available about estrus detection
visual observation [e.g., 12,63,130,153]. Most studies and estrus detection aids [3,133,144,155158]. From
have focused on the most pronounced sign of estrus; this extensive information, it is clear that many aids are
standing heat. Estrus detection efficiency by visual ob- on the market to help the farmer to detect the cows in
servation of standing heat mentioned in different stud- estrus correctly. These aids vary from activity meters,
ies vary a lot from 90% [130] to less than 50% mount detection devices, cameras, temperature mea-
[52,63,154]. surements, impedance or conductivity measurements,
It becomes clear that signs other than standing heat hormone analyses, and so on. Between studies, differ-
are important to detect cows in estrus. An estrus scoring ent detection rates of different aids are mentioned.
system was developed in which points were assigned to Detection rates of pedometers vary between studies
different behaviors (standing heat, being mounted but but are often above 80% [144,157]. Some studies report
not standing, (disorientated) mounting, resting with the detection rates of 100% [37,73]. Detection rates are
chin on the rump of another cow, sniffing the vulva of affected by the threshold that is used to define an
another cow, and restlessness) [27]. With this scoring increase in activity as an estrus period and the time
system, a cow can be detected in heat without showing period that is used to store the number of steps [36].
standing heat. Studies that have observed other signs Accuracy has been reported to be as low as 49% [159]
besides standing heat report quite a high percentage of and over 90% [36,37]. Also, cow and environmental
estrus periods without standing heat (37% [13], 63% factors can affect efficiency of activity meters to detect
[27], 42% [12]). Not only the behaviors that are ob- estrus (see section 5).
served, but also the time of day, frequency, and dura- Another aid in estrus detection is mount detection
tion of observation have an effect on estrus detection. devices. These devices are attached to the sacrum of the
Roelofs et al. [12] found that only 19% of the cows cow and indicate whether a cow has been mounted or
were detected in heat when observations were done not. A non electronic variant of mount detection is the
twice a day for 30 min on standing heat alone. This use of tailpaint. Detection rates vary among studies
percentage increased to 30% when observations were from under 50% [148,160], to up to 80% [146,161], and
performed 3 times per day for half an hour. When, over 85% [145,151]. Again, the efficiency of the de-
besides standing heat, mounting another cow was taken vices is affected by the threshold that is set for identi-
into account, heat detection was 61% when performed fying estrus and the way the device is attached to the
3 times per day for half an hour. When all the behaviors animal. Obviously, such devices would not work prop-
mentioned above were included 3 times per day for 30 erly when brushes are present in the stable. Also, cow
min, heat detection increased to 90%. Van Eerdenburg and environmental factors affect estrus detection effi-
et al. [27] found a detection rate of 12% with three ciency (see section 5).
observations of 30 min daily only observing standing Body temperature changes during the estrus cycle
heat and of 74% when all the behaviors where included. [144]. A rise in temperature can be detected around the
Cavestany et al. [143] studied estrus detection rates LH-surge during estrus [38]. This may be caused by a
with observations of standing heat on different times of higher level of activity during estrus, but the mecha-
the day and of different duration in a pasture based nism behind the temperature change is not clear. Using
system. Highest detection rates (94%) were found when milk temperature measurement, 50% and 84% of the
observations were performed two times per day for 60 estrus cows were detected in two studies [162,163].
min during quiet times (at dawn and dusk), 76% detec- However a very high percentage of false positive alerts
tion rate was found with 30 min observations at the was found [162]. Redden et al. [164] detected 81% of
same time. When observations were performed around the estrus cows by measuring vaginal temperature, with
milking twice a day for 30 min, detection rates de- 14% false positives.
creased more than 30 41%. Several studies have shown that vaginal mucus con-
It is clear that estrus detection rates vary with the ductivity (or resistance) changes during estrus [158].
method of visual observation that is used. Therefore, it Fisher et al. [165] developed an electrodeless conduc-
is possible to compare estrus detection rates between tivity measuring device, but they concluded that there
different studies only when timing, duration, and fre- was too much variation and noise in the conductivity
quency of visual observations, as well as which behav- results and that it was not suitable for detection of
iors are included, are described in detail. estrus. This agrees with the findings of other studies
336 J. Roelofs et al. / Theriogenology 74 (2010) 327344

that found undesirably high rates of false positives and mounted by another cow or bull at all stages of preg-
false negatives [166,167]. nancy [172].
A combination of several estrus detection aids might Manual [173] or ultrasonographic [150] rectal ex-
give the best results in terms of estrus detection effi- amination of the bovine reproductive tract allows cor-
ciency. Peralta et al. [148] used three times daily visual rect diagnosis of estrus when the animal is ready for
observations, a mount detection device, and an activity service. Repeated rectal ultrasound during estrus does
transponder. On its own, visual observation yielded the not alter behavioral estrus or peri-ovulatory hormone
highest detection (49.3%), followed by the mount profiles and can be a useful tool for assessing time of
detection device (48%), and the activity transponder ovulation [150]. The physical properties of the uterus
(37.3%). The combination of the three systems in- [174] and vaginal fluid [16,175] during estrus may also
creased the detection rate to 80.2%. Another study be used as a reference for estrus. A cow can be classi-
combined visual observations by the herdsman with fied as ready for service when the corpus luteum is
either a hormone-treated steer or tailpaint. Observations manually or by ultrasound estimated to be either less
by the herdsman alone gave a detection rate of 77%, than 10 mm or non-detectable, the largest follicle
which was the same as for the combination of visual shows a lack of fluctuation and has an estimated diam-
observations and tailpaint. The detection rate increased eter of 1225 mm, the uterus is highly turgid and
to 89% when the visual observations were combined contractile to the touch, and vaginal discharges are
with the hormone-treated steers. Using a combination copious, fluid, and transparent [173]. Vaginal fluid can
of different traits as activity, milk temperature, milk easily be obtained at the time of insemination by gentle
yield, and conductivity gave detection rates between 67 suction from the cranial vagina using a plastic insemi-
and 94% in different studies [144]. nating sheath and a 50-ml syringe and examined for
transparency, fluidity, and blood or pus contents [16].
6.2. The inseminator and estrus confirmation
In a study of estrus confirmation by palpation per
Inseminating the cow is the final, but by no means rectum performed on 6084 normal repeat dairy cows
least important, act in the process of estrus detection. following their first AI [173], the 150-day non return
The efficiency of cow insemination depends, among rate for rejected cows with a corpus luteum greater than
other factors, on the ability of the inseminator to deliver 15 mm in diameter was 87%. All cows selected had
the semen to the appropriate site in the reproductive normal intervals between first insemination and estrus
tract at the appropriate stage of estrus. Extensive train- (18 26 d). In the same study, cows were considered to
ing of inseminators has been one of the most significant be in estrus but insemination was incorrectly timed
contributions to the successful commercial application when the cow had no significant follicular structure.
of AI in dairy cattle breeding [168]. Unfortunately, The authors suggested that these latter cows were early
there has been a tendency to adopt routine insemination ovulators or estrus detection had been undertaken late
techniques and to ignore inseminator-related factors in estrus. The 150 d non return rate for cows estimated
that influence fertility. Although professional insemina- to be ready for service was 44%, compared to 27% for
tors palpate the reproductive tract of numerous cows every cows in which estrus and insemination were incorrectly
day, most are not trained to examine the uterus and ova- timed. The data of a subsequent, larger study [6] con-
ries and, therefore, to confirm estrus. This poses a serious firm the benefit of examining the reproductive tract per
practical limitation to the success of estrus detection pro- rectum at the time of insemination to inseminate cows
cedures and AI. In a recent study on 10,965 AI includ- in estrus only. In Israel, inseminators are trained to
ing 13 technicians [169], a dramatic significant differ- check the tone and symmetry of the uterus by rectal
ence among inseminators was registered, the likelihood palpation and to examine vaginal fluid. In Israel, it is
of pregnancy decreased by a factor of 0.25 when a cow common practice to evaluate several factors indicative
was inseminated by the worst inseminator compared to of estrus before insemination to avoid the insemination
the best one. As has been noted above, a high rate of AI of pregnant cows, of cows that are not at the appropri-
is performed in cows that are not ready for service or ate stage of the estrus cycle, or of those with purulent
are pregnant. The situation is further worsened by the discharge. During the period of the referred study [6],
fact that the insemination of pregnant cows can cause the total number of cows rejected for re-insemination
embryonic mortality or abortion [170]. The incidence was 55,390 (about 16% of the total cows submitted for
of estrus during pregnancy has been reported exten- re-insemination), with a 95% accuracy of rejection of
sively [4,6,171]. Pregnant cows stood willingly to be 44% of pregnant cows. Main reasons for rejection were
J. Roelofs et al. / Theriogenology 74 (2010) 327344 337

the condition of the vaginal fluid and the tone of the dealing with heat detection errors present different
uterus. characteristics related to the distribution of intervals
Over the last decade, some studies have reported an between estrus dates: estrus intervals between 317 d
increase of infertility worldwide [176 178]. Both di- exceed 10 15%; estrus intervals between 18 24 d are
minished efficiency of AI and failure to detect estrus lower than 60 70%; estrus intervals between 2535 d
correctly should warrant the re-evaluation of insemina- or 2538 d exceed, respectively, 10 15% or 10%;
tor training in order to confirm estrus [3,179]. Exami- estrus intervals between 36 48 d or 39 45 d exceed,
nation of vaginal fluid and uterine palpation prior to respectively, 510 or 10%; estrus intervals longer than
insemination have been shown to improve pregnancy 45 or 48 d exceed 5%.
rates, reduce abortions, and reduce the unnecessary use As well as in herds dealing with estrus detection
of semen, all of which contribute to the improved problems, cows inseminated one day and again within
reproductive performance and consequent profitability three days exceed 5%; several cows checked pregnant
of dairy herds. Further research using ultrasonography to a service earlier than the last one recorded, 4% of the
should be undertaken to find predictors for time of cows in the Netherlands calve normally three to six
ovulation [150]. weeks before the expected calving date [4].
7.2. Evaluation of heat detection efficiency (HDE)
7. Estrus detection rates at herd level
Different general indices have been proposed to ap-
The evaluation of estrus detection is an important proximate the heat detection efficiency. Their use de-
step to interpret reproduction performance at the herd pends on the available data on the farm. Moreover, they
level. Complete and accurate records including all can be used with data observed before or after the
heats, services, birth, and calving dates are necessary. It waiting period (pre and post service HDE).
is also necessary to distinguish between the accuracy and The Woods index is obtained by multiplying by 100
the efficiency of heat detection. Estrus detection is inac- the ratio between the normal cycle length (21 d) and
curate when cattle are inseminated but are not really in average estrus interval between consecutive services or
estrus. Estrus detection is inefficient when the number of heats observed for all heifers or cows or for specific
unobserved or missed heats increases [180 195]. group of cows (primiparous vs. multiparous cows).
Only cows known to be cycling and with at least two
7.1. Evaluation of heat detection accuracy
recorded estrus or AI events are considered in this
Evaluation of heat detection accuracy is important be- calculation. Normally, this ratio will be higher than 75
cause, according to different studies, it appears that [191], i.e., that average interval between estruses will
530% of inseminated animals are not really in heat be less than 29 d. One problem with this method is the
[5,6,184,185,196]. Conversely, it must be noted that 6% high rate of prostaglandin used. Moreover, the method
of pregnant cows will be detected in estrus [153,197]. can underestimate the efficiency of estrus detection in
Milk or blood progesterone analysis is a useful tool case of pathologies like ovarian cysts or pyometra
to evaluate accuracy of heat detection in the following [198].
situations: the cow was observed in heat but was pre- It is also possible to calculate the ratio of 18 24 d
viously diagnosed pregnant; standing heat was ob- and 36 48 d estrus intervals. Normally the ratio will be
served but the estrus interval was abnormally short or higher than 4:1 [186] or 6:1 [195].
long; the cow was detected in heat based solely on It is also possible to suspect a problem when the
secondary signs. To make the evaluation worthwhile, percentage of cows observed not pregnant by a late
1520 cows should be sampled on the day of insemi- pregnancy diagnosis method is lower than 80 90%
nation. If more than 5% of the samples have high according to the stage of pregnancy diagnosis (42 vs.
progesterone, the heat detection error rate is too high. 63 d) and so the frequency of herd visits [183,188].
As proved by different studies [6,173,175], system- More specific expected values of percentages of preg-
atic palpation and vaginoscopy at AI could be used to nant cows have been proposed according to the stage of
confirm estrus and indirectly reinforce its detection pregnancy diagnosis, pregnancy rate, and estrus detec-
accuracy by the farmer. tion rate [198].
The analysis of the distribution of intervals between Calculation of the percentage of cows seen in estrus
estrus and/or inseminations dates is another method to by 50 to 60 d postpartum and mean days in milk at first
suspect a lack of accuracy in estrus detection. Herds estrus is also possible if the farmer has an accurate and
338 J. Roelofs et al. / Theriogenology 74 (2010) 327344

regular system of notation. Moreover, different factors below 60%. An HDE rate below 50% indicates a very
can also interfere with such a method of evaluation strong need of improvement [188].
[195]. A good alternative method is to calculate the Grusenmeyer [201] calculated the breeding interval
percentage of cows not seen in estrus during the first (BI) as follows: (DOWP)/(n AI 1) or as follows:
21 d after the waiting period calculated in the herd. (DO [VWP 10])/(n AI 1). If the conception date
To evaluate HDE before the first service, i.e., during is not known, DO can be replaced by the interval
the waiting period (WP), it is necessary again to en- between the last insemination done and calving. The
courage the farmer to record all estruses observed. This average BI obtained is compared to some proposed
index can contribute to identification of an anestrus values. If averaged BI is 23, 26, 30, 35, 41, 50, or 60 d,
problem in the herd. One method of preservice HDE the % of observed estruses are, respectively, 90, 80, 70,
calculation could be the following [188]: Preservice 60, 50, 40, and 30 [201].
HDE (21/[WP observed Voluntary WP] 11))*100. If all events of estrus or services are available,
Calculating the percentage of cows seen in estrus be- OConnor [199] has proposed using the following for-
fore the waiting period decided by the farmer (usually mula ((n of estrus or services)/(n cows n of days in
60 d) is an alternate method. The herds confronted with the observation period)/21)*100. This method assumes
heat detection efficiency problems observed and re- all cows are cycling. Moreover, this formula is rather
corded very few heats before the first service. Nor- difficult to use in small herds due to the limited number
mally, 85% of cows are detected in estrus by 60 d of observations.
postpartum. Moreover, in herds confronted with estrus The American Association of Bovine Practitioners
has proposed evaluating the heat detection efficiency by
detection efficiency, WP length exceeds 80 d when the
calculating the percentage of possible estruses detected
voluntary waiting period (VWP) decided by the farmer
during a period of time (monthly or yearly according to
is 60 d [199].
the size of the herd) using the following formula:
Postservice HDE can indicate a lack of attention to
(a/(b/21))*100 in which (a) is the number of breedings
breeding cows. Different methods of calculation have
or estruses observed in the period of observation and
been proposed according to the available data. All those
(b) the number of estrus cycle days in the period for
methods concern the breeding or reproduction period,
eligible cows. A specific method for selection of eligi-
i.e., the period between the waiting period or the vol-
ble cows has been proposed [182].
untary waiting period (VWP) adopted by the farmer
and the beginning of pregnancy or the last insemina-
tion. If the VWP is used, 10 d are usually added to the 8. Conclusion
value of the VWP. The last insemination date will, It is clear that a good detection of estrus is critically
preferably, be used in small herds to optimize the avail- important. However, this is easier said than done. Some
able data. herds have no problems at all with fertility while others
Barr [200] has proposed calculating the days lost struggle with their insemination number, calving inter-
due to missed estruses using the following formula: val, and other parameters, which might be caused by
(DO WP) [(services/pregnancy 1) 21]. If the inefficient estrus detection. To know whether or not this
VWP is used, it is necessary to add 10 d to the VWP, problem exists on a farm, record keeping is of the
assuming that the first breedable estrus would be de- utmost importance. When calving dates, cow identifi-
tected on average 10 d after the end of VWP [200]. cation, and estrus dates are recorded, pre- and post-
Bailey [188] evaluated the post service HDE using service heat detection efficiencies can be detected. To-
the following formula: ((Services per pregnancy 1)/ gether with the veterinarian, these parameters can be
(DO WP)/21))*100. The difference between days evaluated to see if there is room for improvement.
open (DO) and WP divided by 21 represents the po- Many factors, environmental, managerial, and cow-
tential number of estruses. The number of services per related, play a role in estrus expression/detection. It is
pregnancy minus 1 (the service that the cow became good to be aware of all those factors that cannot be
pregnant) represents the number of estrus cycles really influenced easily (housing, parity, milk production,
used. For example if the number of services per preg- herd size, season, climate) and try to change the factors
nancy is 1.8; DO 150 d and WP observed 80 d, post that can be influenced (number of observations, length
service HDE will be 24%. Excellent, good, and poor of observation, time of day, record keeping) to improve
HDE rates are respectively higher than 80%, 70%, and estrus detection efficiency. One has to be aware of all
J. Roelofs et al. / Theriogenology 74 (2010) 327344 339

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