R. H. Foote
The history of artificial insemination: Selected notes and notables
2002. 80:1-10. J Anim Sci
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The history of artificial insemination: Selected notes and notables
1
R. H. Foote
2
Department of Animal Science, Cornell University, Ithaca, NY 14853-4801
ABSTRACT: Artificial insemination (AI) was the
first great biotechnology applied to improve reproduc-
tion and genetics of farm animals. It has had an enor-
mous impact worldwide in many species, particularly in
dairy cattle. The acceptance of AI technology worldwide
provided the impetus for developing other technologies,
such as cryopreservation and sexing of sperm, estrous
cycle regulation, and embryo harvesting, freezing, cul-
ture and transfer, and cloning. New, highly effective
methods of sire evaluation were developed. The history
of development of AI is reviewed, particularly in dairy
cattle, in which the impact on genetic improvement and
control of venereal diseases have been greatest. Other
Key Words: Artificial Insemination, Estrus, Livestock, Selection, Semen, Sex Determination
2002 American Society of Animal Science. All rights reserved.
Introduction
Artificial insemination (AI), as practiced by bees and
many other flying insects, has played an important role
in plant reproduction for a very long time. Use of AI in
animals is a human invention and more recent. Undocu-
mented tales exist of Arabs obtaining sperm from mated
mares belonging to rival groups and using the sperm
to inseminate their own mares.
However, our story starts with recorded history,
where facts are available to document noteworthy
achievements. Consequently, the story is related chro-
nologically. Much of the development of AI occurred
before the 1980s when electronic networks became
available, so earlier references are included. The devel-
opments that made AI the most important animal bio-
technology applied to date include improved methods
of male management and semen collection, evaluation,
preservation, and insemination. Detection of estrus and
1
The author is indebted to all those who diligently pioneered re-
search and extension activities to make AI one of the greatest stories
never fully told, and to D. Bevins for assistance with manuscript prep-
aration.
2
Correspondence: 204 Morrison Hall (phone: 607-255-2866; fax:
607-255-9829; E-mail: dgb1@Cornell.edu).
Received March 26, 2001.
Accepted June 8, 2001.
1
species briefly included are swine, horses, sheep, goats,
dogs, rabbits, poultry, and endangered species. Major
landmarks in AI development are cited, along with the
people most closely associated with these develop-
ments. Many of these pioneers helped to develop a new
generation of reproductive physiologists and biotech-
nologists. A bit of the flavor of the times is included,
along with the historical facts. Many of the references
will take the reader back to an era before electronic
networks were available, so these citations of classical
studies will not be found with the press of a key on
the electronic keyboard. Readers are invited to explore
these historical treats that have provided a springboard
for the future.
control of the estrous cycle in the female also were
important. The development of AI is a remarkable story
of tireless workers dedicated to the pursuit of knowl-
edge, to the replacement of fiction with facts, and the
application thereof.
Dairy cattle will be emphasized because AI has had
the greatest genetic impact in that species. Other spe-
cies overviewed include swine, horses, sheep, goats,
dogs, rabbits, poultry, and endangered species.
This review can only provide a taste of the important
discoveries and developments associated with AI and
the people most involved. A more comprehensive over-
view of the technical aspects of AI are available in many
of the books on AI and reproduction (Walton, 1933;
Anderson, 1945; Cole and Cupps, 1959; Maule, 1962;
Mann, 1964; Milovanov, 1964; Perry, 1968; Salisbury
et al., 1978; Watson, 1978; Brackett et al., 1981; Foote,
1981; Herman, 1981; Cupps, 1991). Also, several re-
views are available (Nishikawa, 1962, 1964, 1972; As-
dell, 1969; Bonadonna, 1975; Bonadonna and Succi,
1976; Foote, 1999).
Early History of AI
Leeuwenhoek (1678) and his assistant, Hamm, were
the first persons to see sperm, which they called “ani-
malcules.” Leeuwenhoek did not have an advanced for-
mal education, so he did not study Latin, the scientific
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Foote2
language of the day. However, he was a clever, capable
individual who ground lenses so precisely (one still ex-
ists today with 270 magnifications) that sperm were
visible. His published paper (Leeuwenhoek, 1678)
amazed, and perhaps amused, the reigning king of En-
gland, who regularly read papers submitted to the
Royal Society, where Leeuwenhoek’s paper was pub-
lished.
Another century passed before the first successful
insemination was performed by Spallanzani (1784) in
a dog, which whelped three pups 62 d later. Spallanzani
originally trained to be a priest, but he had a great
interest in natural history and pursued the latter. He
was a professor of natural history in Pavia by the age
of 25. He collected, analyzed, and classified a large
array of butterflies, shells, and other marine and land
animals. His abode was overrun with many collections,
somewhat to the consternation of relatives living there.
But he used these for rigorous, comparative objective
analysis to discern much about animal physiology and
characteristics of fitness.
Another 100 yr passed before Heape (1897) and oth-
ers in several countries reported that AI had been used
in isolated studies with rabbits, dogs, and horses. Heape
was an outstanding reproductive biologist, establishing
much of the basis for the relationship between seasonal-
ity and reproduction. This led to Cambridge becoming
a world center for reproductive studies (Marshall, Ham-
mond, Walton, and students such as M. C. Chang).
AI Becomes a Focal Point of Research
Pioneering efforts to establish AI as a practical proce-
dure were begun in Russia in 1899 by Ivanow (see Iva-
noff, 1922). By 1907 Ivanow (also transliterated as Iva-
nov or Ivanoff) had studied AI in domestic farm ani-
mals, dogs, foxes, rabbits, and poultry. Some of this
research, especially in horses, is included in a paper in
English (Ivanoff, 1922) submitted June 21, 1922, and
published in record time in the July 1922 issue of the
Journal of Agricultural Science. He developed semen
extenders and trained technicians to select superior
stallions and multiply their progeny through AI. Much
of the AI work in Russia was taken over later by Milova-
nov (1938), described in a text translated into English
(Milovanov, 1964). He established major projects for
sheep and cattle breeding. He did not E-mail his orders
for supplies. In his own workshop Milovanov designed
and made practical artificial vaginas and other items,
many similar to those used today. This was an enor-
mous improvement over the earlier method of collecting
semen from sponges placed in the vagina of mount
animals.
The development of AI by Ivanow also stimulated
research outside of Russia. The Japanese scientist Dr.
Ishikawa studied with Ivanow. He returned to Japan
and began a similar program in horses in 1912 (Nishi-
kawa, 1962). This gradually developed into AI being
applied in Japan in cattle, sheep, goats, swine, and
poultry. Other Japanese researchers became involved
(Ito, Niwa, Sato, Yamane, etc.). Because most of the
research was published in Japanese and few westerners
knew Japanese, little was known about this research
in the Western world until Niwa (1958) and Nishikawa
(1962, 1964, 1972) summarized the research in English.
News of the extensive use of AI in Russia following
the Ivanoff (1922) report became widespread in the
Western world with the publication of the book on AI
by Walton (1933). Walton conducted a number of experi-
ments, including a pioneering shipment of ram semen
to Poland, which 2 d later was used for successful insem-
ination of ewes. However, commercial AI did not evolve
rapidly in the United Kingdom.
Some AI work, particularly with horses, had been
performed in the early 1900s in Denmark. Eduard
Sørensen, at The Royal Veterinary College in Copenha-
gen, Denmark, was familiar with the Russian work.
With Gylling-Holm, Sørensen organized the first coop-
erative dairy AI organization in Denmark in 1936. The
program enrolled 1,070 cows the 1st yr and 59% con-
ceived, slightly better than natural service in the same
herds. This was an important stimulus for the develop-
ment of AI in dairy cattle in the United States and
other Western countries.
The Danish veterinarians established the method of
rectovaginal fixation of the cervix, allowing semen to
be deposited deeply into the cervix or into the body
of the uterus. This technique provided a tremendous
advantage because fewer sperm were required for in-
semination of each cow. Another Danish “invention”
was the straw for packaging semen (Sørensen, 1940).
In 1956 I saw some of the original oat straws that Dr.
Sørensen kept in his desk. Subsequently he saw chil-
dren at a birthday party for his daughter sipping punch
with cellophane straws, and he recognized that he had
found the straw that he needed. Later Cassou (1964)
produced straws commercially that have been used
worldwide. So, the French straw is a modified Danish
straw. Dr. Sørensen also was a tough examiner in anat-
omy. Passing his exams was reported to be as tough as
“getting a camel through the eye of a needle.”
Meanwhile, the much earlier research by Spallanzani
led eventually in Italy to the development of an artificial
vagina for dogs by Amantea in 1914 (Perry, 1968). This
work served as a model for the Russian development of
artificial vaginas for bulls, stallions, and rams. Another
Italian, Bonadonna (1937), continued research on AI in
several species. His enthusiasm for the potential value
of AI, along with Lagerlo
¨
f, resulted in the establishment
of the highly successful International Congress on AI
and Animal Reproduction held every 4 yr. The first one
was held in Milan in 1948. One time I remarked about
the extraordinary beauty of the Renaissance works of
art in Italy, and Dr. Bonadonna said “Yes, but remem-
ber the future requires that you do not spend too much
time dreaming about the past.”
In Sweden, Lagerlo
¨
f became known for his research
on infertility problems in bulls. This research was stim-
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History of artificial insemination 3
ulated by his visit with W. W. Williams, a Cornell
D.V.M., who had published methods of staining sperma-
tozoa. Meanwhile, Lagero
¨
f completed his classic Ph.D.
dissertation titled “Changes in the spermatozoa and in
the testes of bulls with impaired or abolished fertility”
(Lagerlo
¨
f, 1934). He established a group with worldwide
influence in training veterinarians in the various as-
pects of fertility and AI. Other Scandanavians, such as
Blom (1950), followed, publishing a steady stream of
excellent papers on abnormal sperm morphology (see
Barth and Oko, 1989). These pioneers were all thinkers
and doers, and they trained many who followed.
Modern Development of AI in Dairy Cattle
Phenomenal growth of AI occurred in the 1940s in
the United States. The procedures developed in the
United States became established worldwide (Salis-
bury et al., 1978). In 1936, Brownell was inseminating
cows in the Cornell herd (Sipher, 1991), and other AI
work was started in the late 1930s in Minnesota and
Wisconsin. In 1938, an AI cooperative was established
in New Jersey, modeled after the Danish system (Perry,
1968). Another one in 1938 followed in the state of New
York (Sipher, 1991). The development of the New York
Artificial Breeders, Cooperative, Inc., currently Genex,
Inc., in Ithaca, New York made possible the close collab-
oration between a farmer cooperative and researchers
and extension personnel at Cornell University. This
was a highly productive relationship resulting in the
experimental insemination of hundreds of thousands of
cows and publication of more than 100 research papers
(Foote, 1998) on sire selection, testicular evaluation,
semen collection, evaluation and processing; and fertil-
ity testing. The present status of AI in many countries
has been summarized recently (Malafosse and Thibier,
1990; Foote, 1999).
Semen Evaluation
The most widely used test of sperm quality from the
initial stages of AI development until the present time
has been the assessment of the proportion of normal,
progressively moving sperm (Anderson, 1945; Maule,
1962; Salisbury et al., 1978). Thus, a good microscope is
the key. In addition to examining sperm with brightfield
microscopes, differential interference contrast micro-
scopes, multiple stains, flow cytometry, and computer-
assisted sperm analysis (CASA) have contributed to
improved quantification of sperm motion (Graham,
1978; Salisbury et al., 1978; Pace et al., 1981; Garner
et al., 1997; Foote, 1998). With frozen semen, evaluation
of post-thaw survival became important. The ability to
evaluate the acrosomal status of sperm was enhanced
by the work of Saacke and Marshall (1968). Techniques
used for evaluating sperm morphology have been re-
viewed by Barth and Oko (1989).
Ejaculate volume and sperm concentration are the
two other critical components of semen evaluation be-
cause they determine the number of sperm obtained.
Volume originally was measured in graduated contain-
ers. Volume today often is determined more accurately
by weight, assuming that the specific gravity is 1.0.
Stallion semen was weighed years ago (Nishikawa,
1959). Rapid optical density methods for measuring
sperm concentration have replaced tedious hemocyto-
metric procedures.
Fertility of sperm is the ultimate test of sperm qual-
ity. Often it is not possible to measure fertility, so many
tests of semen quality in addition to motility and mor-
phology, such as the hypoosmotic swelling test, mucous
or gel penetration, and integrity of the DNA have been
correlated with fertility (Graham, 1978; Saacke, 1981;
Foote, 1998, 1999). Competitive fertilization (Beatty,
1960; Saacke, 1981; Dziuk, 1996; Foote, 1998) with
mixed sperm offers an efficient way to rank the fertility
of males either using in vitro fertilization tests or tests
with animal insemination. However, it is not generally
feasible to mix semen in commercial AI. For commercial
AI, an inexpensive method of estimating fertility, based
on cows not returning for insemination, was developed
as an essential component of the AI program (Thomp-
son and Salisbury, 1947). This made possible the com-
paring of fertility of bulls, inseminators, semen pro-
cessing procedures, and even herd performance under
practical field conditions. It provided a remarkable new
system of recording breeding efficiency. Others had ar-
gued strongly for using pregnancy diagnosis, but this
clearly involved few cows, was performed sporadically,
and did not provide for centralized collection and evalu-
ation of data. The efficiency of the nonreturn method for
monitoring fertility is reduced today because of multiple
suppliers of semen to individual farms and within-
herd inseminators.
Semen Extenders, Semen Cooling, and Extension Rate
Initially the most important problem to resolve was
a method to store semen long enough for shipment and
use in the field. The first major improvement in the
AI procedure initiated in the United States was the
development of a yolk-phosphate semen extender (Phil-
lips and Lardy, 1940). Salisbury et al. (1941) improved
the media by buffering the egg yolk with sodium citrate.
Sperm survival at 5°C permitted use of the semen for
up to 3 d, and the citrate dispersed the fat globules in
egg yolk, making sperm visible for microscopic exami-
nation. This semen extender was used worldwide for
cattle. Glycerol was added later for cryopreservation of
bull sperm.
The next major stimulus to AI of dairy cattle was an
improvement of about 15% in fertility resulting from a
better method of initially protecting sperm from cold
shock (Foote and Bratton, 1949) and the control of some
venereal diseases by the addition of antibiotics (Alm-
quist et al., 1949; Foote and Bratton, 1950). The Cornell
extender (Foote and Bratton, 1950), containing the anti-
biotic mixture of penicillin, streptomycin, and poly-
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Foote4
myxim B, was used for many years as the standard.
Many years were required to eradicate the diseases
from bulls. During that time in vitro treatment of semen
with antibiotics prevented transmission of several dis-
eases. Antibiotics are still included as “insurance” pro-
tection against possible contamination. This treatment
of semen was worth hundreds of millions of dollars to
the dairy world. No patents were filed, and neither
Pennsylvania nor Cornell received any remuneration.
The reward was service to agriculture. Growth of AI was
now ensured, because dairies using only AI eliminated
venereal diseases, reduced embryonic death, and
achieved high fertility.
With AI expanding rapidly, demands for semen from
popular bulls increased. The simplest way to meet this
demand was to “stretch” each ejaculate farther by using
fewer sperm per insemination, providing that this could
be accomplished without sacrificing fertility. Salisbury
and coworkers published several classic papers (see
Salisbury et al., 1978; Foote, 1998) clearly supporting
the concept that only a few million sperm per insemina-
tion were required. In conducting these experiments
Salisbury was criticized by some who declared that “di-
lution” of semen was like “watering the milk.” Conse-
quently, Foote and Bratton (1950) introduced the word
“extender” because the yolk-citrate-antibiotic medium
enhanced and extended the usefulness of semen. This
word has “stuck.” We considered using the word “sus-
pender” as a snappy term, also. The net result of these
experiments was that semen extension could be in-
creased at least 25-fold. Sperm numbers per insemina-
tion with liquid semen were reduced from more than
100 × 10
6
sperm per insemination to 4 × 10
6
sperm per
insemination (see Salisbury et al., 1978; Foote, 1998).
Along with hard work in the laboratory, Salisbury’s
graduate students remember relaxing over gourmet
food in his home.
The yolk-based extender was improved with Cornell
University Extender (CUE, Foote et al., 1960), which
resulted in the highest fertility achieved in AI on hun-
dreds of thousands of inseminations (Salisbury et al.,
1978; Foote, 1998). Shannon visited Cornell in the late
1950s and modified the extender (Shannon et al., 1984)
for use with liquid semen in the intensive breeding
season in New Zealand. Caproic acid and catalase were
included with 5% egg yolk by volume to form “Capro-
gen,” an effective extender for preserving bull sperm at
the moderate ambient temperatures of New Zealand,
with as few as 2 × 10
6
sperm per insemination. Several
researchers (see Salisbury et al., 1978; Foote, 1998) had
reported that the volume of egg yolk used originally
could be greatly reduced, particularly at ambient tem-
peratures, and that catalase might be beneficial at
room temperature.
Milk also was widely used. Following the report by
Michajilov (1950), Almquist and coworkers (Thacker
and Almquist, 1953; O’Dell and Almquist, 1957; Alm-
quist and Wickersham, 1962) published a series of pa-
pers on skim milk and whole milk, establishing the
optimal procedures for detoxification of milk and addi-
tion of glycerol for freezing semen. The milk-glycerol
extender continues to be used by many AI organi-
zations.
Bull Sexual Behavior, Intensity of Semen Collection,
and Sire Power
To meet the high demand for semen from selected
bulls, harvesting the maximal number of sperm per
bull was the other approach to increasing the number
of inseminations possible per bull. Early research on
sexual preparation and intensity of semen collection
was initiated by Bratton and colleagues (Collins et al.,
1951; Bratton and Foote, 1954; Hafs et al., 1959) and
Almquist and colleagues (Hale and Almquist, 1960;
Amann, 1970; Almquist, 1973, 1982). The extensive
studies by Almquist and associates included beef bulls
as well as dairy bulls (Almquist, 1973). These collective
studies resulted in recognizing the importance of evalu-
ating the sexual responses of individual bulls and
applying stimuli along with an optimal frequency of
about six semen collections per week. The result was
a sperm output of 30 to 40 × 10
9
sperm per week per
sire. With a 50-wk-per-year collection schedule and 10 ×
10
6
sperm per insemination dose, these sperm numbers
translate into 200,000 doses of semen for insemination
each year.
Large differences occurred in sperm output of bulls
when semen was collected under comparable condi-
tions. Methods were developed to evaluate both the
quality and quantity of spermatogenesis in bulls (Foote,
1969; Amann, 1970). These studies revealed that the
differences in sperm output were largely due to testicu-
lar size. Testis size was easily measured and was highly
inherited, h
2
= 0.67 (Coulter et al., 1976). So, attention
to testis size was important in selection and evaluation
of sires.
Extensive studies were conducted on nutrition, per-
formance, and aging of bulls (see Foote, 1998). Rapid
growth was important in minimizing the time required
for young bulls to reach puberty and be tested for AI.
Unfortunately, these data are largely unknown because
they were published in bulletin form (Bratton et al.,
1959, 1961), although one classic paper appeared in a
journal (Almquist, 1982). Almquist always kept an open
mind about what might be possible. At one scientific
meeting he handed out note pads less than 1 inch wide
and several inches long to remind people not to be “nar-
row-minded.” Bratton was a perfectionist and did not
publish results until the experiments were completed,
even if they took 10 yr. Tenure then was translated as
10 yr.
Genetic Selection of Bulls for Milk
One of the major reasons for initiating AI was to
make the males that transmit superior genetics for milk
production available to more producers in the animal
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