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Factors associated with early

embryonic mortality
VERN L. CHRISTENSEN
Department of Poultry Science, North Carolina State University, Box
7608, Raleigh, NC 27695-7608, USA

This paper describes the patterns of embryonic mortality in poultry species and
summarises the various causes of mortality. Descriptions of the morphological
stages of development at each of these time periods are given. Data are
presented describing factors affecting development at oviposition, egg storage
and incubation.
~ ~

Keywords: Embryonic development; embryonic growth; embryonic survival

Introduction
Embryonic mortality does not occur randomly at all days of incubation
(Christensen, 1978; Lerner et al., 1993; Krueger, 1993). More embryos die in the
first and third trimesters than in the second. The frequency of ”early embryonic
mortality” has been observed to increase between 2 and 4 days in the chicken and
between 3 and 6 days in the turkey (Hutt and Pilkey, 1930; Insko and Martin, 1935;
Christensen, 1978; Lerner et al., 1993; Krueger, 1993).When comparisons are made
between older (Hutt and Pilkey, 1930; Insko and Martin, 1935) and more recent
studies (Lerner et al., 1993; Krueger, 1993), the increased frequencies of mortality
at these early stages of incubation are similar at both periods of time.
Many physiological and genetic events occur during the initial days of
development. A brief description of these events is included below. The
development is far more complex than is portrayed below, so the reader
interested in greater detail is referred to additional papers (Hamburger and
Hamilton, 1951; Eyal-Giladi, 1984; Gupta and Bakst, 1993). In the chicken Eyal-
Giladi and Kochav (1984) stages I-X occur before oviposition and stages XI-XI11
occur within the first 24 hours of incubation. The remaining stages discussed in
the current paper are described by the Hamburger and Hamilton (1951) stages
1-24. In the turkey Gupta and Bakst (1997) stages I-VII occur before oviposition
and the subsequent stages VIII-XI11 occur during the first 48 hours of incubation.
The remaining stages are described by the Hamburger and Hamilton (1951)
stages 1-18.
0 World’s Poultry Science Association 2001
Worlds Poultry Science Journal, Vol. 57, December 2001
Factors associated with early embryonic mortality: V.L. Christensen
Preoviposital development
Development of the avian embryo begins immediately after fertilisation (Fasenko,
1992) in the infundibulum and continues within the body of the hen at 41.5"C
(Whittow, 1986) for 24-26 hours. The first cleavage is somewhere in the isthmus
6-8 hours after ovulation. The initial development is called phylogenesis because
structures and events (i.e. gastrulation) that are common among animal species
are differentiated at these stages. After fertilisation the ovum is transported to the
shell gland (uterus). By this time, a flat disc of active cytoplasm called the
germinal disc is on the surface of the yolk and is beginning to cleave (Eyal-Giladi,
1984)or is just before the point of cleavage in some domestic avian species (Gupta
and Bakst, 1993).For the next few hours in the shell gland or before the cooling
of the egg following oviposition, cleavage of the germinal disc continues (stages
I-VI according to Eyal-Giladi and Kochav (1976) or stages 7-10 according to
Gupta and Bakst (1993)).By the end of cleavage the germinal disc, now known as
a blastodisc (Eyal-Giladi, 19841, is approximately five or six cells thick at the
centre and one to two cells thick at the periphery (Bellairs, 1971). The blastodisc
is separated from the yolk by a fluid-filled cavity, the subgerminal cavity (Eyal-
Giladi, 1984; Watt et al., 1993).
The final 8-9 hours spent in the shell gland involves the first morphogenic
movements of blastodisc cells into two distinct regions - the area pellucida and
the area opaca (stages VII-X of Eyal-Giladi and Kochav (1976)).As these two areas
differentiatethe diameter of the blastodisc also increases (Eyal-Giladi and Kochav,
1976; Gupta and Bakst, 1993).The blastodisc is now referred to as the blastoderm.
At the time of oviposition, most domestic poultry embryos consist of
30 000-60 000 cells (Eyal-Gialdi and Kochav, 1976; Gupta and Bakst, 1997).

Development of embryos following 24 hours of incubation


Because of its importance in understanding early embryonic mortality, the early
ontogeny of the avian embryo will be briefly described using the Hamburger and
Hamilton (1951) stages of development. Ontogeny is the differentiation of
structures and the embryological events that delineate animal species from each
other. For further information the reader is referred to other sources (Phillips and
Williams, 1944; Hamburger and Hamilton, 1951; Eyal-Giladi and Kochav, 1976;
Christensen, 1978; Gupta and Bakst, 1993). At this stage the embryo is
characterised by its distinct appearance: starting from the periphery of the
blastoderm there is a "ring" of area opaca, then a "transparent belt" of area
pellucida, and in the centre of the blastoderm is the solid circle of hypoblast cells.
The entire embryo is approximately 0.5cm in diameter and is characterised by the
primitive streak that is plainly visible to the unaided eye. Neural folds show at the
cephalic end. The areas pellucida and opaca are visible and form the so-called
"doughnut". The area opaca at this stage is clearly divided into an inner mottled
area vasculosa and an outer lighter area vitellina. Blood islands are abundant
within the area vasculosa and in slightly older embryos it may be possible to see
the formation of the early embryonic blood vessels.

Development of embryos following 48 hours of incubation


Typically, four somites are present. Neural folds anastomose in the head region.
The anterior neuropore is open and sinus rhomboidalis is present. The optic

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Factors associated with early embryonic mortality: V.L. Christensen
vesicle regions begin to bulge. The three major brain divisions are present. No
lateral body folds exist.

Development of embryos following 72 hours of incubation


Typically, 10 somite pairs are present and no primitive streak exists. The anterior
neuropore is not visible and the neural folds are fused to the region just posterior
to the heart. The sinus rhomboidalis is present and the optic cups are formed. The
head and heart regions are covered by the amnion. The extra-embryonic
circulatory system is complete, but no pumping action of the embryonic heart is
visible at this stage of development. No blood is visible, only a few blood islands.
No visceral clefts or arches are present. The upper half of the body begins torsion
to the right (cephalic flexure). The auditory pits are plainly visible.

Development of embryos following 96 hours of incubation


Typically, 38 pairs of somites are present. The amnion covers almost the entire
embryo. The telencephalon is prominently bulged to form the cerebral hemi-
spheres and the fissures of the midbrain and the hindbrain appears. Distinct
divisions of the heart are noticeable and the heart performs pumping. Blood is
clearly visible. Head, cervical, pontine and tail flexures are present. The allantois
is visible. The sinus terminalis is approximately 2.5 cm in diameter. Anterior and
posterior wing and leg buds are visible.

Factors affecting embryonic liveability


Ideally, every fertile egg should produce a healthy hatchling. In commercial
poultry production, however, this optimum is never achieved. The situation is
complicated by a number of factors affecting embryonic liveability These range
from lethal chromosomal abnormalities (Shook, 1969; Shook et al., 1971) to
insufficient availability of nutrients in the egg (Byerly et al., 1932)and the fact that
eggs may be exposed to conditions which do not match the demands of the
developing embryo (Meijerhof, 1992). The factors that may influence the
liveability of early developing embryos of poultry are summarised in Table 1.

Development at oviposition
The stage of embryonic development at oviposition influences hatching results.
Differences in stages of embryonic development at oviposition were reported
many years ago (Hays and Nicolaides, 1934).They reported that pre-gastrula and
early gastrula stages were common in eggs from birds with poor hatching results,
while eggs from birds with good hatching results contained embryos at an
advanced gastrula stage.
The age of the breeder hen may influence the developmental stage at
oviposition. Mather and Laughlin (1977) have reported that the blastoderm area
in fresh unincubated eggs increased with parental age. When incubated, the
development of embryos in eggs laid by older birds was advanced. This is in
agreement with results of Crittenden and Bohren (1962),Smith and Bohren (19751,
Kirk et al. (1980) and Fasenko (1992).
The time of day an egg is oviposited has also been implicated as a factor in the
survival of the early developing embryo (Hutt and Pilkey, 1930, 1934). The time
spent in the oviduct, determined by the length of the oviduct and/or the passage

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Factors associated with early embryonic mortality: V.L. Christensen
Table 1 Factors during the production period reported to influence hatching results and the
possible sources of reported differences

Stage Possible sources Possible mechanisms

Development at Genetics Genetic differences


oviposition Age of hens Ovulation intervals
Time of oviposition Time in oviduct
Egg weight and quality Maternal investment
Body temperature pH, albumen, C 0 2 , embryo metabolism,
chemical/physical properties
Egg storage Genetics Type of egg
development Nest type Cooling rate of eggs
Collection rate Cooling rate of eggs
Heat conductance value Cooling rate of eggs, escape of CO,
of egg components
Egg quality Eggshell porosity
Time in storage pH, C 0 2 and chemicals
Temperature Chemical/physical properties
Humidity Unknown
Incubation Temperature Chemical/physical properties
development Humidity Chemical/physical properties
Ventilation Chemical/physical properties
Turning Adherence to membranes, angiogenesis
Genetics Apoptosis, DNA regulation
Semen storage Unknown
Age of hen Embryo growth rates
Egg storage Embryo growth rates, pH, C 0 2

rate of the egg, will influence the developmental stage. Bernier et al. (1951)
reported that first and last eggs of clutch sequences contained more advanced
embryos, both at oviposition and after a short period of incubation, than
intermediate eggs. Sturkie (1986)reported that eggs in the terminal position in the
sequence remain in the oviduct for a longer period. Coleman et al. (19641,
however, reported that the correlation between embryonic development after 48
hours of incubation and the egg’s position in the clutch sequence was low.
Fasenko (1992) observed a more advanced stage of embryonic development in the
first of a sequence of eggs.
Embryos from eggs laid in the afternoon had slighter lower survival rates than
those from eggs laid in the morning (Hutt and Pilkey, 1930; Funk, 1934a; Moore,
1959; van Middlekoop, 1972; Fasenko, 1992). Others have noted no differences
between the time of day an egg is laid and the embryo survival rate (Nicolaides,
1933; Hays, 1937; Kumanov, 1948). Turkey eggs laid before 17.00 hours have
almost 10% better hatchability than those laid later in the day (Shook, 1969;
Christensen, 1978).
It has been reported from several laboratories that advanced embryonic
development occurs in populations selected for low body weight in both
domestic fowl (McNarry et a1.,1960; Coleman et al., 1964) and turkeys (Weisbroth,
1960; Kosin and Mun, 1965; Arora and Kosin, 1964, 1966). Turkeys selected for
heavy mature body weight produced eggs that more frequently contained
embryos at an early gastrula stage than those from birds selected for low body
weight (Arora and Kosin, 1966). Groups at an advanced stage of development at
oviposition showed a higher rate of development in the first few days of

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Factors associated with early embryonic mortality: KL. Christensen
incubation. In a similar study Coleman and Siegel (1966) reported that hens
selected for low body weight at 8 weeks of age produced eggs with superior
embryonic development at oviposition and an increased survival rate than those
of hens selected for high body weight.
In early studies there was apparent agreement that eggs of average size had less
well developed embryos than large eggs (Marble and Margolf, 1936; Byerly and
Marsden, 1938; Insko et al., 1943; Brunson and Godfrey, 1953; Kosin, 1957).
McNally and Byerly (1936) suggested that egg weight might be positively
correlated with the early development of embryos, and this may explain the
differences observed between birds of different ages. Fasenko (1992) reported that
embryonic development was positively correlated with egg weight as well as
with shell weight. Coleman et al. (1964) noted a positive correlation within lines
between egg weight and embryo development after 42 hours of incubation.
However, Arora and Matsumoto (1968) and Mather and Laughlin (1979) reported
no significant relationship between egg weight and the stage of development after
2 days of incubation. Egg size is a multifaceted variable. Thus, because many of
the previous observations may have been confounded with the genetic back-
ground or the age of the hen, conclusions concerning egg size and embryonic
development are difficult to make. Nonetheless, the preponderance of evidence
indicates a positive relationship between egg size and embryonic development
early in incubation.

The embryo during storage


Normally eggs are stored at the farm, transported to the hatchery, stored at the
hatchery in a cool room and then set into incubators. Orientation of the egg
during storage is normally with the pointed end downwards (Funk, 193413;
Proudfoot, 1967) because the blastoderm is invariably found beneath a restricted
equatorial belt of approximately 1.5cm. When embryos are found outside this
equatorial belt they are generally dead (Romanoff, 1960). In contrast, Proudfoot
(1967, 1969, 1976) failed to concur with Romanoff's (1960) observation. Duration
of the storage period may vary from 1 day to more than 1 week, depending upon
the distance between the farm and hatchery, the capacity of the hatchery and the
market conditions. The temperature history of the egg depends on the type of nest
(Fasenko et al., 1991; Meijerhof, 1992), the time of oviposition, the time and
frequency of egg collection and the environmental conditions in the house (Kirk
et al., 1980; Fasenko et al., 1991). The effects of these factors might be attributed to
differences in the rate of egg cooling and explain why embryo development is
reported to influence hatchability (Kosin, 1956; Skoglund and Brown, 1956;
Becker and Bearse, 1958; Coleman and Siegel, 1966).
Storage of eggs before incubation leads to morphological changes in the
embryo (Byng and Nash, 1962; Bakst and Gupta, 1997). It was observed many
years ago that storage of hatching eggs from 8 to 27 days increased the size of
embryos dramatically as well as the number of embryonic abnormalities (Olsen
and Marsden, 1950; Arora and Kosin, 1966; Weisbroth and Kosin, 1966; Mather
and Laughlin, 1977; Fasenko, 1992). A staging system for six stages of the
regression of blastoderms during egg storage has also been proposed (Olsen and
Marsden, 1950; Arora and Kosin, 1966).Singal and Kosin (1969) reported a slower
growth rate following extended storage and Mather and Laughlin (1979)
observed shrinkage of the blastoderm during storage and a delay in the initiation
of development following storage. Bakst et al. (1997) and Bakst and Gupta (1997)

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Factors associated with early embryonic mortality: V.L. Christensen
saw no changes in the development of the blastoderm (turkey staging procedure)
before and after long term egg storage. They suggested that, while the
development of the embryo is arrested during cool storage, morphological
changes take place. An interesting characteristic that has been observed for many
years is that storage of eggs for a few days seems to have a beneficial effect on the
embryonic survival rate (Scott, 1933; Asmundson, 1947; Asmundson and
MacIlraith, 1948; Funk et al., 1950; Becker et al., 1964; Christensen, 1978).
Heritability estimates of the declines in viability as storage periods increase
were very low, but the decline when eggs are held for longer than 8 days was
more highly heritable than was the decline seen when the holding period was less
than 8 days (Abplanalp and Kosin, 1953). Shook (1969) showed that, although
selection for reduced early embryonic mortality could be difficult because of low
heritability estimates, selection for increased embryonic mortality could be
effected quite easily.
The decrease in the viability of the embryo may be caused by changes in the
embryo or by changes in other components of the egg. Spratt (1947) indicated that
the most important factor in maintaining viability of stored hatching eggs was
stabilisation of the vegetal components (yellow yolk) of the egg. The stabilisation
of the animal components (white yolk) appeared to be less critical. In view of this
hypothesis it is not surprising that much effort has been expended in attempts to
stabilise the vegetal components of the egg. Whether changes to the vegetal
component of the yolk are responsible for the morphological changes of the
blastoderm after prolonged storage is not known.
Temperature is a major factor influencing the stabilisation of egg components
(Butler, 1990). The concept of a physiological zero (the temperature at which
development is arrested totally) becomes important in such considerations.
Edwards (1902) suggested that this temperature lies between 20 and 21"C, based
on earlier work by Dareste and Kaestner (both cited by Edwards (1902)),whereas
Funk and Biellier (1944) suggested 28°C. Lundy (19691, citing other work,
concluded that "physiological zero" lies between 25 and 27°C. Reduced
temperature does slow the decline in embryonic survival seen when eggs are held
for longer than 1 week (Olsen and Haynes, 1948; Landauer, 1967; Funk and
Forward, 1960; Proudfoot, 1964a,b; 1970). An interaction between the holding
time and temperature has also been noted (Proudfoot, 1964a,b; 1969; 1976; Becker
et al., 1967; El Jack and Kalthofen, 1969; Kalthofen and El Jack, 1972; Kirk et al.,
1980). Periodic warming of the eggs during storage has been reported to
overcome the problem (Jackson, 1912; Kosin, 1956; Becker and Bearse, 1958; Kan
et al., 1962; Proudfoot, 1964a,b; 1965; Fasenko, 1992).
The relative humidity during egg storage also influences embryo viability
(Proudfoot, 1969; Reinhart and Hurnik, 1982). Optimal relative humidity for
embryo survival during egg holding lie between 75% and 90%. In this context an
important consideration is the interactions between ventilation and humidity and
temperature. Air movement past eggs does not affect water loss (Kalthofen, 1969;
Spotila et al., 1981) unless it changes the temperature or humidity (Cooney, 1943;
Funk and Forward, 1951).
Keeping eggs in a closed atmosphere using plastic bags reduces gas exchange
and may preserve internal egg quality during storage (Davis and Beeckler, 1962;
Becker, 1964;Warren et al., 1965; Gordon and Siegel, 1966; Becker et al., 1967; 1968;
Kosin and Konishi, 1973). Becker (1964) postulated that the improvement
observed in embryonic survival resulted from the alteration in the amount of
carbon dioxide lost from the egg and the consequent rise in the pH of the egg's

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Factors associated with early emby o n i c mortality: V.L. Christensen
albumen. Subsequent attempts to verify this postulate have produced conflicting
results (Becker et al., 1968; Proudfoot, 1964a, 1965; Benton, 1998).
Proudfoot (196413) observed a deleterious effect on hatchability by flushing
plastic bags containing fertile eggs with carbon dioxide and an enhancement in
embryonic survival rate from flushing with nitrogen. Gowe (1965) confirmed the
beneficial effects from nitrogen flushing, and Pierce (1974) suggested that this gas
might be involved in protein synthesis during embryonic development. Kosin
and Konishi (1973) reported no benefit from flushing eggs in plastic bags with
nitrogen. Romanoff and Romanoff (1949) have suggested that oxygen is required
during egg storage to satisfy continuing enzymatic activity. The optimum
atmospheric conditions for storage within a gaseous environment remain
undefined with respect to carbon dioxide, nitrogen, oxygen and water vapour.
Enos et al. (1974) have suggested that aqueous storage of hatching eggs might be
superior to atmospheric storage for embryonic survival.

Development during incubation


In general, the embryonic survival rate decreases with increased temperature,
with increased exposure time and with younger embryos (Alsop, 1919; Deuchar,
1952; Landauer, 1967; Lundy, 1969; Ande and Wilson, 1981; Stikeleather Swann
and Brake, 1990). As hyperthermia increases, embryonic growth decreases or
stops and the incidence of malformations increases (Tazelaar, 1929). High
incubator temperatures during the first 3 days causes increased brain and neural
tube abnormalities (Alsop, 1919). The area vasculosa and its blood vessels are
most susceptible to an uneven temperature gradient (Tazelaar, 1929). Hyper-
thermia during the first 6 days of incubation causes eye abnormalities, which
were suggested to be the result of circulatory abnormalities (Nilsen, 1968).Others
have reported heart and kidney enlargement, thought to be an indirect
haemodynamic response to congestive heart failure or arterial hypertension
(Leighton et al., 1964), and it has been suggested that embryos undergoing
gastrulation are more severely affected by the inhibition of invagination and the
longitudinal extension of invaginated tissues (Deuchar, 1952). A myriad of
conditions has been attributed to hypothermia. These involve circulatory
problems and enlarged hearts (Leighton et al., 19641, arrhythmia and cardiac
arrest (Tazawa and Rahn, 19861, decreased density of the amniotic fluid and
volume (Romanoff and Hayward, 19431, declines in hepatic glycogen and blood
sugar (Freeman, 1967), retarded growth of the area vasculosa and reduced yolk
utilisation (Deeming, 1989). As embryos age, the sensitivity to hypothermia
increases (Taylor et al., 1933; Romanoff, 1939; Moreng and Bryant, 1954; Romanoff,
1960; Wilson, 1990). A rapid cooling rate is much more damaging to the embryo
than is a slow rate (Moreng and Bryant, 1955). Embryos cooled to 28°C or near to
physiological zero will enter torpor from which they are able to make a full
recovery (Tazawa and Rahn, 1986, 1987). Recovery depends upon the length of
the torpor, the age of the embryo and the temperature.
The relative humidity controls the degree of hydration of an egg during
incubation (Ar, 1990) and may be age dependent. Embryos early in their
development have been thought to be very resistant to a wide rate of desiccation
(Simkiss, 1980; Tullett and Burton, 1982).Eggs that are severely desiccated early in
incubation are harmed to a greater degree than those desiccated later in
development (Snyder and Birchard, 1982). In contrast, Meir and Ar (1986) and
Hulet et al. (1987)showed clearly that eggs losing too much or too little water early

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Factors associated with early embryonic mortality: V.L. Christensen
in incubation can be returned to a normal degree of hydration without significantly
harming embryonic survival. The albumen is known to increase in osmolarity as
the result of evaporation early in incubation and this may be a major factor in
stabilising the vegetal components of the egg (Seymour and Piiper, 1988).
Low rates of oxygen and carbon dioxide diffusion are typical of eggs of many
species during the initial 22% of the incubation period (Tullett and Board, 1976).
This may be a requirement for stabilising the vegetal portion of the egg by
retarding carbon dioxide diffusion during the early stages of embryogenesis
(Raddatz et al., 1987).The amount of oxygen required for early development and
survival is very small but increases exponentially after about 16 days of
incubation in the chick embryo (Rahn and Paganelli, 1990). When Taylor et al.
(1956) varied the carbon dioxide and oxygen concentrations only during the first
4 days of incubation, normal embryonic survival resulted when carbon dioxide
varied between zero and 1%, whereas embryonic survival was reduced at
concentrations greater than 1.1%.Embryos up to 48 hours of incubation appeared
to be more resistant to the higher concentrations than were the 48-96 hour
embryos. During this time the embryo appeared to be very resistant to high
oxygen concentrations but very susceptible to reduced oxygen concentrations.
Combining the stress of high carbon dioxide with low oxygen had additive effects
in decreasing embryonic survival during the first 4 days of incubation (Barott,
1937).As the embryos aged past 4 days of incubation, the tolerance to high carbon
dioxide and low oxygen concentrations increased.
During incubation eggs are turned a minimum of three times per day 20-45
degrees from the horizontal plane in one plane until approximately the 10th day
of incubation (Wilson, 1990).Turning prevents the embryo from adhering either
to the inner shell membrane and resulting in its death, or to the yolk causing
rupture of the vitelline membrane (Eycleshymer, 1907; Chattock, 1925; Buhr,
1989).Premature adhesion is prevented when eggs are turned for at least the first
7 days of incubation. Turning also facilitates the embryo positioning into the
normal hatching profile (Insko and Martin, 1933; Olsen and Byerly, 1936).
Deeming (1989) observed that the failure to turn had an inhibitory effect on the
fusion of the chorionic and allantoic membranes to form the chorioallantoic
membrane and fluid was frequently found between the two membranes. Turning
stimulated growth of the area vasculosa, yolk utilisation and embryonic growth.
Vince et al. (1979) found that turning increased embryonic heart rate, and it has
been suggested that turning may reduce a thermal gradient across the egg
(Roberston, 1961). The cause of mortality from lack of turning may be related to
decreased albumen utilisation, a deficiency in subembryonic fluid decreasing the
oxygen exchange surface area or reduced area vasculosa growth.
Although selection for early embryo liveability during incubation has had little
success (Wilson and Johnson, 1946; Abplanalp and Kosin, 1953; McCartney, 1962;
Nestor, 1971; Nestor and Noble, 1995>, selection for increased embryonic
mortality over a 3 year period has increased embryonic deaths (Shook et al., 1971).
Recent data concerning the cellular and cytokine basis for apoptosis may give an
insight into improving survival during hypoblast formation (Bloom et al., 1998;
Muscarella et al., 1998).
Semen storage for extended periods of time can increase the incidence of early
embryo deaths (Dharamarjan, 1950; Huyghebaert et al., 1984; Fairchild and
Christensen, 1999). Inseminations that bypass biological barriers in the oviduct
can also increase the incidence of early embryo deaths (Van Krey et al., 1966;
Ogasawara et al., 1967; Besulin and Sakhatsky, 1974).

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Factors associated with early embryonic mortality: V.L. Christensen
The age of the dam affects early embryonic mortality as well. The first eggs laid
by pullets have an unusually high incidence of early embryonic mortality (Sunde
and Bird, 1959; Fairchild and Christensen, 1999) as well as producing a high
number of malformations. As hens age into the second and third years, the
survival of their offspring during the early incubation period increases at an
increasing rate (Leighton et al., 1971; Woodard et al., 1976; Krueger, 1993).

Conclusion
This review has attempted to describe factors associated with the premature
death of avian embryos. It has not included an extensive review of genetic, toxic
or nutritional factors, information on which the reader is referred elsewhere
(Landauer, 1967; Lundy, 1969) for more information. It is hoped that, with this
simplified approach, attention will be focused on the detailed regulatory
processes that govern early embryonic survival.

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