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Ultrasonography for pregnancy diagnosis and evaluation in queens
Theriogenology 66 (2006) 135–144 www.journals.elsevierhealth.com/periodicals/the
Ultrasonography for pregnancy diagnosis and evaluation in queens D. Zambelli *, F. Prati Veterinary Clinical Department, Obstetrical and Gynaecological Section, University of Bologna, Via Tolora di Sopra 50, 40064 Ozzano Emilia, Bologna, Italy
Abstract In the present paper, we describe the clinical utility of ultrasonography for diagnosing and evaluating pregnancy in domestic cats. Ultrasonography is a non-invasive technique that permits an accurate diagnosis of pregnancy and allows serial evaluation of the developing embryo/fetus and the extrafetal structures. The first ultrasonographic indication of pregnancy is a gestational chamber seen on day 10 after mating as a small circular anechoic structure. From day 30, it is possible to recognize different fetal organs, and between 38 and 43 days, the gender of the fetus can be determined. Measurements obtained during the second half of gestation can be used to determine fetal age and calculations can then be made that may more accurately predict the time of parturition. Further studies are needed in the queen to determine the applicability of the echo-Doppler technique used routinely in human obstetric medicine. This type of ultrasonography could potentially provide useful information about fetal health and the maturity of the placenta. # 2006 Elsevier Inc. All rights reserved. Keywords: Cat; Pregnancy; Ultrasound
1. Reproduction overview
2. Methods of pregnancy diagnosis
Female domestic cats are seasonally polyestrus and ovulation occurs between 24 and 48 h after coitus. Ova are fertilized in the oviduct and then pass into the uterine horns as morulae by days 5–6 postcoitus [1]. After implantation, which occurs 13–14 days after ovulation, the pregnancy continues to develop with relatively consistent chronological events (Figs. 1 and 2). The placenta is endotheliochorial in structure and zonary in shape. Parturition usually occurs between 63 and 67 days following conception [2].
Different methods may be used for pregnancy diagnosis of the queen, including abdominal palpation [2], radiography [3] and ultrasonography [4]. The laboratory tests commonly used for pregnancy assessment in other domestic animals are currently not applicable to the cat.
* Corresponding author. Tel.: +39 051 2097989; fax: +39 051 2097568. E-mail address: [email protected] (D. Zambelli). 0093-691X/$ – see front matter # 2006 Elsevier Inc. All rights reserved. doi:10.1016/j.theriogenology.2006.04.004
2.1. Palpation Careful palpation of the pregnant uterus through the abdominal wall is the most practical and rapid method of pregnancy diagnosis. It is most successfully performed within 21–25 days after mating when each fetal vesicle is approximately 2.5 cm in diameter. After day 35 of gestation, the uterine swellings become confluent and diagnosis becomes more difficult.
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Fig. 1. Schematic illustration of embryo formation and subsequent implantation (graphic by D. Zambelli).
2.2. Radiography A positive diagnosis of pregnancy can also be made with radiography. Fetal skeletal calcification becomes visible by radiography between 36 and 45 days after breeding [3] even though uterine embryonic swelling of 1.2–2.5 cm may be visualized as early as 17–21 days. 2.3. Ultrasonography Ultrasonography is a non-invasive and inexpensive technology. In the queen, pregnancy can be diagnosed by ultrasonography from 10 days after mating. In addition, fetal age can be assessed, fetal viability confirmed and, possibly, fetal abnormalities can be
determined. Generally, ultrasound units with 7.5– 10 MHz sector transducers can be used. 3. Ultrasound aspects of extrafetal structures 3.1. Uterus, gestational chamber and placenta [5] The earliest ultrasonographic indication of pregnancy in the queen may be the presence of an early (day 4) physiological uterine hyperplasia, although this appearance is common to both gravid and non-gravid queens in diestrus. The gestational chamber, which appears as a small circular anechoic structure normally visible on day 10 of pregnancy (Fig. 3), progressively increases in size from 6.9 mm on day 10 to about
Fig. 2. Longitudinal and transverse (E1–H1) section of gestational chamber. Development of fetal and extrafetal structures shown on days: (A) 10, (B) 14, (C) 16, (D) 17 and 18, (E) 20, (F) 22, (G) 25 and 26 and (H) 30 (graphic by D. Zambelli).
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Fig. 3. Day 10 of pregnancy: ultrasound longitudinal section of the uterus. A gestational chamber (C) can be seen.
35.7 mm on day 30. There is a consequent loss of the spherical shape of the gestational chamber as it undergoes slight elongation toward the classical ‘‘lemon’’ outline. On day 16 of pregnancy, the developing placenta can be recognized within the gestational chamber as two hyperechoic lines separated by a hypoechoic line (Fig. 4). This stratified appearance is maintained throughout pregnancy. From day 25 it is possible to
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Fig. 5. Day 25 of pregnancy: ultrasound longitudinal section of the uterus. Corion leave (Cl) in comparison with the placenta zonata (P) that appears hyperechoic at the level of its internal and external surfaces, while it is hypoechoic in the center.
distinguish the zonary nature of the placenta (Fig. 5) which occupies the entire surface of the gestational chamber with the exception of two poles. The structure of the placenta does not change in ultrasonographic appearance until the end of pregnancy. 4. Ultrasound aspects of embryo and fetus 4.1. Early pregnancy—days 14–30 [5] The embryo is first detected around day 14 of pregnancy as a thickening of the gestational chamber wall, but only on day 16 does it clearly protrude into the cavity (Fig. 4). On day 17 of pregnancy, the embryo appears separated from the wall and the following day it tends to take a characteristic C-form, with the buds of the head, trunk and thoracic limbs becoming visible (Figs. 6–8). Subsequently, the embryo moves toward the center of the gestational chamber (day 20) (Fig. 9), then on day 22 it is situated near the opposite wall. In this position, the development of the embryo continues and by day 26 it takes on its’ definitive shape.
Fig. 4. Day 16 of pregnancy: ultrasound section of the uterus. The developing placenta can be recognized as two hyperechoic lines separated by one hypoechoic line. The embryo (hyperechoic spot) protrudes into the cavity of the gestational chamber.
Fig. 6. Embryos on days 16–18 and 20 of pregnancy.
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Fig. 7. Day 17 of pregnancy: ultrasound section of the gestational chamber. The embryo (E) appears separated from the wall of the gestational chamber.
Fig. 9. Day 20 of pregnancy: ultrasound section of the gestational chamber. The embryo (E) is in the center.
4.2. Mid to late pregnancy—day 30 to term [5] Fetal development progresses rapidly and from day 30 the ultrasonographic visualization of different organs becomes possible (Figs. 10 and 11). 4.2.1. Development of internal organs [5] Between days 29 and 30 it is possible to identify the urinary bladder situated in the caudal abdomen near the umbilical cord and the fluid-filled stomach close to the liver (Figs. 10 and 12). From day 49, the stomach appears to move caudally in relation to the liver (Fig. 13). The kidneys are seen for the first time on day 39, but from day 50 it is possible to distinguish the renal
Fig. 8. Day 18 of pregnancy: ultrasound section of the gestational chamber. The embryo tends to take a characteristic C-form, buds of the head (H) and trunk and the buds of the thoracic limbs (L), yolk sac (Y) and allantois (Al).
Fig. 10. Day 30 of pregnancy: fetus fixed and sectioned longitudinally. Lg, lung; Lv, liver; S, stomach; K, kidney.
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Fig. 11. Embryos on days 20 and 22 of pregnancy and fetuses on days 25 and 30 of pregnancy.
Fig. 12. Day 30 of pregnancy: ultrasound longitudinal section of the fetus. The urinary bladder (U) and the stomach (S) appear as anechoic areas.
cortex from the medulla (Figs. 14 and 15). The small and large intestine is hardly visible until day 40 because of the large size of the liver that occupies almost the entire abdominal cavity. The contrast in echogenicity
Fig. 13. Day 50 of pregnancy: fetus fixed and sectioned longitudinally. Lg, lung; Lv, liver; S, stomach.
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Fig. 14. Days 40–50 of pregnancy: ultrasound transverse section of the trunk, kidneys (K) and intestine (I) of the fetus.
Fig. 15. Days 40–50 of pregnancy: ultrasound longitudinal section of the kidney (K) of the fetus.
Fig. 16. Days 40–50 of pregnancy: ultrasound transverse section of the fetus. The different echogenicity between the liver (Lv) and the lung (Lg).
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Fig. 17. Days 40–50 of pregnancy: ultrasound frontal section of the head of the fetus. The eyes (E) with the crystalline lens (Cl) and cerebral cranium (C) are evident.
Fig. 18. Days 40–50 of pregnancy: ultrasound longitudinal section of the fetus. The stomach (S), the liver (Lv), and the lung (Lg) with the large thoracic vessels (T.V.) are evident.
Fig. 19. (A) Sonogram of the external genitalia of a 40 day male fetus (sagittal section). Prepuce (short arrow) and scrotum (long arrow) are evident. (B) Sonogram of the external genitalia of a 41 day female fetus (arrow) (sagittal section). Gross lateral anatomical view of male (C) and female (D) external genitalia of 43 day fetuses.
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between the liver and the lungs during days 40–50 is shown in Fig. 16. Only after day 54 it is possible to appreciate stratification of the intestinal wall and the presence of meconium. The eyes are recognizable from approximately day 35, and within the rostral position of the eye, after day 50, the crystalline lens becomes apparent (Fig. 17). 4.2.2. Heart beat and fetal activity [5] Fetal heart activity can be detected ultrasonographically between days 16 and 17 and this can confirm fetal viability, but detection of the outline of the heart with its chambers is only feasible after day 50 when it is also possible to evaluate the major vessels (Fig. 18). The umbilical vessels are visible from day 42. Small body fetal movements are often observed from day 33 and they become more evident by day 37. These movements include flexion and extension of the limbs, feet, head and neck, but only from around day 50 is it possible to distinguish specific suckling movements of the mouth. All the skeletal structures can be identified from day 42 and acoustic shadowing becomes visible from day 50. 4.2.3. Gender identification [7] Fetal gender determination can be performed for the first time at days 38–43 of pregnancy (Fig. 19), but later it become more difficult to assess because the fetal tail becomes more adherent to the hind limbs and fetal fluid depth near the perineum decreases. 5. Ultrasound aspects of fetal membranes On day 10, the gestational chamber become visible [5] and is occupied exclusively by the yolk sac (Fig. 3), but after 1 week (approximately day 18) it is possible to distinguish the allantois as a small circular anechoic area (Fig. 8). The allantois increases in dimension, reaching the same volume as the yolk sac at approximately day 20 of pregnancy. At the same time it is possible to appreciate the amnion as a small anechoic area close to the yolk sac (Fig. 20). All the fetal membranes can be easily recognized after day 30 (Fig. 21) because further development results in changes in their size and shape such that they become much enlarged. The yolk sac reduces its volume after day 30 although the amnion remains evident in the space between head and limbs after day 45. The times during gestation at which some fetal and extrafetal structures can be imaged are listed in Tables 1 and 2.
Fig. 20. Day 20 of pregnancy: ultrasound section of the gestational chamber. The allantois (Al) and the yolk sac (Y) have about the same volume; the amnion (A) appears as a small anechoic area.
6. Correlation between age of conceptus and ultrasonographic measurements 6.1. First 30 days of gestation In cats, the positive correlation between anatomic and ultrasonographic measurements of the embryo/ fetus [6] confirms the accuracy of ultrasonography for determining fetal parameters. In that study [6], during the first 30 days of pregnancy a linear correlation was observed between certain ultrasonographic measure-
Fig. 21. Day 25 of pregnancy: ultrasound longitudinal section of the uterus. All the fetal membranes can be distinguished: yolk sac (Y), amnion (A) and allantois (Al).
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Table 1 Time of ultrasound appearance and subsequent development of some fetal and extrafetal structures during the first 30 days of pregnancy in cats
Gestational chamber Spherical shape Lemon shape Uterine wall Hypoechogenic endometrium (non-specific) Layers of the placenta Placenta zonata Position of the embryo Leaning on the wall of the gestational chamber Protruding into the gestational chamber Separated from the wall of the gestational chamber In the center of the gestational chamber Axis > the embryo//the axis of the horn Fetal teguments Yolk sac Allantois Volume of yolk sac = volume of allantois Amnion Volume of amnion = volume of yolk sac Tubular form of the yolk sac (longitudinal section) Embryo and fetus Heart beat C-form (head and trunk) Buds of the anterior limbs Definitive form Sagittal dorsal tube Anechogenic area at the level of the head Stomach (puntiform) Bladder (puntiform) Hyperechogenic lung vs. liver Umbilical cord Hyperechogenic skeleton (long bone anterior limbs and head) Fetal movements (laterality)
Table 2 Time of ultrasound appearance and subsequent development of some fetal and extrafetal structures during the first 30 days of pregnancy in cats
Days after mating
Days after mating
Mode
Range
Mode
Range
10 20
10–11 19–21
30 49 54
30–32 48–50 54–57
4
3–5
16 25
15–17 24–26
40 54
38–42 52–56
14
13–16
35 50
35–39 47–50
16 17
15–17 16–18
40 50
35–40 48–50
20 26
19–21 25–28
33 37 50
32–35 37–40 48–52
Kidneys Isoechogenic with the liver Cortex and medulla
39 50
38–41 48–50
Cardio-vascular apparatus Cardiac chambers Principal vessels
50 42
48–50 40–44
Diaphragm Footpads Choroid plexi
50 35 40
50–56 33–35 38–42
10 18 20 20 25 25
10–11 17–19 19–21 20–21 24–25 25–27
16–17 18 18 26 30 30
16–18 17–19 17–19 24–27 26–30 26–30
30 29–30 30 30 30
29–30 29–32 29–32 30–32 30–33
30
30–34
Stomach Dorsal to the liver Caudal to the liver Mucal folds Intestine Layered structure Eyes Eyes Crystalline lens Skeleton Vertebrae Ossification: long bone diaphysis appeared in the shadow cone Movements Dorso-ventral flexion Limbs, neck and head Hiccups, mouth opening and movements of the tongue
From Zambelli et al. [5].
From Zambelli et al. [5].
ments (length of the embryo/fetus, external and internal diameter of gestational sac) and the gestational age (Table 3). Furthermore, considering that the length of the embryo and the diameter of the gestational sac can be measured accurately only from day 17 and until day 30 of pregnancy, respectively, assessment of gestational age on the basis of one of three measurements is possible by using three line equations, where y = 2.0087x 31.43 (embryo/fetus length), y = 1.602x 12.13 (external
diameter of gestational sac) and y = 1.368x (internal diameter of gestational sac).
11.566
6.2. After 30 days of gestation Valuable information regarding fetal age may be also obtained during the second half of gestation. For example, after day 30 of pregnancy an exponential correlation between the abdominal, head and stomach diameters of the fetus and gestational age has been observed [7] (Table 4). As reported by Zambelli et al. [6], it is possible to predict gestational age using the following equation: T = long(y/a)/b, where y is the observed diameter and T is the gestational age. For the diameter of fetal abdomen, a = 0.405565 and b = 0.0372141; for the diameter of fetal skull, a = 0.483873
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Table 3 Ultrasonographic external and internal diameter of the gestational sacs and of the length of the conceptuses (mean S.E.M.) Number of days following mating
Ultrasonographic internal diameter of the gestational sac (mm)
Ultrasonographic external diameter of the gestational sac (mm)
Ultrasonographic length of the embryo/fetus (mm)
10 14 16 17 18 20 22 25 30
3.51 0.14 5.12 0.18 10.26 0.29 11.42 0.20 12.39 0.23 17.38 0.37 20.42 0.29 21.22 0.24 26.24 0.30
6.93 0.07 8.00 0.04 11.99 0.06 14.06 0.08 15.40 0.41 20.72 1.18 24.94 0.93 28.64 1.70 35.70 1.05
3.33 0.33 5.66 0.44 8.74 0.50 11.20 0.77 17.46 0.72 30.18 0.57
Redrawn from Zambelli et al. [6].
Table 4 Ultrasonographic abdominal, cranial and gastric diameters (cm) of feline fetuses during the second half of gestation (mean S.E.M.) Days after mating
Abdominal diameter (cm)
Biparietal diameter (cm)
Gastric diameter (cm)
30 35 45 50 60
1.32 0.014 1.57 0.017 1.84 0.038 2.81 0.040 3.83 0.016
1.12 0.018 1.35 0.010 1.53 0.013 1.93 0.027 2.60 0.020
0.36 0.010 0.47 0.013 0.62 0.008 0.85 0.008 1.18 0.016
Redrawn from Zambelli et al. [7].
and b = 0.02756; for the diameter of fetal stomach, a = 0.115113 and b = 0.0388901. 7. Discussion Ultrasonographic imaging of the reproductive tract during pregnancy offers useful information on the developmental state of the embryo and the fetus. It appears to be a more accurate method for pregnancy diagnosis than abdominal palpation or radiography, although it does not necessarily provide an accurate estimation of fetal number. To detect pregnancy, ultrasonographic examinations can be performed beginning at 10 days after mating. From day 30 it becomes possible to recognize different fetal organs and, thereafter, it might be possible to detect fetal malformations. The characteristic appearance of the placenta can be recognized on day 16 of pregnancy, but in contrast with humans, no studies have reported any modification in its echo-structure throughout the entire duration of pregnancy. Further studies are needed to evaluate the possibility of grading the placenta, as is done in humans [8]. The positive correlation found between several ultrasonographic measurements and gestational age may be used to monitor the normal development of
pregnancy and to gather information regarding fetal age. Even if the determination of fetal sex appears to be less important than in humans, this diagnosis could be useful for a complete evaluation of the fetus at days 38– 43 of pregnancy. In bitches, several studies have been carried out to evaluate fetal viability through the monitoring of fetal heart rate [9,10]. In queens, further study on fetal evaluation are needed, in fact, it might be important, for example, in determining if and when a Caesarean operation may be indicated. In the cat, further studies are needed to establish the positive use and applicability of the echo-Doppler technique for providing valuable information about fetal health and maturity of the placenta. Moreover, in humans and in other species [11,12], Doppler ultrasound is an important diagnostic tool for evaluating the fetal and maternal vessels and for establishing if there is a sufficient supply of oxygen and nutrients to fetuses. References [1] Denker HW, Eng LA, Mootz U, Hamner CE. Studies on the early development and implantation in the cat. 1. Cleavage and blastocyst formation. Anat Anz 1978;144:457–68. [2] Johnston SD, Root Kustritz MV, Olson PNS. Feline pregnancy. In: Canine and feline theriogenology. Philadelphia, PA: WB Saunders Company; 2001. p. 414–9.
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[3] Boyd JS. Radiographic identification of the various stages of pregnancy in the domestic cat. J Small Anim Pract 1971;12:501–6. [4] Davidson AP, Nyland TG, Tsutsui T. Pregnancy diagnosis with ultrasound in the domestic cat. Vet Radiol 1986;27:109–14. [5] Zambelli D, Caneppele B, Bassi S, Paladini C. Ultrasound aspect of fetal and extrafetal structures in pregnant cats. J Feline Med Surg 2002;4:95–106. [6] Zambelli D, Castagnetti C, Belluzzi S, Bassi S. Correlation between the age of the conceptus and various ultrasonographic measurements during the first 30 days of pregnancy in domestic cats (Felis catus). Theriogenology 2002;57:1981–7. [7] Zambelli D, Castagnetti C, Belluzzi S, Paladini C. Correlation between fetal age and ultrasonographic measurements during the second half of pregnancy in domestic cats (Felis catus). Theriogenology 2004;62:1430–7.
[8] Iaccarino M, Fortunato A, Iaccarino S. In: Ecografia, Ziviello M, Bazzocchi M, editors. Ostetricia: Guido Gnocchi Edizioni S.R.L. Napoli; 1994. p. 759–61 [chapter 22]. [9] Verstegen JP, Silva LDM, Onclin K, Donnay I. Echocardiographic study of heart rate in dog and cat foetuses in utero. J Reprod Fertil Suppl 1993;47:175–80. [10] Zone MA, Wanke MM. Diagnosis of canine fetal health by ultrasonography. J Reprod Fertil Suppl 2001;57: 215–9. [11] Nautrup CP. Doppler ultrasonography of canine maternal and fetal arteries during normal gestation. J Reprod Fertil 1998;112: 301–14. [12] Gu¨nzel-Apel AR, Ko¨ster K, Mo¨hrke C, Poulsen Nautrup C. The use of Doppler sonography for the canine genital tract. In: III Evssae European Congress; 2002.p. 72–3.
Ultrasonography for pregnancy diagnosis and evaluation in queens D. Zambelli *, F. Prati Veterinary Clinical Department, Obstetrical and Gynaecological Section, University of Bologna, Via Tolora di Sopra 50, 40064 Ozzano Emilia, Bologna, Italy
Abstract In the present paper, we describe the clinical utility of ultrasonography for diagnosing and evaluating pregnancy in domestic cats. Ultrasonography is a non-invasive technique that permits an accurate diagnosis of pregnancy and allows serial evaluation of the developing embryo/fetus and the extrafetal structures. The first ultrasonographic indication of pregnancy is a gestational chamber seen on day 10 after mating as a small circular anechoic structure. From day 30, it is possible to recognize different fetal organs, and between 38 and 43 days, the gender of the fetus can be determined. Measurements obtained during the second half of gestation can be used to determine fetal age and calculations can then be made that may more accurately predict the time of parturition. Further studies are needed in the queen to determine the applicability of the echo-Doppler technique used routinely in human obstetric medicine. This type of ultrasonography could potentially provide useful information about fetal health and the maturity of the placenta. # 2006 Elsevier Inc. All rights reserved. Keywords: Cat; Pregnancy; Ultrasound
1. Reproduction overview
2. Methods of pregnancy diagnosis
Female domestic cats are seasonally polyestrus and ovulation occurs between 24 and 48 h after coitus. Ova are fertilized in the oviduct and then pass into the uterine horns as morulae by days 5–6 postcoitus [1]. After implantation, which occurs 13–14 days after ovulation, the pregnancy continues to develop with relatively consistent chronological events (Figs. 1 and 2). The placenta is endotheliochorial in structure and zonary in shape. Parturition usually occurs between 63 and 67 days following conception [2].
Different methods may be used for pregnancy diagnosis of the queen, including abdominal palpation [2], radiography [3] and ultrasonography [4]. The laboratory tests commonly used for pregnancy assessment in other domestic animals are currently not applicable to the cat.
* Corresponding author. Tel.: +39 051 2097989; fax: +39 051 2097568. E-mail address: [email protected] (D. Zambelli). 0093-691X/$ – see front matter # 2006 Elsevier Inc. All rights reserved. doi:10.1016/j.theriogenology.2006.04.004
2.1. Palpation Careful palpation of the pregnant uterus through the abdominal wall is the most practical and rapid method of pregnancy diagnosis. It is most successfully performed within 21–25 days after mating when each fetal vesicle is approximately 2.5 cm in diameter. After day 35 of gestation, the uterine swellings become confluent and diagnosis becomes more difficult.
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Fig. 1. Schematic illustration of embryo formation and subsequent implantation (graphic by D. Zambelli).
2.2. Radiography A positive diagnosis of pregnancy can also be made with radiography. Fetal skeletal calcification becomes visible by radiography between 36 and 45 days after breeding [3] even though uterine embryonic swelling of 1.2–2.5 cm may be visualized as early as 17–21 days. 2.3. Ultrasonography Ultrasonography is a non-invasive and inexpensive technology. In the queen, pregnancy can be diagnosed by ultrasonography from 10 days after mating. In addition, fetal age can be assessed, fetal viability confirmed and, possibly, fetal abnormalities can be
determined. Generally, ultrasound units with 7.5– 10 MHz sector transducers can be used. 3. Ultrasound aspects of extrafetal structures 3.1. Uterus, gestational chamber and placenta [5] The earliest ultrasonographic indication of pregnancy in the queen may be the presence of an early (day 4) physiological uterine hyperplasia, although this appearance is common to both gravid and non-gravid queens in diestrus. The gestational chamber, which appears as a small circular anechoic structure normally visible on day 10 of pregnancy (Fig. 3), progressively increases in size from 6.9 mm on day 10 to about
Fig. 2. Longitudinal and transverse (E1–H1) section of gestational chamber. Development of fetal and extrafetal structures shown on days: (A) 10, (B) 14, (C) 16, (D) 17 and 18, (E) 20, (F) 22, (G) 25 and 26 and (H) 30 (graphic by D. Zambelli).
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Fig. 3. Day 10 of pregnancy: ultrasound longitudinal section of the uterus. A gestational chamber (C) can be seen.
35.7 mm on day 30. There is a consequent loss of the spherical shape of the gestational chamber as it undergoes slight elongation toward the classical ‘‘lemon’’ outline. On day 16 of pregnancy, the developing placenta can be recognized within the gestational chamber as two hyperechoic lines separated by a hypoechoic line (Fig. 4). This stratified appearance is maintained throughout pregnancy. From day 25 it is possible to
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Fig. 5. Day 25 of pregnancy: ultrasound longitudinal section of the uterus. Corion leave (Cl) in comparison with the placenta zonata (P) that appears hyperechoic at the level of its internal and external surfaces, while it is hypoechoic in the center.
distinguish the zonary nature of the placenta (Fig. 5) which occupies the entire surface of the gestational chamber with the exception of two poles. The structure of the placenta does not change in ultrasonographic appearance until the end of pregnancy. 4. Ultrasound aspects of embryo and fetus 4.1. Early pregnancy—days 14–30 [5] The embryo is first detected around day 14 of pregnancy as a thickening of the gestational chamber wall, but only on day 16 does it clearly protrude into the cavity (Fig. 4). On day 17 of pregnancy, the embryo appears separated from the wall and the following day it tends to take a characteristic C-form, with the buds of the head, trunk and thoracic limbs becoming visible (Figs. 6–8). Subsequently, the embryo moves toward the center of the gestational chamber (day 20) (Fig. 9), then on day 22 it is situated near the opposite wall. In this position, the development of the embryo continues and by day 26 it takes on its’ definitive shape.
Fig. 4. Day 16 of pregnancy: ultrasound section of the uterus. The developing placenta can be recognized as two hyperechoic lines separated by one hypoechoic line. The embryo (hyperechoic spot) protrudes into the cavity of the gestational chamber.
Fig. 6. Embryos on days 16–18 and 20 of pregnancy.
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Fig. 7. Day 17 of pregnancy: ultrasound section of the gestational chamber. The embryo (E) appears separated from the wall of the gestational chamber.
Fig. 9. Day 20 of pregnancy: ultrasound section of the gestational chamber. The embryo (E) is in the center.
4.2. Mid to late pregnancy—day 30 to term [5] Fetal development progresses rapidly and from day 30 the ultrasonographic visualization of different organs becomes possible (Figs. 10 and 11). 4.2.1. Development of internal organs [5] Between days 29 and 30 it is possible to identify the urinary bladder situated in the caudal abdomen near the umbilical cord and the fluid-filled stomach close to the liver (Figs. 10 and 12). From day 49, the stomach appears to move caudally in relation to the liver (Fig. 13). The kidneys are seen for the first time on day 39, but from day 50 it is possible to distinguish the renal
Fig. 8. Day 18 of pregnancy: ultrasound section of the gestational chamber. The embryo tends to take a characteristic C-form, buds of the head (H) and trunk and the buds of the thoracic limbs (L), yolk sac (Y) and allantois (Al).
Fig. 10. Day 30 of pregnancy: fetus fixed and sectioned longitudinally. Lg, lung; Lv, liver; S, stomach; K, kidney.
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Fig. 11. Embryos on days 20 and 22 of pregnancy and fetuses on days 25 and 30 of pregnancy.
Fig. 12. Day 30 of pregnancy: ultrasound longitudinal section of the fetus. The urinary bladder (U) and the stomach (S) appear as anechoic areas.
cortex from the medulla (Figs. 14 and 15). The small and large intestine is hardly visible until day 40 because of the large size of the liver that occupies almost the entire abdominal cavity. The contrast in echogenicity
Fig. 13. Day 50 of pregnancy: fetus fixed and sectioned longitudinally. Lg, lung; Lv, liver; S, stomach.
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Fig. 14. Days 40–50 of pregnancy: ultrasound transverse section of the trunk, kidneys (K) and intestine (I) of the fetus.
Fig. 15. Days 40–50 of pregnancy: ultrasound longitudinal section of the kidney (K) of the fetus.
Fig. 16. Days 40–50 of pregnancy: ultrasound transverse section of the fetus. The different echogenicity between the liver (Lv) and the lung (Lg).
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Fig. 17. Days 40–50 of pregnancy: ultrasound frontal section of the head of the fetus. The eyes (E) with the crystalline lens (Cl) and cerebral cranium (C) are evident.
Fig. 18. Days 40–50 of pregnancy: ultrasound longitudinal section of the fetus. The stomach (S), the liver (Lv), and the lung (Lg) with the large thoracic vessels (T.V.) are evident.
Fig. 19. (A) Sonogram of the external genitalia of a 40 day male fetus (sagittal section). Prepuce (short arrow) and scrotum (long arrow) are evident. (B) Sonogram of the external genitalia of a 41 day female fetus (arrow) (sagittal section). Gross lateral anatomical view of male (C) and female (D) external genitalia of 43 day fetuses.
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between the liver and the lungs during days 40–50 is shown in Fig. 16. Only after day 54 it is possible to appreciate stratification of the intestinal wall and the presence of meconium. The eyes are recognizable from approximately day 35, and within the rostral position of the eye, after day 50, the crystalline lens becomes apparent (Fig. 17). 4.2.2. Heart beat and fetal activity [5] Fetal heart activity can be detected ultrasonographically between days 16 and 17 and this can confirm fetal viability, but detection of the outline of the heart with its chambers is only feasible after day 50 when it is also possible to evaluate the major vessels (Fig. 18). The umbilical vessels are visible from day 42. Small body fetal movements are often observed from day 33 and they become more evident by day 37. These movements include flexion and extension of the limbs, feet, head and neck, but only from around day 50 is it possible to distinguish specific suckling movements of the mouth. All the skeletal structures can be identified from day 42 and acoustic shadowing becomes visible from day 50. 4.2.3. Gender identification [7] Fetal gender determination can be performed for the first time at days 38–43 of pregnancy (Fig. 19), but later it become more difficult to assess because the fetal tail becomes more adherent to the hind limbs and fetal fluid depth near the perineum decreases. 5. Ultrasound aspects of fetal membranes On day 10, the gestational chamber become visible [5] and is occupied exclusively by the yolk sac (Fig. 3), but after 1 week (approximately day 18) it is possible to distinguish the allantois as a small circular anechoic area (Fig. 8). The allantois increases in dimension, reaching the same volume as the yolk sac at approximately day 20 of pregnancy. At the same time it is possible to appreciate the amnion as a small anechoic area close to the yolk sac (Fig. 20). All the fetal membranes can be easily recognized after day 30 (Fig. 21) because further development results in changes in their size and shape such that they become much enlarged. The yolk sac reduces its volume after day 30 although the amnion remains evident in the space between head and limbs after day 45. The times during gestation at which some fetal and extrafetal structures can be imaged are listed in Tables 1 and 2.
Fig. 20. Day 20 of pregnancy: ultrasound section of the gestational chamber. The allantois (Al) and the yolk sac (Y) have about the same volume; the amnion (A) appears as a small anechoic area.
6. Correlation between age of conceptus and ultrasonographic measurements 6.1. First 30 days of gestation In cats, the positive correlation between anatomic and ultrasonographic measurements of the embryo/ fetus [6] confirms the accuracy of ultrasonography for determining fetal parameters. In that study [6], during the first 30 days of pregnancy a linear correlation was observed between certain ultrasonographic measure-
Fig. 21. Day 25 of pregnancy: ultrasound longitudinal section of the uterus. All the fetal membranes can be distinguished: yolk sac (Y), amnion (A) and allantois (Al).
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Table 1 Time of ultrasound appearance and subsequent development of some fetal and extrafetal structures during the first 30 days of pregnancy in cats
Gestational chamber Spherical shape Lemon shape Uterine wall Hypoechogenic endometrium (non-specific) Layers of the placenta Placenta zonata Position of the embryo Leaning on the wall of the gestational chamber Protruding into the gestational chamber Separated from the wall of the gestational chamber In the center of the gestational chamber Axis > the embryo//the axis of the horn Fetal teguments Yolk sac Allantois Volume of yolk sac = volume of allantois Amnion Volume of amnion = volume of yolk sac Tubular form of the yolk sac (longitudinal section) Embryo and fetus Heart beat C-form (head and trunk) Buds of the anterior limbs Definitive form Sagittal dorsal tube Anechogenic area at the level of the head Stomach (puntiform) Bladder (puntiform) Hyperechogenic lung vs. liver Umbilical cord Hyperechogenic skeleton (long bone anterior limbs and head) Fetal movements (laterality)
Table 2 Time of ultrasound appearance and subsequent development of some fetal and extrafetal structures during the first 30 days of pregnancy in cats
Days after mating
Days after mating
Mode
Range
Mode
Range
10 20
10–11 19–21
30 49 54
30–32 48–50 54–57
4
3–5
16 25
15–17 24–26
40 54
38–42 52–56
14
13–16
35 50
35–39 47–50
16 17
15–17 16–18
40 50
35–40 48–50
20 26
19–21 25–28
33 37 50
32–35 37–40 48–52
Kidneys Isoechogenic with the liver Cortex and medulla
39 50
38–41 48–50
Cardio-vascular apparatus Cardiac chambers Principal vessels
50 42
48–50 40–44
Diaphragm Footpads Choroid plexi
50 35 40
50–56 33–35 38–42
10 18 20 20 25 25
10–11 17–19 19–21 20–21 24–25 25–27
16–17 18 18 26 30 30
16–18 17–19 17–19 24–27 26–30 26–30
30 29–30 30 30 30
29–30 29–32 29–32 30–32 30–33
30
30–34
Stomach Dorsal to the liver Caudal to the liver Mucal folds Intestine Layered structure Eyes Eyes Crystalline lens Skeleton Vertebrae Ossification: long bone diaphysis appeared in the shadow cone Movements Dorso-ventral flexion Limbs, neck and head Hiccups, mouth opening and movements of the tongue
From Zambelli et al. [5].
From Zambelli et al. [5].
ments (length of the embryo/fetus, external and internal diameter of gestational sac) and the gestational age (Table 3). Furthermore, considering that the length of the embryo and the diameter of the gestational sac can be measured accurately only from day 17 and until day 30 of pregnancy, respectively, assessment of gestational age on the basis of one of three measurements is possible by using three line equations, where y = 2.0087x 31.43 (embryo/fetus length), y = 1.602x 12.13 (external
diameter of gestational sac) and y = 1.368x (internal diameter of gestational sac).
11.566
6.2. After 30 days of gestation Valuable information regarding fetal age may be also obtained during the second half of gestation. For example, after day 30 of pregnancy an exponential correlation between the abdominal, head and stomach diameters of the fetus and gestational age has been observed [7] (Table 4). As reported by Zambelli et al. [6], it is possible to predict gestational age using the following equation: T = long(y/a)/b, where y is the observed diameter and T is the gestational age. For the diameter of fetal abdomen, a = 0.405565 and b = 0.0372141; for the diameter of fetal skull, a = 0.483873
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Table 3 Ultrasonographic external and internal diameter of the gestational sacs and of the length of the conceptuses (mean S.E.M.) Number of days following mating
Ultrasonographic internal diameter of the gestational sac (mm)
Ultrasonographic external diameter of the gestational sac (mm)
Ultrasonographic length of the embryo/fetus (mm)
10 14 16 17 18 20 22 25 30
3.51 0.14 5.12 0.18 10.26 0.29 11.42 0.20 12.39 0.23 17.38 0.37 20.42 0.29 21.22 0.24 26.24 0.30
6.93 0.07 8.00 0.04 11.99 0.06 14.06 0.08 15.40 0.41 20.72 1.18 24.94 0.93 28.64 1.70 35.70 1.05
3.33 0.33 5.66 0.44 8.74 0.50 11.20 0.77 17.46 0.72 30.18 0.57
Redrawn from Zambelli et al. [6].
Table 4 Ultrasonographic abdominal, cranial and gastric diameters (cm) of feline fetuses during the second half of gestation (mean S.E.M.) Days after mating
Abdominal diameter (cm)
Biparietal diameter (cm)
Gastric diameter (cm)
30 35 45 50 60
1.32 0.014 1.57 0.017 1.84 0.038 2.81 0.040 3.83 0.016
1.12 0.018 1.35 0.010 1.53 0.013 1.93 0.027 2.60 0.020
0.36 0.010 0.47 0.013 0.62 0.008 0.85 0.008 1.18 0.016
Redrawn from Zambelli et al. [7].
and b = 0.02756; for the diameter of fetal stomach, a = 0.115113 and b = 0.0388901. 7. Discussion Ultrasonographic imaging of the reproductive tract during pregnancy offers useful information on the developmental state of the embryo and the fetus. It appears to be a more accurate method for pregnancy diagnosis than abdominal palpation or radiography, although it does not necessarily provide an accurate estimation of fetal number. To detect pregnancy, ultrasonographic examinations can be performed beginning at 10 days after mating. From day 30 it becomes possible to recognize different fetal organs and, thereafter, it might be possible to detect fetal malformations. The characteristic appearance of the placenta can be recognized on day 16 of pregnancy, but in contrast with humans, no studies have reported any modification in its echo-structure throughout the entire duration of pregnancy. Further studies are needed to evaluate the possibility of grading the placenta, as is done in humans [8]. The positive correlation found between several ultrasonographic measurements and gestational age may be used to monitor the normal development of
pregnancy and to gather information regarding fetal age. Even if the determination of fetal sex appears to be less important than in humans, this diagnosis could be useful for a complete evaluation of the fetus at days 38– 43 of pregnancy. In bitches, several studies have been carried out to evaluate fetal viability through the monitoring of fetal heart rate [9,10]. In queens, further study on fetal evaluation are needed, in fact, it might be important, for example, in determining if and when a Caesarean operation may be indicated. In the cat, further studies are needed to establish the positive use and applicability of the echo-Doppler technique for providing valuable information about fetal health and maturity of the placenta. Moreover, in humans and in other species [11,12], Doppler ultrasound is an important diagnostic tool for evaluating the fetal and maternal vessels and for establishing if there is a sufficient supply of oxygen and nutrients to fetuses. References [1] Denker HW, Eng LA, Mootz U, Hamner CE. Studies on the early development and implantation in the cat. 1. Cleavage and blastocyst formation. Anat Anz 1978;144:457–68. [2] Johnston SD, Root Kustritz MV, Olson PNS. Feline pregnancy. In: Canine and feline theriogenology. Philadelphia, PA: WB Saunders Company; 2001. p. 414–9.
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[3] Boyd JS. Radiographic identification of the various stages of pregnancy in the domestic cat. J Small Anim Pract 1971;12:501–6. [4] Davidson AP, Nyland TG, Tsutsui T. Pregnancy diagnosis with ultrasound in the domestic cat. Vet Radiol 1986;27:109–14. [5] Zambelli D, Caneppele B, Bassi S, Paladini C. Ultrasound aspect of fetal and extrafetal structures in pregnant cats. J Feline Med Surg 2002;4:95–106. [6] Zambelli D, Castagnetti C, Belluzzi S, Bassi S. Correlation between the age of the conceptus and various ultrasonographic measurements during the first 30 days of pregnancy in domestic cats (Felis catus). Theriogenology 2002;57:1981–7. [7] Zambelli D, Castagnetti C, Belluzzi S, Paladini C. Correlation between fetal age and ultrasonographic measurements during the second half of pregnancy in domestic cats (Felis catus). Theriogenology 2004;62:1430–7.
[8] Iaccarino M, Fortunato A, Iaccarino S. In: Ecografia, Ziviello M, Bazzocchi M, editors. Ostetricia: Guido Gnocchi Edizioni S.R.L. Napoli; 1994. p. 759–61 [chapter 22]. [9] Verstegen JP, Silva LDM, Onclin K, Donnay I. Echocardiographic study of heart rate in dog and cat foetuses in utero. J Reprod Fertil Suppl 1993;47:175–80. [10] Zone MA, Wanke MM. Diagnosis of canine fetal health by ultrasonography. J Reprod Fertil Suppl 2001;57: 215–9. [11] Nautrup CP. Doppler ultrasonography of canine maternal and fetal arteries during normal gestation. J Reprod Fertil 1998;112: 301–14. [12] Gu¨nzel-Apel AR, Ko¨ster K, Mo¨hrke C, Poulsen Nautrup C. The use of Doppler sonography for the canine genital tract. In: III Evssae European Congress; 2002.p. 72–3.