Reproductive Ultrasound of the Bitch and Queen

Reproductive Ultrasound of the Bitch and Queen

TOPICAL REVIEW Reproductive Ultrasound of the Bitch and Queen Autumn P. Davidson, DVM, MS, Dipl ACVIM,a and Tomas W. Baker, MSb Ultrasonographic eval...

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TOPICAL REVIEW

Reproductive Ultrasound of the Bitch and Queen Autumn P. Davidson, DVM, MS, Dipl ACVIM,a and Tomas W. Baker, MSb Ultrasonographic evaluation of the reproductive tract is an important component in the evaluation of the bitch and queen. Information is obtained concerning normal events involving the reproductive system (eg, ovulation, pregnancy) as well as pathologic conditions (eg, ovarian cysts, metritis). The appearance of the female reproductive tract normally changes with phases of the cycle; these changes need to be interpreted with knowledge of the ovarian cycle. Serial ultrasonographic evaluation of the diseased reproductive tract can be very helpful in evaluating response to therapy. © 2009 Elsevier Inc. All rights reserved. Keywords: ultrasound, female reproduction, pregnancy, uterus, ovary

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iagnostic ultrasound has become an important component of small animal theriogenology since its introduction to practice in 1978. The use of ultrasound as a tool in canine and feline reproduction has expanded from its initial role in safe and early pregnancy diagnosis to its current use in the approach to clinical reproduction (obstetrics, infertility, urogenital disorders, and pediatrics).1 The availability of ultrasonography in veterinary practice increased as reasonably priced, better-quality diagnostic ultrasound equipment became commercially available to veterinarians. Ultrasonography has become a standard of practice in many communities, with diagnostic ultrasound available at primary private practices, via readily accessible referral centers or from mobile specialty practices. Veterinary school curricula and continuing education courses now commonly include ultrasonography, providing students and graduates with the training to perform and interpret diagnostic ultrasound. Recent developments in scanhead technology have allowed improved visualization of reproductive anatomy. Before performing the specific evaluation of the female reproductive tract, the abdomen should be evaluated methodically with the animal in dorsal recumbency. The discovery of abnormalities in other systems can be relevant to reproductive disorders.2

aSchool

of Veterinary Medicine, Department of Medicine and Epidemiology, University of California, Davis, Davis, CA, USA. bSchool of Veterinary Medicine, Department of Radiology and Surgical Sciences, University of California, Davis, Davis, CA, USA. Address reprint requests to: Autumn P. Davidson, DVM, MS, Dipl ACVIM, (Internal Medicine) Clinical Professor, School of Veterinary Medicine, Department of Medicine and Epidemiology, VMTH/SAC, University of California, Davis, 1 Shields Ave, Davis, CA 95616. E-mail: [email protected] © 2009 Elsevier Inc. All rights reserved. 1527-3369/06/0604-0171\.00/0 doi:10.1053/j.tcam.2008.11.002

Normal Female Reproductive Tract: The Bitch and Queen A full urinary bladder acts as an acoustic window to improve imaging the uterus; clients should be reminded not to let their pets urinate just before the examination. The normal uterus is best located by scanning transversely between the urinary bladder and the colon. The cervix and uterine body are seen in transverse as a continuous hypoechoic oval structure dorsal to the anechoic urinary bladder and ventral to the hyperechoic, crescent-shaped colon. Thinking of the urinary bladder as a clock face, the uterine body will be located at 5 o’clock or 7 o’clock, on one side or the other of the colon (Fig 1). With the scanhead in transverse, begin in the mid abdomen and slide caudally until the transverse image of the urinary bladder appears. Try to position the gas-filled colon exactly underneath the bladder at the 6 o’clock position. Now visualize the uterus as an ovoid structure positioned between the urinary bladder and colon. Continue to travel caudally until the image of the uterus is blocked by the artifactual shadow produced by the pubis, confirming it is the body of the uterus, rather than a horn.3 Measurements (height, width, wall thickness) of the uterine body in the transverse image should be taken. The body should then be evaluated in the sagittal view. It will be positioned longitudinally between the dorsal urinary bladder wall and the gas-filled colon. Continue to travel caudally, visualizing the uterus dorsal to the trigonal area of the urinary bladder and dorsal to the urethra. Evaluate the uterine body for the presence or lack of fluid within the lumen and the character of the endometrial wall, which is normally smooth and uniform. Sagittal measurements of the longitudinal uterine body and endometrial wall (full thickness, wall thickness) should be taken (Fig 2). The normal image will change depending on the period of the estrous cycle, ie, the anestrous uterus differs from the diestrual uterus (see description that follows). The cervix is located slightly cranial to the bladder trigone and is best seen when under hormonal (estrogen or

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Figure 1. Transverse image of the uterine body (UT) seen positioned between the urinary bladder (UB) and colon. progesterone) influence rather than during anestrus. The cervix is an oblique, hyperechoic, linear structure in the sagittal view (Fig 3). The uterine body is smaller in diameter than the cervix and usually extends to the cranial one third of the bladder. The bifurcation of the uterus into the uterine horns can sometimes be imaged; the horns are typically difficult to image unless enlarged because of hormonal influence during the estrous cycle, pregnancy, or from pathology. The uterus is composed of 3 layers: the mucosa, the muscularis, and the serosa. The endometrium and myometrium cannot usually be differentiated in the normal state. The uterine lumen is generally not seen, although it may be visible as a bright echogenic central area, representing a small amount of intraluminal mucus, or as a hypoechoic to anechoic region if fluid is present. During anestrus, the uterine body is flat, with no fluid in the lumen and no changes in the endometrium (Fig 4). During proestrus and estrus, the uterus is thicker from estrogen influence, with scant fluid present in the lumen (Fig 5). In diestrus, the uterus is thickest, with glandular endometrial development from progesterone influence (Fig 6).

Figure 2. Sagittal image of the uterine body (cursors).

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Figure 3. Sagittal image of the cervix, delineated by a hyperechoic line (cursors). The uterine body is seen extending cranially. The normal ovaries are located caudal and slightly lateral to the caudal poles of the ipsilateral kidneys. Their location can be facilitated by the appearance of the artifactual edge artifact dorsal to each ovary (Fig 7).3 The appearance of the ovaries also varies with stages of the estrous cycle. Normal ovarian dimensions have been established for average-sized dogs.1 During anestrus, the ovaries appear as small oval- to bean-shaped structures with a homogenous echogenicity similar to the renal cortex (Fig 7). The cortex and medulla are not usually differentiated in the bitch and queen. Multiple anechoic or hypoechoic cyst-like structures can be visualized in the ovarian parenchyma during folliculogenesis; thickerwalled cystic structures are present during the luteal phase (Figs 8 and 9).

Ovulation Timing Serial evaluation of the ovaries (3 times daily) can be used to detect changes suggesting ovulation has just occurred. During proestrus, multiple anechoic follicular cystic structures can be identified, enlarging with time (up to ⬎ 1 cm in diam-

Figure 4. Sagittal image of the uterine body in anestrus (cursors). The uterus is homogenous without fluid in the lumen.

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Figure 5. Sagittal image of the uterine body in proestrus/ estrus. Under estrogen influence, scant fluid is seen in the uterine lumen, and the uterus is mildly increased in size.

eter). These structures ultimately have distinct walls and anechoic fluid centers with distal enhancement. The surface of the ovary may become irregular or lumpy. The anechoic fluid-filled follicles acutely become isoechoic to hyperechoic corpora hemorrhagica at the time of ovulation (Fig 10), progressing over several days to hypoechoic corpora lutea (Fig 11). The ovarian follicles do not collapse in the bitch and queen. During diestrus, the ovaries may be lobular, and the corpora lutea are obvious hypoechoic structures of variable size. Precise ovulation timing is best accomplished with a combination of techniques: vaginal cytology, serum progesterone levels, luteinizing hormone (LH) assays, and vaginoscopy, with ultrasound providing confirmatory information.4

Figure 6. Sagittal image of the uterine body in diestrus (cursors). Under progesterone influence, the endometrium is thickened, reflecting glandular development. Scant fluid can be present in the lumen. The uterus will be thickest during diestrus.

Figure 7. Sagittal image of the right ovary; edge artifact facilitates identification.

Pregnancy Diagnosis Pregnancy detection by abdominal palpation (at approximately 30 gestational days) or radiography (43-46⫹ days post LH peak, the later the better) can confirm the presence of fetuses at these points in time. Before fetal skeletal mineralization, other causes for uterine enlargement cannot be ruled out radiographically. Radiography cannot be used to assess fetal viability in a timely fashion. Once profound postmortem changes have occurred, radiography can detect intrafetal gas accumulation or abnormal skeletal arrangement suggesting fetal death. Early fetal resorption cannot be detected radiographically. Definite ultrasonographic diagnosis of pregnancy in the queen based on the appearance of a “fetal pole” can be made at 15 to 17 days postcoitus, although gravid uterine enlargement (4-14 days) and the presence of a gestational sac (11-14

Figure 8. Follicular phase of the ovarian cycle. Multiple thinwalled hypoechoic follicles are noted (arrow).

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Figure 9. Luteal phase of the ovarian cycle, left ovary. Corpora lutea, when mature, have thicker walls and maintain hypoechoic fluid within.

Figure 10. Sagittal image of an ovary (cursors) having recently undergone ovulation. The corpora hemorrhagica are isoechoic to the ovarian parenchyma as compared with the previous follicles.

Figure 12. (A) Early pregnancy (20 days). The fetal pole is evident dorsally within the gestational sac (cursors). (B) Early pregnancy (28 days). The fetus has recognizable morphology within the gestational sac (cursors). Fetal membranes are evident. (C) Sagittal image of feline pregnancy, 35 days.

Figure 11. Postovulatory left ovary, corpora lutea (CL) are present for 45 to 60 days. CLs tend to have thicker walls (cursors) than follicles.

days) can be detected even earlier. Ultrasonographic detection of the canine blastocyst (a 2- to 3-mm spherical hypoechoic structure surrounded by a hyperechoic rim within the uterus) occurs at 19 to 20 days post LH peak (Fig 12, A). Ultrasonography permits evaluation of early fetal cardiac motion (21-22 days post LH peak), fetal movement (31-32 days post LH peak), and the fetal heart rate, enabling assess-

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Figure 13. Late-gestation fetus. Cursors indicate proper positioning for measurement of the biparietal diameter. Ossification is evident. ment of viability. By 30 days’ gestation (30 days after the LH surge), pregnancy diagnosis with ultrasonography is straightforward (Fig 12, B). Fetal age determination by ultrasonography is accomplished in 2 ways: 1. The first appearance of visible structures and 2. The measurement of certain parameters. Predicting fetal age by noting the first appearance of visible structures corresponding to gestational length is often more accurate than measurements, but is technically more difficult. Measurements such as the gestational sac diameter, fetal occipitosacral (crown-rump) length and fetal skull (biparietal)

Table 1. Formulas to Predict Gestational Age and Days Before Parturition in the Dog and Cat

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Figure 14. Sagittal image of the right uterine horn. The endometrium is markedly cystic.

diameter can be obtained ultrasonographically, relate closely to fetal age, and permit estimation of gestational length and parturition dates, especially useful if ovulation timing was not performed (Figs 12, B and C, and 13; Table 1) Variation in breed size (especially in the dog) and individual variation in measuring technique are sources of inaccuracy in predicting fetal age with ultrasound.1,2 Ultrasonography is less accurate than radiography in estimating litter size, particularly later in gestation, because of its dynamic nature. Keep in mind that fetal resorption or abortion can alter litter size after early ultrasound estimates are made. The best time to evaluate litter size with ultrasound is at ⬃30 days of gestation, when minimal overlapping of fetuses is present.2 Beginning at the uterine bifurcation, evaluate one horn and then the other in transverse, scanning from caudal to cranial. This helps prevent counting individual fetuses more than once.

Gestational age in the dog (⫾ 3 days) Less than 40 days GA ⫽ (6 ⫻ GSD) ⫹ 20 GA ⫽ (3 ⫻ CRL) ⫹ 27 Greater than 40 days GA ⫽ (15 ⫻ HD) ⫹ 20 GA ⫽ (7 ⫻ BD) ⫹ 29 GA ⫽ (6 ⫻ HD) ⫹ (3 ⫻ BD) ⫹ 30 Days before parturition in the dog DBP ⫽ 65–GA Gestational age in the cat (⫾ 2 days) Greater than 40 days GA ⫽ 25 ⫻ HD ⫹ 3 GA ⫽ 11 ⫻ BD ⫹ 21 Days before parturition in the cat DBP ⫽ 61–GA Gestational age (GA) is based on days post-luteinizing hormone (LH) surge in the dog and days postbreeding in the cat. Gestational sac diameter (GSD), crown-rump length (CRL), head diameter (HD), and body diameter (BD) measurements are in centimeters. Days before parturition (DBP) are based on 65 ⴞ 1 day post-LH surge in the dog and 61 days postbreeding in the cat. Data modified from Nyland et al.

Figure 15. Cystic endometrial hyperplasia. Fluid is present in the left uterine horn lumen; anechoic cysts (cursor) are present in the endometrium.

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Figure 16. Abnormal fluid accumulation within the uterine horn (cursors). The fluid is anechoic, suggesting, but not diagnostic for, hydrometra or mucometra.

Disorders of the Reproductive Tract

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Figure 18. Open pyometra. Abnormal fluid accumulation within the uterine lumen (cursors). The endometrium is convoluted and jagged. Echogenic uterine walls suggest chronicity.

Ultrasonographic evaluation of the uterus provides important information concerning uterine wall thickness and composition (presence of cystic structures), lumen size and content, and overall organ symmetry and position. Cystic endometrial hyperplasia is characterized by endometrial thickening with focal anechoic structures noted in the uterine wall representing dilated cystic glands and tortu-

ous glandular ducts (Figs 14 and 15). With advanced disease, these changes do not disappear ultrasonographically during anestrus. Fluid accumulation in the uterine lumen may represent hydrometra, mucometra, or developing pyometra, and can be very difficult to differentiate (echogenicity may suggest cellularity) (Fig 16). Because of the potential for peritonitis, centesis is not generally advocated.1 Cytology (⫹/⫺ culture) of vaginal secretions is preferred. Because pyometra is associated with diestrus, measurement of a serum progesterone level can support the diagnosis and help differentiate it from hydrometra and mucometra, both of which can proceed to pyometra. Additional hematologic and biochemical abnormalities associated with pyometra (leukocytosis, azotemia, polydipsia/ polyuria) should be sought. Uterine enlargement with pyometra is variable and usually dependent on the patency of the cervix (Fig 17). Evaluation of the uterine lumen postpartum for retained placentae, mummified fetuses, or masses is best accomplished

Figure 17. Closed pyometra. Marked dilation of multiple uterine horn segments (arrow) is present.

Figure 19. Postpartum uterine horn (cursors) showing a former site of placental attachment. There is minimal fluid in the lumen.

In the bitch and queen, documented abnormalities of the estrous cycle call for ultrasonographic evaluation of the uterus and ovaries. Serial examinations may be necessary during various parts of the estrous cycle to evaluate differences in ovarian and uterine appearance with normal hormonal fluctuations (ie, ovarian “cyst” vs normal corpora lutea) and after parturition (ie, postpartum metritis vs subinvolution).

Cystic Endometrial Hyperplasia/Pyometra, Postpartum Metritis

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Volume 24, Number 2, May 2009 with ultrasound. Postpartum metritis is best differentiated from the normal postpartum uterine enlargement by a failure of normal progressive decrease in uterine lumen contents and horn width (Figs 18 and 19). The bitch involutes and repairs for 16 weeks, making the normal postpartum uterus prominent. Subinvolution of placental sites (causing prolonged vaginal bleeding postpartum secondary to failure of the trophoblast to regress) is differentiated from postpartum metritis clinically, because the ultrasonographic appearances can be similar (increased fluid in the uterine horn lumen, prominent placental attachment sites). The diagnosis and medical management of the cystic endometrial hyperplasia/pyometra complex or postpartum metritis (usually with prostaglandins, progesterone inhibitors, and antiprolactins) are best monitored by serial evaluations of uterine luminal contents and horn width with ultrasound along with hematology, biochemistry, and clinical parameters (appetite, fever, vaginal discharge) (Fig 20, A and B). The therapeutic use of prostaglandins should always be preceded

Figure 21. Doppler evaluation of a fetus. Minimal morphologic changes occur with early fetal demise, making detection of a lack of cardiac motion important.

by an ultrasound evaluation for pregnancy because of their action as effective abortifacients.

Pregnancy Termination and Intrauterine Fetal Death Purposeful induction of abortion with drugs (prostaglandins, dexamethasone, antiprogestins) also requires serial ultrasonographic evaluations to determine the endpoint of therapy because most protocols will result in delivery of viable neonates if terminated prematurely. Early fetal death is characterized by the preservation of fetal anatomy but lack of a heartbeat. Over time, fetal demise results in loss of recognizable fetal anatomy and loss of normal vesicle fluid content

Figure 20. (A) Transverse image of the bifurcation of the uterine body into horns (cursors). The endometrium is thickened, and excess fluid is present within the lumen of the horns. (B) Transverse image of the bifurcation of the uterine body into horns, postprostaglandin therapy. The right uterine horn (R) is reduced in size, with less fluid in the lumen and more normal endometrial wall layering. The left remains fluid filled and abnormally enlarged.

Figure 22. Fetal death. There is a loss of recognizable fetal anatomy and reduction in the amount of fluid within the vesicle. Note the adjacent fluid-filled uterine horn, ventral and cranial to the left kidney.

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Figure 23. Ovarian follicular cysts.

and shape (Figs 21 and 22). Loss of fetal viability usually precedes expulsion of fetuses by 12 to 48 hours.2

Infertility Differentiation of infertility due to a failure to conceive versus resorption or abortion can only be accomplished with serial ultrasonographic examinations of the uterus after breeding. Early resorption of fetuses can be documented by serial ultrasound evaluations of the gravid uterus. The ovaries can be imaged to evaluate their presence, size, and echogenicity. Fluid-filled, pathologic follicular, luteal, or nonfunctional cysts within ovaries can be readily imaged and persist over time, supporting the diagnosis of cystic ovarian disorders causing abnormalities in the estrous cycle (prolonged estrus, prolonged interestrus intervals). Cystic ovarian disease is characterized by persistent cystic structures in the ovarian parenchyma with clinical correlation (abnormal estrogen or progesterone effect).

Figure 24. Ovarian luteal cysts. Differentiation of follicular from luteal cysts requires clinical evaluation (vaginal cytologies, serum progesterone levels).

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Figure 25. Hematoma, uterine stump (cursors). Multiple anechoic structures of variable size are present at sites of hemorrhage resulting from loose ligatures. Follicular (estrogen-producing) cysts tend to be large and thin walled, with hypoechoic contents. Ovarian luteal cysts (producing progesterone) can have thicker walls; the contents remain hypoechoic (Figs 23 and 24). Pathologic ovarian cysts can be unilateral or bilateral, single or multiple, but must be differentiated clinically from normal cystic structures during appropriate parts of the estrous cycle (follicles, corpora lutea). Follicles would not be expected to persist for more than 21 to 30 days, corpora lutea for no more than 45 to 60 days.

Post-ovariohysterectomy Disorders/Abnormal Vaginal Discharge Ultrasound permits evaluation of the cervix, complementing vaginoscopic evaluations in which the caudal os can be the only part visualized. Uterine stump pyometra (if functional ovarian tissue is present), stump granuloma (secondary to local disease), or hematoma (coagulopathy or surgical error) can be visualized

Figure 26. Uterine stump granuloma. Hyperechoic slashes can represent a foreign body (grass awn, reactive suture material).

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Figure 27. Complex soft tissue mass within the uterine lumen. Leiomyoma, leiomyosarcoma, and adenoma or adenocarcinoma are the most common uterine neoplasias.

just cranial to the pubis, between the bladder and colon as a complex mass lesion (Fig 25). Vaginal foreign bodies (grass awns) can sometimes be imaged ultrasonographically in the cranial vagina and cervical area. The affected stump is characterized by echogenic material (Fig 26).5,6

Neoplasia Finally, uterine neoplasia is typically of altered echogenicity to the surrounding uterine tissue, having complex internal architecture, and may project into the uterine lumen (Fig 27). Alterations in ovarian dimensions or echogenicity can occur with neoplastic disorders, necessitating laparotomy,

Figure 29. Acute septic mastitis. Cursors indicate a hypoechoic fluid accumulation suggesting abscessation. ovariectomy, and biopsy (Fig 28). Tumors of the ovaries can also be unilateral or bilateral and can be functional, causing estrous cycle abnormalities. Histopathology is usually required to differentiate pathologic ovarian cysts from neoplasia; both can occur simultaneously.

The Mammary Gland Breast ultrasonography is commonly used in human medicine to further evaluate subtle changes noted with mammography. Ultrasound of the canine and feline mammary gland can be useful in identifying and characterizing mass lesions too small for detection by palpation, and to evaluate for associated lymphadenomegaly. Ultrasound of a mastitic mammary gland can be helpful in identifying fluid pocket development (abscessation) that warrants surgical intervention, as well as monitoring response to therapy (Fig 29).

References

Figure 28. Ovarian luteoma. The diagnosis of ovarian neoplasia depends on histopathologic evaluation of ovarian tissue. Bitches or queens ovariohysterectomized due to abnormal estrous cycles should always have pathology performed on the ovaries.

1. Nyland TG, Mattoon JS, Herrgesell EJ, et al: Physical principles, instrumentation, and safety of diagnostic ultrasound, in Nyland TG, Mattoon JS (eds): Small Animal Diagnostic Ultrasound, ed 2. Philadelphia, WB Saunders, 2002, pp 1-18 2. Baker TW: Performing the complete abdominal ultrasound evaluation, in Proceedings of the Swedish Annual Course in Small Animal Reproduction, Uppsala, Sweden, 2004 3. Penninck DG: Artifacts, in Nyland TG, Mattoon JS (eds): Small Animal Diagnostic Ultrasound, ed 2. Philadelphia, WB Saunders, 2002, pp. 19-29 4. Goodman M: Ovulation timing; concepts and controversies. Vet Clin North Am Small Anim Pract 31(2):219-235, 2001 5. Nyland TG, Mattoon JS, Herrgesell EJ, et al: Urinary tract, in Nyland TG, Mattoon JS (eds): Small Animal Diagnostic Ultrasound, ed 2. Philadelphia, WB Saunders, 2002, pp 158-195 6. Baker TW: Diagnostic imaging of the reproductive tract and adnexa in cats and dogs, in Proceedings of the Norwegian Annual Congress in Small Animal Reproduction, 2007