REPBIO-93; No. of Pages 5 reproductive biology xxx (2013) xxx–xxx

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Technical Note

3D ultrasound imaging of the human corpus luteum§ Christoph Brezinka * Department of Gynecological Endocrinology and Reproductive Medicine, Medical University Innsbruck, Anichstreet 35, A-6020 Innsbruck, Austria

article info

abstract

Article history:

The aim of this article was to present the extent to which the state-of-the art ultrasono-

Received 3 May 2013

graphic imaging can be used to visualize the features of the human corpus luteum (CL). In

Accepted 12 November 2013

the late 1970s, the first ultrasonographic images of human CLs were published. The advent of transvaginal, high-resolution transducers has greatly improved the quality of imaging as did

Keywords:

the subsequent introduction of color Doppler and 3D ultrasonography. In the present

Ultrasound

technical note, the examples of the various technical and imaging modalities used to

Ultrasonography

examine the human CLs are shown. CL is a short-lived structure with a highly variable

Corpus luteum

morphological appearance and the 3D ultrasonographic technique is an ideal tool to perform

3D ultrasound

standardized measurements on the CL. The introduction of new imaging techniques in

Ovary

clinical reproductive medicine can only be successful if operators are properly trained.

Imaging

# 2013 Published by Elsevier Urban & Partner Sp. z o.o. on behalf of Society for Biology of

Fertility

Reproduction & the Institute of Animal Reproduction and Food Research of Polish Academy of Sciences in Olsztyn.

1.

Introduction

Ultrasonographic imaging using transvaginal probes plays a leading role in monitoring the patients undergoing ovarian stimulation in infertility therapies: most protocols demand an ultrasonographic assessment of the patient's ovaries and endometrium prior to the commencement of medication [1]. During the stimulated cycles, follicular and endometrial development are monitored at regular intervals and the optimal timing for human chorionic gonadotropin (hCG) administration, based largely on the assessment of follicular volume, is determined [2]. Similarly, the monitoring of

unstimulated cycles, either for intercourse timing, insemination or ‘‘natural’’ cycle IVF (IVF performed using mature oocytes retrieved from dominant follicles in a natural cycle) all rely heavily on transvaginal ultrasound [3,4]. While the developing pre-ovulatory follicles, either ‘‘natural’’ or ‘‘stimulated’’, are at the centre of clinical interest, the ultrasonographic morphology of the human corpus luteum has received comparatively less attention [5]. Knowledge of the morphology of the corpus luteum has, since Fraenkel's time, been obtained from surgical and autopsy specimens, and prior to the advent of ultrasound a coherent morphologic continuum was established [6]: in the hours following ovulation, serous exudate permeates the ovary and the wall

§ The material described in this article was presented as an invited lecture at Ludwig Fraenkel Symposium ‘‘Endocrine Control of Corpus Luteum Function’’ in Wroclaw, Poland (5–6 September, 2013). * Tel.: +43 0512 504 81052; fax: +43 0512 504 23277. E-mail addresses: [email protected], [email protected]. 1642-431X/$ – see front matter # 2013 Published by Elsevier Urban & Partner Sp. z o.o. on behalf of Society for Biology of Reproduction & the Institute of Animal Reproduction and Food Research of Polish Academy of Sciences in Olsztyn. http://dx.doi.org/10.1016/j.repbio.2013.11.002

Please cite this article in press as: Brezinka C. 3D ultrasound imaging of the human corpus luteum. Reprod Biol (2013), http://dx.doi.org/ 10.1016/j.repbio.2013.11.002

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Fig. 1 – Peripheral vascularization of the corpus luteum or a circular pattern called the ‘‘ring of fire’’ that can be demonstrated on the 3D color Doppler images.

of the former follicle shrinks, becoming thicker and more vascularized. The first ultrasonographic images of postovulatory ovaries were published in the late 1970s using a transabdominal approach [7]. With the advent of transvaginal

B-mode ultrasonographic, even before the introduction of color Doppler and 3D ultrasonographic techniques, the wide variability in the appearance of the corpus luteum was demonstrated, and novel sonoanatomical criteria for a CL

Fig. 2 – 3D image of the central fluid-filled structure of a corpus luteum using the Sono-AVCTM mode that automatically tracks and calculates the volume of the fluid-filled part. Please cite this article in press as: Brezinka C. 3D ultrasound imaging of the human corpus luteum. Reprod Biol (2013), http://dx.doi.org/ 10.1016/j.repbio.2013.11.002

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Fig. 3 – Corpus luteum in the TUITM mode giving successive tomography-like images of consecutive slices through the ovary.

Fig. 4 – The VocalTM analysis of a corpus luteum in situ. Through a succession of rotational steps, the corpus luteum is traced along the edge thus producing an image and determining the volume of the CL.

classification system, based on both thickness and echogenicity of the CL wall and the appearance of the central region, were proposed [8].

2. Human corpus luteum ultrasonographic morphology In the majority of cycles observed, the follicle that until ovulation had been a round, hypoechoic structure, fills with blood, which by clotting and subsequently liquefying gives a wide array of sonographic appearances. This type of morphology has been described as ‘‘central fluid-filled cavity’’ (CFFC), a term first used in ultrasonographic reports from domestic animals [9]. However, the content of the cavity is rarely homogenous on ultrasonographic images and blood clots can

Fig. 5 – Corpus luteum inside the ovary after manual tracing using the VOCALTM and the ‘‘magicut’’ techniques.

Please cite this article in press as: Brezinka C. 3D ultrasound imaging of the human corpus luteum. Reprod Biol (2013), http://dx.doi.org/ 10.1016/j.repbio.2013.11.002

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(1) Color Doppler ultrasound is an invaluable tool in detecting the corpus luteum by using its strong circular vascularization, the ‘‘ring of fire’’, as a marker (Fig. 1). (2) Sono-AVC, a technique now widely used for monitoring stimulated cycles, recognizes fluid-filled structures such as follicles, and automatically tracks them and calculates the volume of each structure (Fig. 2). (3) Tomographic ultrasonographic imaging (TUI) allows for visualization of parallel slices of an acquired volume. Using TUI, it is possible to assess the proportion of the volume occupied by the corpus luteum in a post-ovulatory ovary (Fig. 3). (4) VOCAL (virtual organ computer-aided analysis) enables the operator to further analyze the images acquired during the ultrasonographic examination off-line. A manual mode enables the operator to trace the contours of the corpus luteum through a succession of pre-defined rotational steps (Fig. 4). The images obtained can be further modified using techniques such as ‘‘magicut’’ (Fig. 5), ‘‘niche’’(Fig. 6a) or ‘‘wiremesh’’(Fig. 6b).

4.

Fig. 6 – (a) The corpus luteum ‘‘sliced open’’ using the NicheTM mode; (b) the corpus luteum from Figs. 4–6a visualized using the ‘‘wiremesh’’ mode.

have a jagged, bizarre appearance, resembling the solid components of a malignant tumor [10]. While in any other human tissue, the substantial rupture followed by localized haemorrhage and clotting is associated with the damage and loss of function of the tissue, this does not seem to affect the ability of the corpus luteum to produce progesterone. In a group of 50 women who underwent daily ultrasonographic examinations from day 12 after menses to encompass the next menses and two ovulations, the appearance of a corpus luteum after the disappearance of a dominant follicle was observed in all subjects [9]. These authors used computer-assisted image analysis based on mean numerical pixel values (NPVs) of the ultrasonographic images obtained with B-mode, thus avoiding counting ovarian stroma and the fluid filled areas inside towards the corpus luteum.

3.

Ultrasonographic imaging techniques

Recently, a number of new ultrasonographic imaging techniques have improved our ability to visualize the corpus luteum. Most of these are based on the development and application of 3D ultrasonographic imaging techniques.

Conclusions

In summary, new developments in ultrasonographic technology have provided the clinicians working in reproductive medicine with a vast number of imaging modalities, many of which, however, are rarely used in daily practice. Nevertheless, with increasing utilization of the technology by all manufacturers, improved training of operators and high patient demand for plausible imaging, the wealth of data generated by 3D ultrasonography and its different applications promises to improve our understanding of more than the corpus luteum function.

Conflict of interest None.

references

[1] Abloulghar MM. Ultrasound monitoring for ovulation induction: pitfalls and problems. In: Aboulghar M, Rizk B, editors. Ovarian stimulation. Cambridge: Cambridge, UP; 2011. p. 217–32 [chapter 20]. [2] Raine-Fenning N, Deb S, Jayaprakasan K, Clewes J, Hopkisson J, Campbell B. Timing of oocyte maturation and egg collection during controlled ovarian stimulation: a randomized controlled trial evaluating manual and automated measurements of follicle diameter. Fertility and Sterilty 2010;94:184–8. [3] Son WY, Chung JT, Herrero B, Dean N, Demirtas E, Holzer H, et al. Chian RC,Tan SL. Selection of the optimal day for oocyte retrieval based on the diameter of the dominant follicle in hCG-primed in vitro maturation cycles. Human Reproduction 2008;23:2680–5. [4] Gordon JD, Dimattina M, Reh A, Botes A, Celia G, Payson M. Utilization and success rates of unstimulated in vitro fertilization in the United States: an analysis of the Society

Please cite this article in press as: Brezinka C. 3D ultrasound imaging of the human corpus luteum. Reprod Biol (2013), http://dx.doi.org/ 10.1016/j.repbio.2013.11.002

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for Assisted Reproductive Technology database. Fertility and Sterilty 2013;100:392–5. [5] Backstrom T, Nakata M, Pierson RA. Ultrasonography of normal and aberrant luteogenesis. In: Jaffe R, Pierson RA, Abramowicz JS, editors. Imaging in infertility and reproductive endocrinology. Philadelphia: Lippincott; 1994. p. 143–54. [6] Clement PB. Anatomy and histology of the ovary. In: Kurman RJ, editor. Blaustein's pathology of the female genital tract. New York: Springer; 2002. p. 649–73. [7] Hackeloer BJ, Robinson HP. Ultrasound examination of the growing ovarian follicle and corpus luteum during the normal physiological menstrual cycle (in German). Geburtshilfe und Frauenheilkunde 1978;38:163–7.

[8] Nakata M, Selstam G, Olofsson J, Backstrom T. Investigation of the human corpus luteum by ultrasonography: a proposed scheme for clinical investigation. Ultrasound in Obstetrics and Gynecology 1992;2:190–6. [9] Baerwald AR, Adams GP, Pierson RA. Form and function of the corpus luteum during the human menstrual cycle. Ultrasound in Obstetrics and Gynecology 2005;25 :498–507. [10] Valentin L, Ameye L, Franchi D, Guerriero S, Jurkovic D, Savelli L, et al. Risk of malignancy in unilocular cysts: a study of 1148 adnexal masses classified as unilocular cysts at transvaginal ultrasound and review of the literature, Ultrasound in Obstetrics and. Gynecology 2013;41:80–9.

Please cite this article in press as: Brezinka C. 3D ultrasound imaging of the human corpus luteum. Reprod Biol (2013), http://dx.doi.org/ 10.1016/j.repbio.2013.11.002

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3D ultrasound imaging of the human corpus luteum.

The aim of this article was to present the extent to which the state-of-the art ultrasonographic imaging can be used to visualize the features of the ...
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