Suitability of antral follicle counts and computer-assisted analysis of ultrasonographic and magnetic resonance images for estimating follicular reserve in porcine,ovine and bovine ovaries ex situ

Abstract

This study was conducted to determine if correlations exist between the numbers of microscopic follicles comprising ovarian follicular reserve (OFR) and antral follicle counts (AFCs), and to assess the usefulness of computerized analyses of ovarian ultrasonograms and magnetic resonance (MR) images for estimating OFR in excised porcine, ovine and bovine ovaries. As a pre-requisite to these analyses, we characterized and compared ovarian cortical histomorhpology and follicle populations in the three species varying in prolificacy and overall reproductive longevity, and hence the total number of microscopic and antral follicles. Ultrasonographic and MR images were obtained at the scanner settings optimized to provide opposing contrasts between antral follicles and the ovarian stroma. Commercially available ImageProPlus® analytical software was used to calculate numerical pixel values (NPVs) and pixel heterogeneity (standard deviation of the pixel values) along the computer-generated lines (4–6) placed in the area corresponding to the ovarian cortex. The numbers of primordial (r = 0.38, P < 0.01) and intermediate follicles (r = 0.37, P < 0.01) were correlated with the numbers of antral follicles in bovine ovarian sections. The numbers of primordial (r = 0.28, P < 0.05), intermediate (r = 0.31, P < 0.01) and primary follicles (r = 0.27, P < 0.05) correlated directly with mean NPVs of the ultrasonographic ovarian images in cattle. There was a negative correlation between primary follicle numbers and NPVs of MR images (3D FAST-SPOILED GRADIENT ECHO) of the porcine ovarian cortex (r = −0.31, P < 0.05). To summarize, the numbers of primordial and intermediate follicles could only be estimated from AFCs in cows. Using ultrasound NPVs, the numbers of primordial, intermediate and primary follicles could be directly estimated in bovine ovaries and the quantitative image attributes of MR images were useful for quantifying porcine primary follicles. The bovine ovarian model is compatible with human situation and hence future studies should be undertaken to ascertain the usefulness of AFCs and ultrasonographic image analyses for estimating OFR in women.

Keywords

Ovarian follicle reserve ovarian histology ultrasonography magnetic resonance imaging digital image analysis

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References

Myers

Britt

Wreford

Ebling

Kerr

. Methods for quantifying follicular numbers within the mouse ovary. Reproduction 2004; 127: 569–80.

Kelsey

Anderson

Wright

Nelson

Wallace

WHB

. Data-driven assessment of the human ovarian reserve. Mol Hum Reprod 2011; 18: 79–87.

Wallace

WHB

Kelsey

. Human ovarian reserve from conception to menopause. PLoS ONE 2011; 5: e8772–e8772.

Chatterjee

Modi

Maitra

Kadam

Patel

Gokrall

Meherji

. Screening for FOXL2 gene mutations in women with premature ovarian failure: an Indian experience. Reprod Biomed Online 2007; 15: 554–60.

Lass

. Assessment of ovarian reserve: Is there still a role for ovarian biopsy in the light of new data? Hum Reprod 2004; 19: 467–9.

Lambalk

de Koning

Flett

Van Kasteren

Gosden

Homburg

. Assessment of ovarian reserve. Ovarian biopsy is not a valid method for the prediction of ovarian reserve. Hum Reprod 2004; 19: 1055–9.

Kwok

Johnson

. Ovarian biopsy has no role as a routine diagnostic test of ovarian reserve: a systematic review. Reprod Biomed Online 2012; 24: 492–4.

Jain

Soules

Collins

. Comparison of basal follicle stimulating hormone versus the clomiphene citrate challenge test for ovarian reserve screening. Fertil Steril 2004; 82: 180–5.

Jirge

. Ovarian reserve tests. J Hum Reprod Sci 2011; 4: 108–13.

10.

Kwee

Schats

McDonnell

Schoemaker

Lambalk

. The clomiphene citrate challenge test versus the exogenous follicle-stimulating hormone ovarian reserve test as a single test for identification of low responders and hyperresponders to in vitro fertilization. Fertil Steril 2006; 85: 1714–22.

11.

Ficicioglu

Kutlu

Baglam

Bakacak

. Early follicular antimullerian hormone as an indicator of ovarian reserve. Fertil Steril 2006; 85: 592–6.

12.

Carvalho BR, Sobrinho DBG, Vieira ADD, Resende MPS, Barbosa ACP, Silva AA, Nakagawa HM. Ovarian reserve assessment for infertility investigation. ISRN Obstet Gynecol, http://www.ncbi.nlm.nih.gov/pmc/articles/PMC3302183/ (Published online 26 January 2012). DOI: 10.5402/2012/576385.

13.

Waberski D, Kunz-Schmidt A, Borchard Neto G, Richter L, Weitze K. Real-time ultrasound diagnosis of ovulation and ovarian cysts in sows and its impact on artificial insemination efficiency. Proc Am Soc Anim Sci, www.asas.org/jas/symposia/proceedings/0944.pdf (1999) (accessed August 2014).

14.

Birtch

Baerwald

Olatunbosun

Pierson

. Ultrasound image attributes of human ovarian dominant follicles during natural and oral contraceptive cycles. Reprod Biol Endocrinol 2005; 3: 12–12.

15.

Ginther

Gastal

Bergfelt

Baerwald

Pierson

. Comparative study of the dynamics of follicular waves in mares and women. Biol Reprod 2004; 71: 1195–201.

16.

Sarty

Adams

Pierson

. Three-dimensional magnetic resonance imaging for the study of ovarian function in a bovine in vitro model. J Reprod Fertil 2000; 119: 69–75.

17.

Hilton

Sarty

Adams

Pierson

. Magnetic Resonance Image attributes of the ovarian follicle wall during development and regression. Biol Reprod 2001; 65: 1067–73.

18.

Ireland

Scheetz

Jimenez-Krassel

Themmen

Ward

Lonergan

Smith

Perez

Evans

Ireland

. Antral follicle count reliably predicts number of morphologically healthy oocytes and follicles in ovaries of young adult cattle. Biol Reprod 2008; 79: 1219–25.

19.

Adams

Pierson

. Bovine model for study of ovarian follicular dynamics in humans. Theriogenology 1995; 43: 113–20.

20.

Baerwald

Adams

Pierson

. A new model for ovarian follicular development during the human menstrual cycle. Fertil Steril 2003; 80: 116–22.

21.

Liu

Hart

Petrik

Nykamp

Bartlewski

. Relationships between ultrasonographic image attributes, histomorphology and proliferating cell nuclear antigen expression of bovine antral follicles and corpora lutea ex situ. Reprod Dom Anim 2008; 43: 27–34.

22.

Payan-Carreira

Pires

. Multioocyte follicles in domestic dogs: A survey of frequency of occurrence. Theriogenology 2008; 69: 977–82.

23.

Jaiswal

Singh

Adams

. Developmental pattern of small antral follicles in the bovine ovary. Biol Reprod 2004; 71: 1244–51.

24.

Mossa

Jimenez-Krassel

Folger

Ireland

JLH

Smith

Lonergan

Evans

ACO

Ireland

. Evidence that high variation in the antral follicle count during follicular waves is linked to alterations in ovarian androgen production in cattle. Reproduction 2010; 140: 713–20.

25.

Silva-Santos

Siloto

Santos

GMG

Morotti

Marcantonio

Seneda

. Comparison of antral and preantral ovarian follicle populations between Bos indicus and Bos indicus-taurus cows with high or low antral follicles counts. Reprod Dom Anim 2014; 49: 48–51.

26.

Kerong

Xuefeng

Liying

Dengke

Yunhai

Yonghui

Xuemei

Xiaoxiang

Changxin

Ning

. Advanced methods of isolation and identification of porcine primordial follicles. Anim Reprod Sci 2007; 101: 163–71.

27.

Muruvi

Picton

Rodway

Joyce

. In vitro growth of oocytes from primordial follicles isolated from frozen-thawed lamb ovaries. Theriogenology 2005; 64: 1357–70.

28.

Aerts

Bols

. Ovarian follicular dynamics: a review with emphasis on the bovine species. Part I: Folliculogenesis and pre-antral follicle development. Reprod Dom Anim 2010; 45: 171–9.

29.

Singh

Adams

Pierson

. Promise of new imaging technologies for assessing ovarian function. Anim Reprod Sci 2003; 78: 371–99.

30.

Pierson

. Three-dimensional ultrasonography. J Obstet Gynecol 2007; 29: 205–6.

31.

Pierson

Adams

. Computer-assisted image analysis, diagnostic ultrasonography and ovulation induction: Strange bedfellows. Theriogenology 1998; 43: 105–12.