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Vertebrate reproductive science and technology
RESEARCH ARTICLE

Ultrasound biomicroscopy: a non-invasive approach for in vivo evaluation of oocytes and small antral follicles in mammals

L. F. M. Pfeifer A , G. P. Adams B D , R. A. Pierson C and J. Singh B
+ Author Affiliations
- Author Affiliations

A Brazilian Agricultural Research Corporation – Embrapa Rondônia, Route BR 364 – Km 5,5 – Zona Rural, PO Box 127 – Porto Velho – RO, 76815-800, Brazil.

B Veterinary Biomedical Sciences, University of Saskatchewan, 52 Campus Drive, Saskatoon, SK, S7N 5B4, Canada.

C Obstetrics, Gynecology and Reproductive Sciences, University of Saskatchewan, 103 Hospital Drive, Saskatoon, SK, S7N 0W8, Canada.

D Corresponding author. Email: gregg.adams@usask.ca

Reproduction, Fertility and Development 26(1) 48-54 https://doi.org/10.1071/RD13305
Published: 5 December 2013

Abstract

The use of ultrasonography has changed our understanding of the ovarian function in live animals. However, most of the studies that have used ultrasonography to image the ovary have provided data only of structures >1 mm in diameter. The recent availability of high-resolution ultrasound technology with high-frequency transducers (25–70 MHz), offers the potential to examine the developmental dynamics of small antral follicles and the cumulus–oocyte complex (COC) in vivo. In this review we provide data from a series of studies performed by Veterinary Biomedical Sciences Laboratory describing the advantages and disadvantages, as well as image characteristics, of ultrasound biomicroscopy (UBM) to study ovarian biology in mammals. Data and images of small ovarian structures in rabbits, cattle, mice and humans are shown. The UBM technique allowed visualisation of small antral follicles ranging in size from 300 to 700 μm in all species examined, as well as COC within follicles in rabbits, cattle and humans. Furthermore, UBM permitted clear distinction of the follicular wall from the surrounding ovarian stroma in cattle and humans. At present, the limited depth of penetration of UBM restricts the use of this technique to an experimental setting. In that regard, further studies using UBM will probably result in a greater understanding of the pattern and control of early antral folliculogenesis and oogenesis.

Additional keywords: folliculogenesis, images, ovary.


References

Adams, G. P., Jaiswal, R., Singh, J., and Malhi, P. (2008). Progress in understanding ovarian follicular dynamics in cattle. Theriogenology 69, 72–80.
Progress in understanding ovarian follicular dynamics in cattle.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXhsVSmu7nK&md5=e770b7553312bf08a9ff5e99081c0d1cCAS | 17980420PubMed |

Baerwald, A., Dauk, S., Kanthan, R., and Singh, J. (2009). Use of ultrasound biomicroscopy to image human ovaries in vitro. Ultrasound Obstet. Gynecol. 34, 201–207.
Use of ultrasound biomicroscopy to image human ovaries in vitro.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD1MrjsVajtA%3D%3D&md5=e8e4644ead10dfa3df14d1699c6e8637CAS | 19606428PubMed |

Baerwald, A. R., Adams, G. P., and Pierson, R. A. (2012). Antral ovarian folliculogenesis during the human menstrual cycle: a systematic review. Hum. Reprod. Update 18, 73–91.
Antral ovarian folliculogenesis during the human menstrual cycle: a systematic review.Crossref | GoogleScholarGoogle Scholar | 22068695PubMed |

Birtch, R. L., Baerwald, A. R., Olatunbosun, O. A., and Pierson, R. A. (2005). Ultrasound image attributes of human ovarian dominant follicles during natural and oral contraceptive cycles. Reprod. Biol. Endocrinol. 3, 12.
Ultrasound image attributes of human ovarian dominant follicles during natural and oral contraceptive cycles.Crossref | GoogleScholarGoogle Scholar | 15829004PubMed |

Braw-Tal, R., and Yossefi, S. (1997). Studies in vivo and in vitro on the initiation of follicle growth in the bovine ovary. J. Reprod. Fertil. 109, 165–171.
Studies in vivo and in vitro on the initiation of follicle growth in the bovine ovary.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2sXhs1Gls7w%3D&md5=b55890ed5478c73348a2ddd0fe3ed7e8CAS | 9068428PubMed |

Cervantes, M. P., Singh, J., Palomino, J. M., and Adams, G. P. (2013). Surgical translocation and ultrasound bio-microscopy of the ovaries in rabbits. Anim. Reprod. Sci. 138, 133–141.
Surgical translocation and ultrasound bio-microscopy of the ovaries in rabbits.Crossref | GoogleScholarGoogle Scholar |

Czarnota, G. J., Kolios, M. C., Vaziri, H., Benchimol, S., Ottensmeyer, F. P., Sherar, M. D., and Hunt, J. W. (1997). Ultrasonic biomicroscopy of viable, dead and apoptotic cells. Ultrasound Med. Biol. 23, 961–965.
Ultrasonic biomicroscopy of viable, dead and apoptotic cells.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaK2svks1CisA%3D%3D&md5=4a3c08d31e64fa4251b216b5165709ebCAS | 9301000PubMed |

Fair, T. (2003). Follicular oocyte growth and acquisition of developmental competence. Anim. Reprod. Sci. 78, 203–216.
Follicular oocyte growth and acquisition of developmental competence.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXksF2gtrw%3D&md5=8220acec5279e61f2fc031c38d1697e5CAS | 12818645PubMed |

Fortune, J. E. (2003). The early stages of follicular development: activation of primordial follicles and growth of preantral follicles. Anim. Reprod. Sci. 78, 135–163.
The early stages of follicular development: activation of primordial follicles and growth of preantral follicles.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXksF2gsbc%3D&md5=9c3b8629cf54554acacadb669d75c714CAS | 12818642PubMed |

Foster, F. S., Pavlin, C. J., Harasiewicz, K. A., Christopher, D. A., and Turnbull, D. H. (2000). Advances in ultrasound biomicroscopy. Ultrasound Med. Biol. 26, 1–27.
Advances in ultrasound biomicroscopy.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD3c7ltVCqtA%3D%3D&md5=29adc108a0f145117d20211c2eebdcb3CAS | 10687788PubMed |

Ginther, O. J., Kastelic, J. P., and Knopf, L. (1989). Composition and characteristics of follicular waves during the bovine estrous cycle. Anim. Reprod. Sci. 20, 187–200.
Composition and characteristics of follicular waves during the bovine estrous cycle.Crossref | GoogleScholarGoogle Scholar |

Hirshfield, A. N. (1991). Development of follicles in the mammalian ovary. Int. Rev. Cytol. 124, 43–101.
Development of follicles in the mammalian ovary.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK3MXlsFSmsr4%3D&md5=25d277870b934f41a1ffecb9f2a8d95dCAS | 2001918PubMed |

Jaiswal, R. S., Singh, J., and Adams, G. P. (2004). Developmental pattern of small antral follicles in the bovine ovary. Biol. Reprod. 71, 1244–1251.
Developmental pattern of small antral follicles in the bovine ovary.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXnvVGqtb4%3D&md5=dfb2b01f74f557781b94cfba3f5770f8CAS | 15189825PubMed |

Jaiswal, R. S., Singh, J., and Adams, G. P. (2009). High-resolution ultrasound biomicroscopy for monitoring ovarian structures in mice. Reprod. Biol. Endocrinol. 7, 69.
High-resolution ultrasound biomicroscopy for monitoring ovarian structures in mice.Crossref | GoogleScholarGoogle Scholar | 19580664PubMed |

Mircea, C. N., Lujan, M. E., Jaiswal, R. S., Singh, J., Adams, G. P., and Pierson, R. A. (2009). Ovarian imaging in the mouse using ultrasound biomicroscopy (UBM): a validation study. Reprod. Fertil. Dev. 21, 579–586.
Ovarian imaging in the mouse using ultrasound biomicroscopy (UBM): a validation study.Crossref | GoogleScholarGoogle Scholar | 19383264PubMed |

Pallares, P., and Gonzalez-Bulnes, A. (2008). The feasibility of ultrasound biomicroscopy for non-invasive and sequential assessment of ovarian features in rodents. Reprod. Biol. 8, 279–284.
The feasibility of ultrasound biomicroscopy for non-invasive and sequential assessment of ovarian features in rodents.Crossref | GoogleScholarGoogle Scholar | 19092988PubMed |

Pallares, P., Letelier, C., and Gonzalez-Bulnes, A. (2009). Progress toward ‘in vivo virtual histology’ of ovarian follicles and corpora lutea by ultrasound biomicroscopy. Fertil. Steril. 91, 624–626.
Progress toward ‘in vivo virtual histology’ of ovarian follicles and corpora lutea by ultrasound biomicroscopy.Crossref | GoogleScholarGoogle Scholar | 18692818PubMed |

Pfeifer, L. F., Siqueira, L. G., Adams, G. P., Pierson, R. A., and Singh, J. (2012). In vivo imaging of cumulus–oocyte-complexes and small ovarian follicles in cattle using ultrasonic biomicroscopy. Anim. Reprod. Sci. 131, 88–94.
In vivo imaging of cumulus–oocyte-complexes and small ovarian follicles in cattle using ultrasonic biomicroscopy.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BC38rhtFemsg%3D%3D&md5=9a34ac0f2e235bc65ce66ea0ded47de0CAS | 22464335PubMed |

Pierson, R., and Adams, G. P. (1995). Computer-assisted image analysis, diagnostic ultrasonography and ovulation induction: strange bedfellows Theriogenology 43, 105–112.
Computer-assisted image analysis, diagnostic ultrasonography and ovulation induction: strange bedfellowsCrossref | GoogleScholarGoogle Scholar |

Salamone, D. F., Adams, G. P., and Mapletoft, R. J. (1999). Changes in the cumulus–oocyte complex of subordinate follicles relative to follicular wave status in cattle. Theriogenology 52, 549–561.
Changes in the cumulus–oocyte complex of subordinate follicles relative to follicular wave status in cattle.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD3c7pvVGgsg%3D%3D&md5=d30ffc28d9e39ed8ae3ef2dd741cd012CAS | 10734355PubMed |

Singh, J., Pierson, R. A., and Adams, G. P. (1998). Ultrasound image attributes of bovine ovarian follicles and endocrine and functional correlates. J. Reprod. Fertil. 112, 19–29.
Ultrasound image attributes of bovine ovarian follicles and endocrine and functional correlates.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1cXitVKqsbY%3D&md5=6949c11efc609f56f4edd725b74ab4e8CAS | 9538326PubMed |

Singh, J., Adams, G. P., and Pierson, R. A. (2003). Promise of new imaging technologies for assessing ovarian function. Anim. Reprod. Sci. 78, 371–399.
Promise of new imaging technologies for assessing ovarian function.Crossref | GoogleScholarGoogle Scholar | 12818654PubMed |

Singh, J., Dominguez, M., Jaiswal, R., and Adams, G. P. (2004). A simple ultrasound test to predict the superstimulatory response in cattle. Theriogenology 62, 227–243.
A simple ultrasound test to predict the superstimulatory response in cattle.Crossref | GoogleScholarGoogle Scholar | 15159116PubMed |

Tom, J. W., Pierson, R. A., and Adams, G. P. (1998). Quantitative echotexture analysis of bovine ovarian follicles. Theriogenology 50, 339–346.
Quantitative echotexture analysis of bovine ovarian follicles.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD3c7ps1Kkug%3D%3D&md5=50e77901624b1e1712f3721de4ef8de7CAS | 10732129PubMed |

Vassena, R., Mapletoft, R. J., Allodi, S., Singh, J., and Adams, G. P. (2003). Morphology and developmental competence of bovine oocytes relative to follicular status. Theriogenology 60, 923–932.
Morphology and developmental competence of bovine oocytes relative to follicular status.Crossref | GoogleScholarGoogle Scholar | 12935869PubMed |