Unpredicted ovulations and conceptions during early pregnancy: an explanatory mechanism of human superfetation
Juan J. Tarín A E , Miguel A. García-Pérez B , Carlos Hermenegildo C and Antonio Cano DA Department of Functional Biology and Physical Anthropology, Faculty of Biological Sciences, University of Valencia, Burjassot, Valencia 46100, Spain.
B Research Unit-INCLIVA, Hospital Clínico de Valencia and Department of Genetics, Faculty of Biological Sciences, University of Valencia, Burjassot, Valencia 46100, Spain.
C Research Unit-INCLIVA, Hospital Clínico de Valencia and Department of Physiology, Faculty of Medicine, University of Valencia, Valencia 46010, Spain.
D Department of Pediatrics, Obstetrics and Gynecology, Faculty of Medicine, University of Valencia, Valencia 46010, Spain.
E Corresponding author. Email: tarinjj@uv.es
Reproduction, Fertility and Development 25(7) 1012-1019 https://doi.org/10.1071/RD12238
Submitted: 19 July 2012 Accepted: 11 September 2012 Published: 9 October 2012
Abstract
In this bioessay, a literature review on human superfetation was performed in order to find epidemiological variables associated with this phenomenon. Thereafter, an explanatory mechanism of superfetation compatible with the endocrinological, histological and physiological changes undergone by women during early pregnancy is proposed. Superfetation can be defined as the ovulation, fertilisation and implantation of a second or additional embryo(s) during pregnancy. The literature review evidences a small discordance in gestational age between dizygotic twins in humans (range: 2–4 weeks; mean ± s.e.m.: 3.3 ± 0.3 weeks). This difference is compatible with a luteal out-of-phase (LOOP; i.e. atypical increase in E2 levels in the mid-luteal phase)-like event occurring between 1 and 3 weeks after the ovulation that allowed the first pregnancy to take place. The LOOP-like event may allow passive sperm transport from the vaginal fornix to the Fallopian tube ipsilateral to the ovulatory ovary and trigger a LH peak and ovulation. Furthermore, during very early pregnancy, the decidual reaction is not yet completed and at least one proximal Fallopian ostium may be opened, allowing the passage of the spermatozoa ascending to the fertilisation site and the extra embryo(s) descending to the implantation site(s).
Additional keywords: decidual reaction, luteal out-of-phase event, peristaltic uterine contractions, very early pregnancy.
References
Adams, G. P. (1999). Comparative patterns of follicle development and selection in ruminants. J. Reprod. Fertil. Suppl. 54, 17–32.| 1:STN:280:DC%2BD3c7lslagsw%3D%3D&md5=91a15913e382f676f1d3447ce1440e32CAS | 10692842PubMed |
Al-Azemi, M., Ledger, W. L., Diejomaoh, M., Mousa, M., Makhseed, M., and Omu, A. (2003). Measurement of inhibin A and inhibin pro-alphaC in early human pregnancy and their role in the prediction of pregnancy outcome in patients with recurrent pregnancy loss. Fertil. Steril. 80, 1473–1479.
| Measurement of inhibin A and inhibin pro-alphaC in early human pregnancy and their role in the prediction of pregnancy outcome in patients with recurrent pregnancy loss.Crossref | GoogleScholarGoogle Scholar | 14667886PubMed |
Asch, R. H., Kotoulas, I. B., Smith, G., Eddy, C. A., and Balmaceda, J. P. (1984). Pituitary responsiveness to LH-RH during gestation and puerperium in the rhesus monkey. Acta Eur. Fertil. 15, 15–23.
| 1:CAS:528:DyaL2cXks1Kgtr4%3D&md5=c6f1057607b4cec3e8fbdfab9ea9131bCAS | 6428125PubMed |
Baerwald, A. R., Adams, G. P., and Pierson, R. A. (2012). Ovarian antral folliculogenesis during the human menstrual cycle: a review. Hum. Reprod. Update 18, 73–91.
| Ovarian antral folliculogenesis during the human menstrual cycle: a review.Crossref | GoogleScholarGoogle Scholar | 22068695PubMed |
Baijal, N., Sahni, M., Verma, N., Kumar, A., Parkhe, N., and Puliyel, J. M. (2007). Discordant twins with the smaller baby appropriate for gestational age – unusual manifestation of superfoetation: a case report. BMC Pediatr. 7, 2.
| Discordant twins with the smaller baby appropriate for gestational age – unusual manifestation of superfoetation: a case report.Crossref | GoogleScholarGoogle Scholar | 17239246PubMed |
Baird, D. D., Weinberg, C. R., McConnaughey, D. R., and Wilcox, A. J. (2003). Rescue of the corpus luteum in human pregnancy. Biol. Reprod. 68, 448–456.
| Rescue of the corpus luteum in human pregnancy.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXntVCjtQ%3D%3D&md5=c4a4af073c495bdebb525016479b07d5CAS | 12533407PubMed |
Becher, N., Waldorf, K. A., Hein, M., and Uldbjerg, N. (2009). The cervical mucus plug: structured review of the literature. Acta Obstet. Gynecol. Scand. 88, 502–513.
| The cervical mucus plug: structured review of the literature.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXhtVSntbvO&md5=ed91e01c0bc79ed5588d72b107282c60CAS | 19330570PubMed |
Bergfelt, D. R., Kastelic, J. P., and Ginther, O. J. (1991). Continued periodic emergence of follicular waves in nonbred progesterone-treated heifers. Anim. Reprod. Sci. 24, 193–204.
| Continued periodic emergence of follicular waves in nonbred progesterone-treated heifers.Crossref | GoogleScholarGoogle Scholar |
Bianchi, P. H., Serafini, P., da Rocha, A., Hassun, P. A., da Motta, E., Baruselli, P., and Baracat, E. (2010). Follicular waves in the human ovary: a new physiological paradigm for novel ovarian stimulation protocols. Reprod. Sci. 17, 1067–1076.
| Follicular waves in the human ovary: a new physiological paradigm for novel ovarian stimulation protocols.Crossref | GoogleScholarGoogle Scholar |
Bonnar, G. L. (1865). A critical inquiry regarding superfetation, with cases. Edinburgh Med. J. 10, 582–598.
Bourgoin, P., Marc, J., Merger, C., and Delatte, J. N. (1995). A case of a dizygotic twin pregnancy where superfetation seems indisputable. J. Gynecol. Obstet. Biol. Reprod. (Paris) 24, 440–443.
| 1:STN:280:DyaK2MznvVGqug%3D%3D&md5=615991caa7bbe16388f641c4fc34fcc1CAS |
Broekmans, F. J., Soules, M. R., and Fauser, B. C. (2009). Ovarian aging: mechanisms and clinical consequences. Endocr. Rev. 30, 465–493.
| Ovarian aging: mechanisms and clinical consequences.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXhtFaisbnP&md5=456058ed1e88007c14fa4f0bf4a6b07fCAS | 19589949PubMed |
Brook, J. D., Gosden, R. G., and Chandley, A. C. (1984). Maternal ageing and aneuploid embryos – evidence from the mouse that biological and not chronological age is the important influence. Hum. Genet. 66, 41–45.
| Maternal ageing and aneuploid embryos – evidence from the mouse that biological and not chronological age is the important influence.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaL2c7jsVSitw%3D%3D&md5=8c6d34b8a685ba434bc29b37a4530265CAS | 6538182PubMed |
Bsat, F. A., and Seoud, M. A. (1987). Superfetation secondary to ovulation induction with clomiphene citrate: a case report. Fertil. Steril. 47, 516–518.
| 1:STN:280:DyaL2s7mt1GrtQ%3D%3D&md5=09bb916da86763422625ec7a434dd158CAS | 3556628PubMed |
Ceric, F., Silva, D., and Vigil, P. (2005). Ultrastructure of the human periovulatory cervical mucus. J. Electron Microsc. (Tokyo) 54, 479–484.
| Ultrastructure of the human periovulatory cervical mucus.Crossref | GoogleScholarGoogle Scholar |
de Vries, K., Lyons, E. A., Ballard, G., Levi, C. S., and Lindsay, D. J. (1990). Contractions of the inner third of the myometrium. Am. J. Obstet. Gynecol. 162, 679–682.
| 1:STN:280:DyaK3c7ps1Srug%3D%3D&md5=aa918383d1c504790c3ee9f25e3801a6CAS | 2180303PubMed |
DiZerega, G., and Hodgen, G. D. (1979). Pregnancy-associated ovarian refractoriness to gonadotrophin: a myth. Am. J. Obstet. Gynecol. 134, 819–822.
| 1:STN:280:DyaE1M3ivFWrsQ%3D%3D&md5=3377c2602e1f7bbfed00d7c50976d594CAS | 111553PubMed |
DiZerega, G. S., Williams, R. F., Morin, M. L., and Hodgen, G. D. (1979). Anovulation after pregnancy termination: ovarian versus hypothalamic–pituitary factors. J. Clin. Endocrinol. Metab. 49, 594–599.
| Anovulation after pregnancy termination: ovarian versus hypothalamic–pituitary factors.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaL3c%2Fgs12gtw%3D%3D&md5=066e63b86a5e511effeabec9d5a7b2c1CAS | 113424PubMed |
Dmowski, W. P., DeOrio, L., and Rana, N. (1997). Embryo implantation during menstruation in the absence of adequate oestradiol and progesterone support, with subsequent normal response to ovulation induction and superfetation. Fertil. Steril. 68, 538–541.
| Embryo implantation during menstruation in the absence of adequate oestradiol and progesterone support, with subsequent normal response to ovulation induction and superfetation.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaK2svmtVGnug%3D%3D&md5=d7060eeb8015985f8965875ef23cfc2fCAS | 9314930PubMed |
Ecochard, R., and Gougeon, A. (2000). Side of ovulation and cycle characteristics in normally fertile women. Hum. Reprod. 15, 752–755.
| Side of ovulation and cycle characteristics in normally fertile women.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3cXivF2lsbc%3D&md5=3bcdc3ca54d8f519b3529b706b340df9CAS | 10739814PubMed |
Evans, A. C. (2003). Characteristics of ovarian follicle development in domestic animals. Reprod. Domest. Anim. 38, 240–246.
| Characteristics of ovarian follicle development in domestic animals.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD3svis1Srsg%3D%3D&md5=3d08c13efc85dcd737ea997b039fd35fCAS | 12887563PubMed |
Fontana, J., and Monif, G. R. G. (1979). Superfetation. Obstet. Gynecol. 35, 585–588.
Ginther, O. J., and Bergfelt, D. R. (1992). Associations between FSH concentrations and major and minor follicular waves in pregnant mares. Theriogenology 38, 807–821.
| Associations between FSH concentrations and major and minor follicular waves in pregnant mares.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD283pvF2nsQ%3D%3D&md5=c033eda5697853f453e488bc0f2e4c0dCAS | 16727181PubMed |
Ginther, O. J., Kot, K., Kulick, L. J., Martin, S., and Wiltbank, M. C. (1996). Relationships between FSH and ovarian follicular waves during the last six months of pregnancy in cattle. J. Reprod. Fertil. 108, 271–279.
| Relationships between FSH and ovarian follicular waves during the last six months of pregnancy in cattle.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2sXntFSqtQ%3D%3D&md5=da14ee25889593b19e785659a34dedbdCAS | 9038786PubMed |
Govan, A. D. (1968). The human ovary in early pregnancy. J. Endocrinol. 40, 421–428.
| The human ovary in early pregnancy.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaF1c7ptFWhsg%3D%3D&md5=25c15c80b0dcea48e917511ac473878dCAS | 5643418PubMed |
Govan, A. D. (1970). Ovarian follicular activity in late pregnancy. J. Endocrinol. 48, 235–241.
| Ovarian follicular activity in late pregnancy.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaE3cXltFyitLc%3D&md5=97d65e3504d6d19f96a7f0ccf37ae4b9CAS | 5471864PubMed |
Hale, G. E., and Burger, H. G. (2009). Hormonal changes and biomarkers in late reproductive age, menopausal transition and menopause. Best Pract. Res. Clin. Obstet. Gynaecol. 23, 7–23.
| Hormonal changes and biomarkers in late reproductive age, menopausal transition and menopause.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD1M%2FnvVKqtQ%3D%3D&md5=79e025a53c235e953a9b2bbef4eee9c5CAS | 19046657PubMed |
Hale, G. E., Zhao, X., Hughes, C. L., Burger, H. G., Robertson, D. M., and Fraser, I. S. (2007). Endocrine features of menstrual cycles in middle and late reproductive age and the menopausal transition classified according to the Staging of Reproductive Aging Workshop (STRAW) staging system. J. Clin. Endocrinol. Metab. 92, 3060–3067.
| Endocrine features of menstrual cycles in middle and late reproductive age and the menopausal transition classified according to the Staging of Reproductive Aging Workshop (STRAW) staging system.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXptl2hsb8%3D&md5=dfeadd77dbe56415eeab0ca6a51a9360CAS | 17550960PubMed |
Hale, G. E., Hughes, C. L., Burger, H. G., Robertson, D. M., and Fraser, I. S. (2009). Atypical oestradiol secretion and ovulation patterns caused by luteal out-of-phase (LOOP) events underlying irregular ovulatory menstrual cycles in the menopausal transition. Menopause 16, 50–59.
| Atypical oestradiol secretion and ovulation patterns caused by luteal out-of-phase (LOOP) events underlying irregular ovulatory menstrual cycles in the menopausal transition.Crossref | GoogleScholarGoogle Scholar | 18978637PubMed |
Harrison, A., Valenzuela, A., Gardiner, J., Sargent, M., and Chessex, P. (2005). Superfetation as a cause of growth discordance in a multiple pregnancy. J. Pediatr. 147, 254–255.
| Superfetation as a cause of growth discordance in a multiple pregnancy.Crossref | GoogleScholarGoogle Scholar | 16126061PubMed |
Honoré, L. H., and Nickerson, K. G. (1977). Combined intrauterine and tubal ectopic pregnancy: a possible case of superfetation. Am. J. Obstet. Gynecol. 127, 885–887.
| 851148PubMed |
Hwang, J. L., Lin, Y. H., and Tsai, Y. L. (1997). Pregnancy after immature oocyte donation and intracytoplasmic sperm injection. Fertil. Steril. 68, 1139–1140.
| Pregnancy after immature oocyte donation and intracytoplasmic sperm injection.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaK1c%2FnvF2gtA%3D%3D&md5=361b5ce864b1239a3bcb603e86b13cd9CAS | 9418713PubMed |
Illingworth, P. J., Groome, N. P., Duncan, W. C., Grant, V., Tovanabutra, S., Baird, D. T., and McNeilly, A. S. (1996). Measurement of circulating inhibin forms during the establishment of pregnancy. J. Clin. Endocrinol. Metab. 81, 1471–1475.
| Measurement of circulating inhibin forms during the establishment of pregnancy.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK28Xit1OnsLk%3D&md5=acb29e8666bfb141779817687f78bfe0CAS | 8636353PubMed |
Irwin, J. C., and Giudice, L. C. (1999). Decidua. In ‘Encyclopedia of Reproduction. Vol 1’. (Eds E. Knobil and J. D. Neill.) pp. 823–835. (Academic Press: San Diego, USA.)
Jeppsson, S., Rannevik, G., and Thorell, J. I. (1977). Pituitary gonadotrophin secretion during the first weeks of pregnancy. Acta Endocrinol. (Copenh.) 85, 177–188.
| 1:CAS:528:DyaE2sXktF2ks7w%3D&md5=5175452aeb1700e7a2f3bdd6a452ef24CAS |
Krenn, V., Marx, A., Wiedemann, R., Müller-Hermelink, H. K., and Kranzfelder, D. (1995). Superfetation occurring in connection with gamete intrafallopian transfer: a case report. Virchows Arch. 426, 647–649.
| Superfetation occurring in connection with gamete intrafallopian transfer: a case report.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaK2MzosVCrtw%3D%3D&md5=1158d2f60d5f690f819d1986fb1a0f4bCAS | 7655748PubMed |
Kunz, G., Beil, D., Huppert, P., and Leyendecker, G. (2006). Control and function of uterine peristalsis during the human luteal phase. Reprod. Biomed. Online 13, 528–540.
| Control and function of uterine peristalsis during the human luteal phase.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD28rnvFWrug%3D%3D&md5=73aae42f2113eec2fa347ceda1b1dccfCAS | 17007674PubMed |
La Marca, A., Giulini, S., Orvieto, R., De Leo, V., and Volpe, A. (2005). Anti-Müllerian hormone concentrations in maternal serum during pregnancy. Hum. Reprod. 20, 1569–1572.
| Anti-Müllerian hormone concentrations in maternal serum during pregnancy.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXksVSjsL0%3D&md5=6a70de543b636a55784095cc36854ca7CAS | 15734752PubMed |
Lantieri, T., Revelli, A., Gaglioti, P., Menato, G., Gennarelli, G., Delle Piane, L., and Massobrio, M. (2010). Superfetation after ovulation induction and intrauterine insemination performed during an unknown ectopic pregnancy. Reprod. Biomed. Online 20, 664–666.
| Superfetation after ovulation induction and intrauterine insemination performed during an unknown ectopic pregnancy.Crossref | GoogleScholarGoogle Scholar | 20211584PubMed |
Lefebvre, G., Vauthier, D., Gonzales, J., and Lesourd, S. (1990). Assisted reproductive technology and superfetation: a case report. Fertil. Steril. 53, 1100–1101.
| 1:STN:280:DyaK3c3ns1KksA%3D%3D&md5=94bff34960dbc29ca436fc82f9e5b6e4CAS | 2112495PubMed |
Lenton, E. A., and Woodward, A. J. (1988). The endocrinology of conception cycles and implantation in women. J. Reprod. Fertil. Suppl. 36, 1–15.
| 1:CAS:528:DyaL1cXmtVGjtrY%3D&md5=434e011c4e18fd06de3e47e9c8f52348CAS | 3057192PubMed |
Lenton, E. A., de Kretser, D. M., Woodward, A. J., and Robertson, D. M. (1991). Inhibin concentrations throughout the menstrual cycles of normal, infertile and older women compared with those during spontaneous conception cycles. J. Clin. Endocrinol. Metab. 73, 1180–1190.
| Inhibin concentrations throughout the menstrual cycles of normal, infertile and older women compared with those during spontaneous conception cycles.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK38Xht1WisLs%3D&md5=417657270167816b5e30eab01656c627CAS | 1955499PubMed |
Maqueo, M., and Goldzieher, J. W. (1966). Hormone-induced alterations of ovarian morphology. Fertil. Steril. 17, 676–683.
| 1:STN:280:DyaF2s%2Fhs1ehsg%3D%3D&md5=25dbc370d4012a20acc8758e0282d13bCAS | 4162082PubMed |
Mendizábal, A. F., Quiroga, S., Farinati, Z., Lahoz, M., and Nagle, C. (1984). Hormonal monitoring of early pregnancy by a direct radioimmunoassay of steroid glucuronides in first morning urine. Fertil. Steril. 42, 737–740.
| 6489546PubMed |
Messinis, I. E. (2006). Ovarian feedback, mechanism of action and possible clinical implications. Hum. Reprod. Update 12, 557–571.
| Ovarian feedback, mechanism of action and possible clinical implications.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28Xotl2lsrk%3D&md5=3c1b69b6c676591474cc7e7c51fdb296CAS | 16672246PubMed |
Moench, G. L. (1927). Uterus duplex bicollis, vagina simplex and superfetation. Am. J. Obstet. Gynecol. 13, 60–64.
Murless, B. C., and McLaughlin, F. L. (1937). Does superfetation occur? BMJ 1, 1309–1311.
| Does superfetation occur?Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BC3MzmslSgtw%3D%3D&md5=5580da70fd5c0d6dcb2412cc18468afeCAS | 20780746PubMed |
Nance, W. E., Winter, P. M., Segreti, W. O., Corey, L. A., Parisi-Prinzi, G., and Parisi, P. (1978). A search for evidence of hereditary superfetation in man. Prog. Clin. Biol. Res. 24, 65–70.
| 724709PubMed |
Nelson, W. W., and Greene, R. R. (1958). Some observations on the histology of the human ovary during pregnancy. Am. J. Obstet. Gynecol. 76, 66–90.
| 1:STN:280:DyaG1c%2FovVantw%3D%3D&md5=b782c561c37a9e66ca0d0ad7bdc1277aCAS | 13545282PubMed |
Nepomnaschy, P. A., Weinberg, C. R., Wilcox, A. J., and Baird, D. D. (2008). Urinary hCG patterns during the week following implantation. Hum. Reprod. 23, 271–277.
| Urinary hCG patterns during the week following implantation.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXptlCktA%3D%3D&md5=0fd4ea4dc71a2d6a0f60ce2276f40052CAS | 18083748PubMed |
Nilsson, E., Rogers, N., and Skinner, M. K. (2007). Actions of anti-Müllerian hormone on the ovarian transcriptome to inhibit primordial to primary follicle transition. Reproduction 134, 209–221.
| Actions of anti-Müllerian hormone on the ovarian transcriptome to inhibit primordial to primary follicle transition.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXhtVKlsrfO&md5=89fe7fbdc5738395d0cb0c101346f1d1CAS | 17660231PubMed |
Nørgaard-Pedersen, B., Moller, J., Trolle, D., and Sorensen, S. A. (1976). Alpha-fetoprotein concentration in cord blood from twins and from a set of quadruplets – a case of superfetatio? Hum. Hered. 26, 72–80.
| Alpha-fetoprotein concentration in cord blood from twins and from a set of quadruplets – a case of superfetatio?Crossref | GoogleScholarGoogle Scholar |
Okamura, K., Murotsuki, J., Iwamoto, M., Endo, H., Watanabe, T., Ohashi, K., and Yajima, A. (1992). A probable case of superfecundation. Fetal Diagn. Ther. 7, 17–20.
| A probable case of superfecundation.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaK38zgsVClsw%3D%3D&md5=d8d26ab7ec161c6b2068a903dba22d01CAS | 1610497PubMed |
Pape, O., Winer, N., Paumier, A., Philippe, H. J., Flatrès, B., and Boog, G. (2008). Superfetation: case report and review of the literature. J. Gynecol. Obstet. Biol. Reprod. (Paris) 37, 791–795.
| Superfetation: case report and review of the literature.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD1cjovVaksA%3D%3D&md5=74454e722810a538b7567258c2f3f897CAS |
Plaisier, M., Koolwijk, P., Willems, F., Helmerhorst, F. M., and van Hinsbergh, V. W. (2008). Pericellular-acting proteases in human first trimester decidua. Mol. Hum. Reprod. 14, 41–51.
| Pericellular-acting proteases in human first trimester decidua.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXlsV2nurc%3D&md5=fed2f99ec25edcf30b66a54233d28b1aCAS | 18175789PubMed |
Radasch, H. E. (1921). Superfetation or superfecundation? Surg. Gynecol. Obstet. 32, 339–352.
Roellig, K., Goeritz, F., Fickel, J., Hermes, R., Hofer, H., and Hildebrandt, T. B. (2010). Superconception in mammalian pregnancy can be detected and increases reproductive output per breeding season. Nat. Commun. 1, 78.
| Superconception in mammalian pregnancy can be detected and increases reproductive output per breeding season.Crossref | GoogleScholarGoogle Scholar | 20865801PubMed |
Roellig, K., Menzies, B. R., Hildebrandt, T. B., and Goeritz, F. (2011). The concept of superfetation: a critical review on a ‘myth’ in mammalian reproduction. Biol. Rev. Camb. Philos. Soc. 86, 77–95.
| The concept of superfetation: a critical review on a ‘myth’ in mammalian reproduction.Crossref | GoogleScholarGoogle Scholar | 20394608PubMed |
Sammour, A., Biljan, M., Tan, S. L., and Tulandi, T. (2001). A documented clomiphene-induced follicular development in pregnancy. Hum. Reprod. 16, 1098–1099.
| A documented clomiphene-induced follicular development in pregnancy.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD3MzhsVWitg%3D%3D&md5=7540482982a8579e290420fadded2e0fCAS | 11387275PubMed |
Schindler, A. E. (2005). Endocrinology of pregnancy: consequences for the diagnosis and treatment of pregnancy disorders. J. Steroid Biochem. Mol. Biol. 97, 386–388.
| Endocrinology of pregnancy: consequences for the diagnosis and treatment of pregnancy disorders.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXht1OntL3P&md5=eae417cc294a0f1e00bd60cfaa522ddaCAS | 16216491PubMed |
Schwarz, T., and Wierzchoś, E. (2010). The distribution of corpora lutea and ovarian follicular development in pregnant goats. Reprod. Biol. 10, 53–66.
| 20349023PubMed |
Scrimgeour, J. B., and Baker, T. G. (1974). A possible case of superfetation in man. J. Reprod. Fertil. 36, 69–73.
| A possible case of superfetation in man.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaE2c%2Fnt1Oqtw%3D%3D&md5=eef06a739d38fe08c49e536b965cf3e6CAS | 4809712PubMed |
Serafini, P., Yee, B., Vargyas, J., and Marrs, R. P. (1985). Development of multiple ovarian follicles for in vitro fertilization in a patient with an undiagnosed ectopic pregnancy. Fertil. Steril. 43, 656–658.
| 1:STN:280:DyaL2M7otVWjtQ%3D%3D&md5=110ee6906d2c18a2a9e67fd3872d710bCAS | 3157607PubMed |
Shalev, J., Blankstein, J., Mashiach, R., Lampley, C. E., Bar-Hava, I., Vardimon, D., Ben-Rafael, Z., and Meizner, I. (2000). Sonographic visualization of normal-size ovaries during pregnancy. Ultrasound Obstet. Gynecol. 15, 523–526.
| Sonographic visualization of normal-size ovaries during pregnancy.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD3cvltFajtg%3D%3D&md5=d1a167fb1c503d17b35bf5e57f7cb35aCAS | 11005122PubMed |
Sharma, V., Riddle, A., Collins, W., Campbell, S., and Mason, B. (1987). Gonadotrophin-induced successful follicular development, oocyte recovery, fertilization and cleavage of embryos in undiagnosed early pregnancy. J. In Vitro Fert. Embryo Transf. 4, 61–63.
| Gonadotrophin-induced successful follicular development, oocyte recovery, fertilization and cleavage of embryos in undiagnosed early pregnancy.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaL2s3isVCrsw%3D%3D&md5=06608db8b95c93b3ffa2f9e3ad598838CAS | 3108426PubMed |
Soudre, G., Guettier, X., Marpeau, L., Larue, L., Jault, T., and Barrat, J. (1992). In utero early suspicion of superfetation by ultrasound examination: a case report. Ultrasound Obstet. Gynecol. 2, 51–54.
| In utero early suspicion of superfetation by ultrasound examination: a case report.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD3s3ntVCkuw%3D%3D&md5=626870ae630d32d14d3e46638aac172cCAS | 12797008PubMed |
Squires, E. L., Garcia, M. C., and Ginther, O. J. (1974). Effects of pregnancy and hysterectomy on the ovaries of pony mares. J. Anim. Sci. 38, 823–830.
| 1:STN:280:DyaE2c7ksFKntQ%3D%3D&md5=6fecfd5f0f43e9173a76c9e7d29d11efCAS | 4823192PubMed |
Studdiford, W. E. (1936). Is superfetation possible in the human being? Am. J. Obstet. Gynecol. 31, 845–855.
Tabaste, J. L., Peter, J., Catanzano, G., and Grousseau, D. (1981). Bilateral extrauterine pregnancy. A case of super-fetation? Nouv. Presse Med. 10, 133–134.
| 1:STN:280:DyaL3M7nsVKltg%3D%3D&md5=c6a3801275a31a1de56c7d7b08f58a7eCAS | 7220307PubMed |
Tavaniotou, A., Smitz, J., Bourgain, C., and Devroey, P. (2001). Ovulation induction disrupts luteal phase function. Ann. N. Y. Acad. Sci. 943, 55–63.
| Ovulation induction disrupts luteal phase function.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXnvVygur4%3D&md5=ba224d8591b9d3a306ef0bc2a58aae29CAS | 11594558PubMed |
te Velde, E. R., and Pearson, P. L. (2002). The variability of female reproductive ageing. Hum. Reprod. Update 8, 141–154.
| The variability of female reproductive ageing.Crossref | GoogleScholarGoogle Scholar | 12099629PubMed |
Tovanabutra, S., Illingworth, P. J., Ledger, W. L., Glasier, A. F., and Baird, D. T. (1993). The relationship between peripheral immunoactive inhibin, human chorionic gonadotrophin, oestradiol and progesterone during human pregnancy. Clin. Endocrinol. (Oxf.) 38, 101–107.
| The relationship between peripheral immunoactive inhibin, human chorionic gonadotrophin, oestradiol and progesterone during human pregnancy.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK3sXitVGntLk%3D&md5=88ac18e92e101037e205dcc0befd05c4CAS |
Tuppen, G. D., Fairs, C., de Chazal, R. C., and Konje, J. C. (1999). Spontaneous superfetation diagnosed in the first trimester with successful outcome. Ultrasound Obstet. Gynecol. 14, 219–221.
| Spontaneous superfetation diagnosed in the first trimester with successful outcome.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD3c%2FhvVGnug%3D%3D&md5=23173a17303252edaaeb1aeffe72c748CAS | 10550885PubMed |
Urman, B. C., and McComb, P. F. (1989). A biphasic basal body temperature record during pregnancy. Acta Eur. Fertil. 20, 371–372.
| 1:STN:280:DyaK3M3gsF2lsA%3D%3D&md5=22c4d7cdeb0b732424f74df276b5f2b7CAS | 2488983PubMed |
van Gestel, I., Ijland, M. M., Hoogland, H. J., and Evers, J. L. (2003). Endometrial wave-like activity in the non-pregnant uterus. Hum. Reprod. Update 9, 131–138.
| Endometrial wave-like activity in the non-pregnant uterus.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD3s3ivFOmuw%3D%3D&md5=1225474ce01026d0f809cde8eb94239eCAS | 12751775PubMed |
Weinberg, P. C. (1961). Superfetation. Report of a case and proposed method of radiological diagnosis. Am. J. Obstet. Gynecol. 82, 226–227.
| 1:STN:280:DyaF3c7gsVWhug%3D%3D&md5=057ac4fb2b8cd46ffa61d6a7b8382e4fCAS | 13783883PubMed |
White, C. A., and Bradbury, J. T. (1965). Ovarian theca lutein cysts: experimental formation in women prior to repeat caesarean section. Am. J. Obstet. Gynecol. 92, 973–980.
| 1:STN:280:DyaF2M7isFOrug%3D%3D&md5=4b88903d65aa0712934a7575362df171CAS | 14321114PubMed |