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Hewitt Centre for Reproductive Medicine, Liverpool Women’s NHS Foundation Trust, Liverpool, UK
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Hewitt Centre for Reproductive Medicine, Liverpool Women’s NHS Foundation Trust, Liverpool, UK
Liverpool Women's NHS Foundation Trust, Member of Liverpool Health Partners, Liverpool, UK
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Liverpool Women's NHS Foundation Trust, Member of Liverpool Health Partners, Liverpool, UK
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Liverpool Women's NHS Foundation Trust, Member of Liverpool Health Partners, Liverpool, UK
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Liverpool Women's NHS Foundation Trust, Member of Liverpool Health Partners, Liverpool, UK
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Abstract
Embryo implantation is vital for successful conception but remains to be fully understood. Trophoblast invasion is key for implantation, with anchorage and depth of placentation determined by its extent. There is a dearth of synchronous information regarding IVF, implantation site, and trophoblastic thickness (TT). Our aim was to determine whether pregnancy implantation site and TT, had an impact on outcomes of IVF pregnancies. This prospective observational study was undertaken at a tertiary referral UK fertility unit over 14 months, collecting data on implantation site and TT from three-dimensional (3D) images of the uterus following early pregnancy scan. Of the 300 women recruited, 277 (92%) had live births, 20 (7%) miscarried, 2 (0.7%) had stillbirths, and 1 (0.3%) had a termination. Significantly more pregnancies that resulted in miscarriage (7/20, 35%) were located in the lower uterine cavity when compared to ongoing pregnancies (15/277, 5%) (P < 0.01). TT was significantly higher in ongoing pregnancies when compared with those who miscarried (7.2 mm vs 5.5 mm; P < 0.01). Implantation in the lower half of the uterine cavity and decreased TT are significantly associated with an increased rate of miscarriage. Identification of those at risk should prompt increased monitoring with the aim of supporting these pregnancies.
Lay summary
Implantation of an embryo in the womb is vital for a successful pregnancy. We wanted to find out whether findings on an ultrasound scan in early pregnancy had an impact on outcomes of IVF pregnancies. Three hundred women were recruited to the study, 277 (92%) had live births and unfortunately 20 (7%) had a miscarriage, 2 (0.7%) had stillbirths, and 1 (0.3%) had a termination. Many more of the pregnancies that miscarried implanted in the lower part of the womb. The thickness of the infiltration of the pregnancy into the womb was significantly higher in the ongoing pregnancies. We concluded that implantation in the lower half of the womb and reduced infiltration of the pregnancy seen on scan are associated with an increased rate of miscarriage. We propose that when we identify those at risk, we should increase monitoring, with the aim of supporting these pregnancies.
Colorado State University, Fort Collins, Colorado, USA
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Omaha’s Henry Doorly Zoo and Aquarium, Omaha, Nebraska, USA
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Omaha’s Henry Doorly Zoo and Aquarium, Omaha, Nebraska, USA
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The refinement of embryo culture media is essential in improving embryo viability and in vitro production efficiency. Our previous work demonstrated that the nutrients (carbohydrates, amino acids, and vitamins) in traditional culture media far exceed the need for an embryo and producing developmentally competent embryos in a reduced nutrient environment is feasible. Here, we aim to evaluate the impact of exogenous lipid and l-carnitine supplementation on bovine blastocyst development and refine our RN condition further. Zygotes were cultured in the control medium (100% nutrients) and reduced nutrient media containing 6.25% of the standard nutrient concentrations supplemented with l-carnitine and lipid-free or lipid-rich BSA. Increased blastocyst development was observed in the reduced nutrient lipid-rich medium compared to the other two groups. However, in both reduced nutrient conditions, blastocyst cell numbers were lower than those obtained in the control condition. We then examined the expression level of 18 transcripts correlated with lipid metabolism, glucose metabolism, redox balance, and embryo quality, along with mitochondrial DNA copy numbers, ATP productions, and lipid profile. The results indicated that lipid metabolism, embryo quality, and redox enzyme-related genes were upregulated while the glucose-related gene was downregulated in embryos derived from reduced nutrient lipid-rich condition. Finally, we identified that the lipid-rich BSA has enriched linoleic, stearic, oleic, palmitic, and alpha-linoleic fatty acids, a lipid profile that may contribute to the increased lipid metabolism and improved blastocyst development of the bovine embryos under the reduced nutrient condition.
Lay summary
Assisted conception is a vital technique for cattle breeding. Embryos can be produced by IVF and grow in a special substance known as embryo culture medium. Previous studies suggested that culture medium with a high level of nutrients may have a negative impact on embryo growth. Here, we developed a special culture medium with very low levels of carbohydrates, amino acids, and vitamins, which contained more lipids and a special compound, to make it easier for lipids to move into the cells. The cattle embryos in this culture medium used more lipids and less glucose, and develop much better than ones in the culture medium with high levels of nutrients. Our work provides a unique model to study embryo metabolism and to help improve culture medium.
GROW School for Oncology and Reproduction, Maastricht University, Universiteitssingel, Maastricht, The Netherlands
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Department of Clinical Genetics, Maastricht University Medical Centre (MUMC+), Maastricht, The Netherlands
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GROW School for Oncology and Reproduction, Maastricht University, Universiteitssingel, Maastricht, The Netherlands
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GROW School for Oncology and Reproduction, Maastricht University, Universiteitssingel, Maastricht, The Netherlands
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GROW School for Oncology and Reproduction, Maastricht University, Universiteitssingel, Maastricht, The Netherlands
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Department of Clinical Genetics, Maastricht University Medical Centre (MUMC+), Maastricht, The Netherlands
Division of Obstetrics and Gynaecology, Department of Clinical Science, Intervention & Technology (CLINTEC), Karolinska Institutet, Stockholm, Sweden
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GROW School for Oncology and Reproduction, Maastricht University, Universiteitssingel, Maastricht, The Netherlands
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Graphical abstract
Abstract
Sex steroids are converted to bioactive metabolites and vice versa by endometrial steroid-metabolising enzymes. Studies indicate that alterations in this metabolism might affect endometrial receptivity. This pilot study determined whether the endometrial formation and inactivation of 17β-oestradiol differed between the supposedly embryo-receptive endometrium and non-receptive endometrium of women undergoing IVF/intracytoplasmic sperm injection (ICSI).
Endometrial biopsies were obtained from IVF/ICSI patients 5–8 days after ovulation in a natural cycle, prior to their second IVF/ICSI cycle with fresh embryo transfer (ET). Endometrial biopsies from patients who achieved clinical pregnancy after fresh ET (n = 15) were compared with endometrial biopsies from patients that did not conceive after fresh ET (n = 15). Formation of 17β-oestradiol (oxidative 17β-hydroxysteroid dehydrogenases (HSDs)), oestrone (reductive HSD17Bs) and inhibition of HSD17B1 activity were determined by high-performance liquid chromatography. The endometrial transcriptome was profiled using RNA sequencing followed by principal component analysis and differentially expressed gene analysis. The false discovery rate-adjusted P < 0.05 and log fold change >0.5 were selected as the screening threshold.
Formation and inactivation of 17β-oestradiol resulted similar between groups. Inhibition of HSD17B1 activity was significantly higher in the non-pregnant group when only primary infertile women (n = 12) were considered (27.1%, n = 5 vs 16.2%, n = 7, P = 0.04). Gene expression analysis confirmed the presence of HSD17B1 (encoding HSD17B1), HSD17B2 (encoding HSD17B2) and 33 of 46 analysed steroid metabolising enzymes in the endometrium. In the primary infertile subgroup (n = 10) 12 DEGs were found including LINC02349 which has been linked to implantation. However, the exact relationship between steroid-metabolising enzyme activity, expression and implantation outcome requires further investigation in larger, well-defined patient groups.
Lay summary
Sex hormones are produced and broken down by enzymes that can be found in the endometrium (the inner lining of the womb). This enzyme activity might influence the chances of becoming pregnant. We compared (i) enzyme activity in the endometrium of 15 women who did and 15 women who did not become pregnant in their second in vitro fertilisation attempt, (ii) how enzyme activity can be blocked by an inhibitor, and (iii) differences in gene expression (the process by which instructions in our DNA are converted into a product). Enzyme activity was similar between groups. We found that in women who have never been pregnant in the past, inhibition of enzyme activity was higher and found differences in a gene that has been linked to the implantation of the embryo, but future studies should be performed in larger, well-defined patient groups to confirm these findings.
Genus PLC/ABS, Mogi Mirim, SP, Brazil
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Department of Livestock Development, Bureau of Biotechnology in Livestock Production, Pathum Thani, Thailand
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The WNT inhibitory protein DKK1 has been shown to regulate the development of the preimplantation embryo to the blastocyst stage. In cattle, DKK1 increases the number of trophectoderm cells that are the precursor of the placenta. DKK1 can affect cells by blocking WNT signaling through its receptors KREMEN1 and KREMEN2. Here it was shown that the mRNA for KREMEN1 and KREMEN2 decline as the embryo advances in development. Nonetheless, immunoreactive KREMEN1 was identified in blastocysts using western blotting. DKK1 also decreased the amount of immunoreactive β-catenin in blastocysts, as would be expected if DKK1 was signaling through a KREMEN-mediated pathway. Thus, it is likely that KREMEN1 functions as a receptor for DKK1 in the preimplantation bovine embryo.
Lay summary
DKK1 is a molecule produced by the lining of the womb (uterus) that regulates the development of the early embryo. Here it was shown that a substance that responds to DKK1 called KREMEN1 is found in the embryos of cattle. In other cells, joining of DKK1 to KREMEN1 results in reduction in amounts of a protein called β-catenin. For the present study, it was shown that DKK1 treatment also reduced β-catenin in the cattle, which suggests that DKK1 can regulate the cattle embryo by attaching to KREMEN1.
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Bisphenol A (BPA) is an endocrine-disrupting compound, used as the key monomer of polycarbonate plastics and epoxy resins. BPA has been detected in both humans and farm animals and has been correlated with decreased sperm counts and motility. BPS and BPF are structural analogs of BPA and are increasingly being used in manufacturing as BPA substitutes. In this study, we aim to assess the direct outcomes of BPA, bisphenol S (BPS), and bisphenol F (BPF) exposure on bovine sperm parameters in vitro to elucidate how they affect sperm quality and fertilization potential, and to assess whether BPS and/or BPF are less harmful than BPA. Sperm from three or more bulls was obtained from either fresh samples or cryopreserved straws and exposed to 0.05 mg/mL of BPA, BPS, and BPF in vitro. After 4 h incubation, motility, capacitation, apoptosis/necrosis, and mitochondrial membrane potential levels were measured by computer-assisted sperm analysis or computational flow cytometry. Results showed that BPA exposure significantly reduced both fresh and cryopreserved sperm motility, capacitation, viability and mitochondrial membrane potential levels. Furthermore, BPF significantly decreased motility, capacitation and mitochondrial membrane potential in cryopreserved sperm only. BPS did not have any significant effects on any of the parameters measured. Our results suggest that BPA is the most harmful to sperm, while BPF is toxic under certain conditions, and BPS seems to be the least detrimental. Overall, this study provides an understanding of how the ubiquitous environmental chemicals, bisphenols, may impact male fertility even after ejaculation.
Lay summary
Bisphenol A (BPA) is a widespread man-made compound found in plastic products and the environment, and has been detected in human and animal biological fluids. BPA has been previously investigated for its negative effects on health, including its detrimental impacts on reproductive cells. Concerns over the use of BPA has led to its ban in some countries and has introduced the use of ‘BPA-free’ products, which typically contain substitutes such as bisphenols S and F (BPS and BPF). This current study investigates the effects of bull sperm exposure to BPA, BPS, and BPF to evaluate their impacts on sperm quality. After exposure, both BPA and BPF lowered sperm mobility, organelle function (by reducing mitochondrial activity), and overall survival; while BPS had no effects. Overall, this study shows that BPA and its common replacement, BPF, can both act on sperm directly, reducing their overall quality and function.
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Paediatric Oncology, Leeds Children’s Hospital, Leeds, UK
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In the context of a cancer diagnosis, fertility preservation interventions are used to mitigate the potential impact of gonadotoxic cancer treatment upon fertility. They provide patients with cancer the option to freeze their reproductive material to have their own biological child following treatment. The evidence suggests some clinicians are less likely to have fertility preservation discussions with patients who have an aggressive or metastatic cancer which has a poor prognosis. Although this is contrary to current policy recommendations, there is a lack of guidance relating to offering fertility preservation in the context of a poor prognosis to support clinicians. Controversy surrounds posthumous reproduction, and whether the wishes of the cancer patient, when living and deceased should take precedence over others’ well-being. We consider the question of whether cancer patients with a poor prognosis should be offered fertility preservation from an ethics perspective. We structure the paper around key arguments to which multiple ethical principles might pertain, first establishing a central argument in favour of offering fertility preservation based on respect for autonomy, before exploring counterarguments. We conclude by proposing that a defeasible assumption should be adopted in favour of offering fertility preservation to all cancer patients who might benefit from it. It is important to recognise that patients could benefit from fertility preservation in many ways, and these are not limited to having a parenting experience. The burden of proof rests on the clinician in collaboration with their multidisciplinary team, to show that there are good grounds for withholding the offer.
Lay summary
When a person is diagnosed with cancer, they may wish to consider undergoing fertility preservation procedures. These procedures give patients a chance to have their own biological child after completing cancer treatment. However, research suggests that cancer patients who have a poor prognosis are less likely to be offered fertility preservation treatment. In this paper, we consider the ethical implications of offering (or not) fertility preservation to this patient group, including using their sperm or eggs to reproduce after their death. We conclude that fertility preservation treatments should be offered to all cancer patients who might benefit from it, and we outline the many ways that benefit from this treatment can be gained. The decision to withhold the offer of fertility preservation treatment should be made between the patient’s clinician and their wider care team. They must be able to provide good reasons to explain why it was withheld.
APC Microbiome Ireland, University College Cork, Cork, Ireland
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Many parts of the animal and human body host groups of bacteria, viruses, and fungi that together are known as the microbiome. Microbiomes do not cause disease but are important for the healthy working of many systems in the body, including for reproduction and fertility. While the microbiome that lives in a reproductive tract play the most direct role, microbiomes from other areas of the body may also affect reproductive health. However, not much is known about how these groups of microorganisms regulate fertility as well as the health of parents and offspring and help animals to cope with environmental changes. Furthermore, compared to the large amount of research in laboratory species and humans, there is less information about domestic or wild animal species. This special series of Reproduction and Fertility on microbiomes is aimed at filling this gap with articles from experts highlighting important evidence in reproductive microbiomes, current research gaps, and new directions.
Department of Production Animal Studies, Faculty of Veterinary Science, University of Pretoria, Onderstepoort, South Africa
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Mammal Research Institute, Faculty of Natural and Agricultural Sciences, University of Pretoria, Hatfield, South Africa
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Recent loss of rhinoceros subspecies has renewed interest in using more advanced assisted reproductive technologies (ART) in rhinoceroses and elephants. Currently, only semen collection, semen preservation and artificial insemination (AI) have been used repeatedly with success in these species. Although ovum pick-up (OPU) and intra-cytoplasmic sperm injection (ICSI) have been reported recently in rhinoceroses, the techniques are not yet optimised. In contrast, multiple ART applications are routinely used in the horse. Since elephants and rhinoceroses share some reproductive features with equids, we postulate that procedures such as OPU, ICSI, in vitro fertilisation (IVF) and embryo transfer (ET), which are well established in the horse, may represent a basis to develop protocols for endangered pachyderms. In this review, we summarise current knowledge on reproductive physiology relevant to ART. We discuss the current state of ART in all three families and the requirements for the successful implementation of OPU, ICSI, IVF and ET in these species.
Lay summary
Wild rhinoceros and elephant populations are facing ongoing threats; therefore, additional measures are required to protect these species for future generations. Assisted reproductive technologies (ART) include the collection of semen to directly inseminate females or to fertilise oocytes (eggs) in a laboratory to produce embryos, which can be transferred into a recipient female at a later date. While these techniques are routinely used in humans and domestic animals such as the horse, more research is needed to incorporate such technologies into the breeding of elephants and rhinoceroses. As the horse is the closest related domestic species to the rhinoceros, it may serve as the best possible role model. We discuss the current state of ART in the horse, elephant and rhinoceros and the possibilities for future use of these techniques in breeding such endangered animals.
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McMaster University Health Sciences Center, Hamilton, Ontario, Canada
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Endometriosis is a chronic disease associated with debilitating pain that affects many people assigned female at birth, from menarche through menopause, not just causing pain and infertility but also negatively impacting quality of life, participation in daily activities, productivity, and income. It is associated with increased incidence of obstetric and neonatal complications, anxiety, other chronic diseases, and substantial healthcare costs. Despite the profound negative impact of endometriosis on quality of life, current treatment options remain suboptimal and many patients express dissatisfaction with current care. The prevailing acute-care, single-provider model in which the provider works in relative isolation and thus with limited diagnostic and therapeutic strategies readily available proves inadequate for treating endometriosis. Patients would benefit from earlier diagnosis and referral to a center capable of providing a comprehensive and multimodal management plan that utilizes a chronic care model. Often this can only be achieved through multidisciplinary teams of providers with expertise in endometriosis. The authors acknowledge that many low- and middle-income countries do not have the resources to support such centers but could still benefit from any breakthroughs in treatment they bring about. Researchers need to agree on standardized core outcome measures, relevant to patients with endometriosis and the healthcare system as a whole. Only through increased societal and healthcare provider education and recognition of endometriosis as a chronic disease can we achieve better treatment outcomes.
Lay summary
Endometriosis is a disease that affects about one out of every women. It occurs when tissue like that which is normally located inside the uterus is present outside the uterus. The body’s reaction to this tissue causes inflammation and pain, usually so severe that it disrupts daily activities. Our current medical system does not serve these patients well. Patients with endometriosis often must see many different doctors over many years before learning of their disease and getting treatment. We need to increase awareness of endometriosis and think of it as a chronic disease like diabetes or heart disease. We can improve care by creating centers where experienced teams work together to treat patients and study treatment impacts on quality of life. It is time to adopt a new model for caring for patients with endometriosis.
Department of Medical Biotechnology, National Biotechnology Development Agency, Abuja, Nigeria
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Sickle cell disease (SCD) poses an increased risk of infertility, pregnancy complications and maternal and perinatal mortality among women of reproductive age. This risk is particularly higher for women in sub-Saharan Africa, where the disease burden is highest and access to comprehensive health care is limited, as well as in other countries with a high SCD prevalence due to migration. Disease-modifying treatments for SCD could directly and indirectly harm the ovaries, potentially compromising the quality and quantity of existing oocytes. Therefore, it is essential to explore alternative interventions, such as nutritional modifications that are less harmful and cost-effective in order to improve reproductive outcomes and enhance the overall well-being of both mother and child in this population. Maintaining optimal levels of B12 may possibly provide benefits to the ovaries and pregnancy by decreasing homocysteine levels, increasing nitric oxide (NO) bioavailability and promoting antioxidant and anti-inflammatory activities. Individuals living with SCD are more susceptible to vitamin B12 (B12) deficiency. However, there is a lack of clinical data investigating the relationship between systemic levels of B12, its supplementation, and reproductive outcome measures in SCD women. Therefore, this review aims to examine the current evidence regarding the impact of SCD on female reproductive health and the role of B12 in the reproductive biology of women living with SCD.
Lay summary
Poor reproductive health is a concern for patients with sickle cell disease (SCD). SCD can lead to damage to the ovaries. Most of the therapies for sickle cell disease are toxic to the ovaries, expensive and unavailable to affected women, particularly those living in resource-poor areas such as sub-Saharan Africa. There is a need to seek less harmful and affordable interventions such as nutrition to improve reproductive outcomes for women with SCD who are of child-bearing age. Good levels of vitamin B12 have been found to maintain ovarian health and pregnancy. Patients with SCD have been reported to have a high risk of vitamin B12 deficiency, but the impact of B12 on reproduction in this group of women is yet to be evaluated. The review explores current evidence of the impact of both SCD and B12 on female reproduction.
