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NIHR Applied Research Collaboration Wessex, Southampton, UK
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NIHR Applied Research Collaboration Wessex, Southampton, UK
NIHR Southampton Biomedical Research Centre, University of Southampton and University Hospital Southampton NHS Foundation Trust, Southampton, UK
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Complete Fertility, Princess Anne Hospital, Southampton, UK
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Graphical Abstract
Abstract
Endometriosis is a chronic and debilitating condition which can affect the entire reproductive life course of women with a potentially detrimental effect on pregnancy. Pregnancy (and increasing parity) can affect endometriosis by modulating disease severity and suppressing symptoms. Multiparous women could be less likely to suffer from endometriosis-related pregnancy complications than primiparous women. We aimed to systematically review the evidence examining the role of parity in the relationship between pregnancy outcomes and endometriosis. A systematic search of MEDLINE, EMBASE, CINAHL, Web of Science, and Cochrane Library was performed from inception to May 2022. We searched for experimental and observational studies. Grading of Recommendations, Assessment, Development, and Evaluation was used to assess the quality of evidence with the risk of bias in non-randomised studies of interventions tool incorporated. Eleven studies were included in the meta-analysis. Primiparous women with endometriosis had almost double the risk of hypertensive disorders of pregnancy (OR: 1.99, 95% CI: 1.50–2.63, P < 0.001) compared to multiparous women with endometriosis. Primiparous women with endometriosis were at significantly increased risk of preterm delivery, caesarean delivery, and placenta praevia compared to primiparous women without endometriosis. There were no significant differences in outcomes when multiparous women with endometriosis were compared to multiparous women without endometriosis. There is limited evidence to suggest that primiparous women with endometriosis may be at higher risk of adverse pregnancy outcomes compared to multiparous women. The modulatory role of parity in the pathophysiology of endometriosis and its impact on pregnancy outcomes should be investigated.
Lay summary
Endometriosis can adversely affect pregnancy and cause complications that can affect both mother and baby. The severity and symptoms of endometriosis are lessened in pregnancy and with increasing births. Women who have previously given birth could experience fewer pregnancy complications than women giving birth for the first time. We reviewed the literature to compare pregnancy outcomes in women with endometriosis by whether they had given birth before or not. Our review included 11 studies. More women with endometriosis giving birth for the first time had blood pressure disorders in pregnancy than women with endometriosis who had given birth before. First-time mothers with endometriosis tended to have a baby born early, caesarean delivery, and an abnormally located placenta compared to those without endometriosis. This study supports the theory that women with endometriosis in their first pregnancy are at higher risk of complications and may benefit from additional monitoring.
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Reproductive Medicine Research Group, School of Medicine, Ninewells Hospital and Medical School, University of Dundee, Dundee, UK
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Sperm cryopreservation for men with severely impaired spermatogenesis is one of the commonest reasons for short-term sperm storage, usually in advance of fertility treatment. Cryopreservation is generally very effective, although not all spermatozoa survive the process of freezing and thawing. This review considers various aspects of freezing sperm, including an overview of methods, appropriate use of cryoprotectants and practical considerations, as well as oxidative stress and mechanisms of cell cryodamage.
Lay summary
Cryopreservation involves freezing of cells or tissues to preserve them for future use. Sperm cryopreservation for men with a very low sperm count is one of the commonest reasons for short-term sperm storage, usually in advance of fertility treatment. Cryopreservation is generally very effective, although not all sperm cells survive the process of freezing and thawing. This review covers various aspects of freezing sperm, including consideration of methods used and mechanisms of cell damage.
Ningbo Jiangshan High School, Ningbo, Zhejiang, PR China
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Skin Diseases Research Center, Yangtze Delta Region Institute of Tsinghua University, Jiaxing, Zhejiang, PR China
Zhejiang Provincial Key Laboratory of Applied Enzymology, Yangtze Delta Region Institute of Tsinghua University, Jiaxing, Zhejiang, PR China
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The Chinese soft-shelled turtle, Pelodiscus sinensis (Reptilia: Trionychidae), is a typical seasonal breeding species, and its spermatogenesis pattern is complex. In this study, the process of sperm cell development was studied using histology. The process of sperm cell development may be divided into six stages based on a combination of different cell types in the seminiferous epithelium. A close examination revealed two patterns of sperm cell development in the seminiferous tubules during the breeding season. The first is a normal sperm cell development pattern, in which the process of sperm cell development and maturation are completed in the seminiferous epithelium without round spermatozoa in the lumen. The second is rapid sperm cell development, in which the first batches of round spermatozoa fall off the seminiferous epithelium before they mature, thus beginning a second batch of sperm cell development. The round sperm cells are shed into the lumen and further mature in the seminiferous tubules and epididymis. This rapid sperm cell development process of the Chinese soft-shelled turtle is rare in other vertebrate species and may be an adaptation to cope with seasonal breeding. The results of this study provide insight into the theory of seasonal reproduction in reptiles.
Lay summary
The Chinese soft-shelled turtle is a typical seasonal breeding species, and the process of sperm cell development is complex. In this study, the process of sperm cell development is divided into six stages in Chinese soft-shelled turtles and revealed two patterns of sperm cell development in the testis during the breeding season. The first is a normal sperm cell development pattern, in which the process of sperm cell development and maturation are completed in the testis. The second is a rapid pattern, in which the round sperm cells fall off before they mature and further mature in the epididymis. This rapid sperm cell development process of the Chinese soft-shelled turtle is rare in other vertebrate species and may be an adaptation to cope with seasonal breeding. The results of this study provide insight into the theory of seasonal reproduction in reptiles.
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Lay summary
Anabolic steroids (also known as ‘steroids’) are banned drugs like testosterone, which make muscles bigger in men. These drugs are dangerous because they stop the testes from making natural testosterone and can cause heart attacks. Men stopping steroids have very low testosterone, which makes them feel weak, depressed, suicidal, infertile, and unable to have erections. We surveyed over 100 doctors to find out how they treat men giving up steroids. We report that doctors differ widely in the way they treat these men. Most doctors simply advise men to wait for the natural recovery of testosterone levels to happen. But 20% of doctors give men drugs to boost testosterone and make men feel better. Unfortunately, many patients had not recovered by the time of our survey. In summary, our survey highlights differences and limitations in the treatment of men giving up steroids. The use of steroids is increasing rapidly among young men, so we recommend further work to improve the treatment of men who are motivated to give up steroids.
Regenerative Biology Group, Fertility Reserve Bank San Clemente, California, USA
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Ovarian platelet-rich plasma (PRP) is claimed to restore the fertility potential by improving reserve, an effect perhaps mediated epigenetically by platelet-discharged regulatory elements rather than gonadotropin-activated G-protein coupled receptors, as with stimulated in vitro fertilization (IVF). The finding that fresh activated platelet releasate includes factors able to promote developmental signaling networks necessary to enable cell pluripotency tends to support this theory. The mechanistic uncertainty of intraovarian PRP notwithstanding, at least two other major challenges confront this controversial intervention. The first challenge is to clarify how perimenopausal ovarian function is reset to levels consistent with ovulation. Perhaps a less obvious secondary problem is to confine this renewal such that any induced recalibration of cellular plasticity is kept within acceptable physiologic bounds. Thus, any ‘drive’ to ovarian rejuvenation must incorporate both accelerator and brake. Ovarian aging may be best viewed as a safeguard against pathologic overgrowth, where senescence operates as an evolved tumor-suppression response. While most ovary cells reach the close of their metabolic life span with low risk for hypertrophy, enhanced lysosomal activity and the proinflammatory ‘senescence-associated secretory phenotype’ usually offsets this advantage over time. But is recovery of ovarian fitness possible, even if only briefly prior to IVF? Alterations in gap junctions, bio-conductive features, and modulation of gene regulatory networks after PRP use in other tissues are discussed here alongside early data reported from reproductive medicine.
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Faculty of Medicine, Universitas Trisakti, Jakarta, Indonesia
National Research and Innovation Agency, Jakarta, Indonesia
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School of Medical Science, Griffith University, Gold Coast Campus, QLD, Australia
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Polycystic ovary syndrome (PCOS) is an endocrine metabolic disorder that appears to have a genetic predisposition and a fetal origin. The fetal ovary has two major somatic cell types shown previously to be of different cellular origins and different morphologies and to differentially express 15 genes. In this study, we isolated the somatic gonadal ridge epithelial-like (GREL) cells (n = 7) and ovarian fetal fibroblasts (n = 6) by clonal expansion. Using qRT-PCR, we compared the gene expression levels of PCOS candidate genes with previous data on the expression levels in whole fetal ovaries across gestation. We also compared these levels with those in bovine adult ovarian cells including fibroblasts (n = 4), granulosa cells (n = 5) and surface epithelial cells (n = 5). Adult cell types exhibited clear differences in the expression of most genes. In fetal ovarian cells, DENND1A and ERBB3 had significantly higher expression in GREL cells. HMGA2 and TGFB1I1 tended to have higher expression in fetal fibroblasts than GREL cells. The other 19 genes did not exhibit differences between GREL cells and fetal fibroblasts and FBN3, FSHB, LHCGR, FSHR and ZBTB16 were very lowly expressed in GREL cells and fibroblasts. The culture of fetal fibroblasts in EGF-containing medium resulted in lower expression of NEIL2 but higher expression of MAPRE1 compared to culture in the absence of EGF. Thus, the two fetal ovarian somatic cell types mostly lacked differential expression of PCOS candidate genes.
Lay summary
Polycystic ovary syndrome (PCOS) is one of the most common reproductive problems. The cause is not known so there are no specific treatments or prevention strategies. We know it can be linked to issues that occur in the womb and that some people may be more likely to get PCOS due to their genetic makeup. Our recent studies showed that many of the genes linked to PCOS were found to be switched on in the fetal ovary and are likely to be involved in the development of the fetal ovary. In order to improve our understanding of PCOS, we need to identify the type of cells in the fetal ovary where these genes are switched on. In this study, we examined the PCOS genes in two types of cells that mature as the fetal ovary develops and found very little difference between them but bigger differences to their mature adult counterparts.
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Extracellular vesicles (EVs) contained in seminal plasma, vehicle RNA, proteins, and other molecules able to influence the biological function of sperm. The aim of this study was to improve the fertilizing capacity of male gametes of low-fertility bulls using EVs isolated by ultracentrifugation from the seminal plasma of a bull of proven fertility. After a dose–response curve study, 10×106 sperm of low-fertility bulls were co-incubated for 1 h with 400×106 EVs/mL. In addition, it has been verified that the incorporation of EVs, which takes place in the sperm midpiece, is maintained for 5 h and even after cryopreservation. Subsequently, the spermatozoa of low-fertility bulls, with EVs incorporated, were used for the in vitro production of embryos. The rate of blastocyst at seventh day yield in vitro, with the use of sperm with EVs incorporated, increased by about twice the yield obtained with the same sperm in the absence of EVs: bulls having an average embryonic yield of 6.41 ± 1.48%, 10.32 ± 4.34%, and 10.92 ± 0.95% improved their yield to 21.21 ± 1.99%, 22.17 ± 6.09%, and 19.99 ± 5.78%, respectively (P < 0.05). These encouraging results suggest that it might be possible to keep breeding bulls with poor fertility. Further studies will be needed to evaluate the in vivo fertility of sperm treated with EVs and understand how the content of EVs is involve in the sperm–vesicle interaction and in the improved sperm performance.
Lay summary
Sperm can fertilize eggs after they mature as they move through the tube in the testes. As they move, the sperm communicate with the lining of the tubes, thanks to small sacs which are made by the tube itself. These sacs contain many molecules that may play a part in the mechanisms that help sperm fertilize eggs. In veterinary medicine, as with humans, there are fertile and less-fertile individuals. It is possible that the sacs of the semen from a bull which is known to be fertile are different to those from a bull with low fertility. For this reason, sacs from bulls with proven fertility were mixed with sperm from the less-fertile bulls to test in the laboratory how the sperm was able to fertilize eggs and produce embryos. The results show that, in the laboratory, the number of embryos produced is doubled. This suggests it would be possible to improve the fertility of people who are less fertile.
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Risk factors associated with equine reproductive efficiency have been identified along with those associated specifically with early pregnancy loss (EPL). In contrast, no studies have reported risk factors associated with abortion (loss between days 70 and 300 post-cover). Given the causes of abortion differ from those of EPL, likely too will the risk factors. A retrospective cohort study was carried out to identify risk factors associated with abortion in UK- and Irish-based Thoroughbreds, collecting data on 20 exposure variables over a 5-year period. A generalized linear mixed model was utilized to evaluate the associations between exposure variables and abortion, with clustering of observations accounted for at the mare and farm level. Variables with a likelihood ratio test (LRT) P value < 0.2 were entered into the model in a forward stepwise approach. Pregnancy outcome was available on 4439 pregnancies from 2510 mares. Having had two or more prior abortions (odds ratio (OR): 7.91, 95% CI: 2.86, 21.88), conceiving on the second or subsequent covered estrous cycle (OR: 1.84, 95% CI: 1.22, 2.78) and conceiving multiple conceptuses (OR: 1.68, 95% CI: 1.02, 2.76) were associated with an increased risk of abortion compared to null parous, first estrous cycle covers and singleton conceptions, respectively. Increasing paternal age (OR: 0.95, 95% CI: 0.90, 0.99) was associated with a decreasing risk of abortion. Mare and farm variance were not significant in the final model, LRT P = 0.43. These findings provide evidence-based data to inform Thoroughbred breeding management practices to help mitigate abortion risk.
Lay summary
This is the first study to identify the risk factors (characteristics which change the chance of an event) for abortion (miscarriage between days 70 and 300 of pregnancy) in the horse. Statistical models were used to account for the interactions between 20 different factors. The factor which increased the mare’s risk of having an abortion the most was when she had had two or more abortions prior to the pregnancy. Additionally, when the mare was initially pregnant with twins but one of those pregnancies was reduced, the remaining pregnancy was at an increased risk of aborting. Older mares were not at an increased risk of abortion like in humans; however, pregnancies fathered by older stallions were less likely to abort than those from younger stallions. The findings of this study can inform horse breeding practices to help reduce the chance of an abortion.
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Beaumont Hospital, Dublin, Ireland
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The purpose of this study was to determine if a comprehensive flow cytometry panel could be used to assess immunophenotype profiles in menstrual blood of patients experiencing reproductive failure and age-matched controls of proven fertility. Menstrual blood samples of 58 recurrent pregnancy loss and repeated implantation failure patients, along with 15 age-matched controls of proven fertility, were obtained within the first 24 h of the onset of menstruation to non-invasively assess the local immunophenotype. Using a comprehensive multi-parameter flow panel, the lymphocyte sub-populations were described and compared. In relation to well-established peripheral blood immunophenotyping values, distinct lymphocyte population differences were noted between the subgroups. The ratios of CD4+ and CD8+ T-cells were inverted in relation to peripheral blood, and uterine natural killler (NK) cells represented by CD56bright were distinctly visualised, emphasising the distinction between menstrual and peripheral blood. In relation to controls, there were marked increases in CD3+ve T-cells (P = 0.009), CD4:CD8 ratio (P = 0.004), CD19 B-cells (P = 0.026) and CD56dim NK cells (P = 0.002) in the reproductive failure cases. The study shows that flow cytometric evaluation could provide a rapid and objective analysis of lymphocyte subpopulations in many forms of tissue and fluid. The findings show significant variations in cellular composition of immune cells indicating a distinct compartment, with differences between cases and controls. Immunological assessment of the menstrual blood immunophenotype, in clinically appropriate patients, may provide insight into the aetiology of adverse reproductive outcome, without the risks and inconveniences associated with a more invasive endometrial biopsy.
Lay summary
Unexplained infertility is a difficult issue for patients and physicians, but despite diagnostic strides and innovative methods, there are no clear solutions. The involvement of an overactive or underactive immune system in selected cases is undeniable, and the endometrial lining is the most relevant area for investigation because this is where the embryo implants. Endometrial investigations, however, are highly invasive, involve medication and have to be done at the right time. The method described and evaluated here is an alternative assessment which avoids these difficulties and can be used in a clinical setting.
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Departamento de Ginecologia, Universidade Federal de São Paulo, São Paulo, Brazil
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Biobehavioral Pediatric Pain Lab, Department of Psychiatry, Boston Children’s Hospital, Boston, Massachusetts, USA
Pain and Affective Neuroscience Center, Department of Anesthesiology, Critical Care, and Pain Medicine, Boston Children’s Hospital, Massachusetts, USA
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Wellcome Centre for Human Genetics, University of Oxford, Oxford, UK
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Endometriosis is a chronic condition that affects ~10% of women globally. Its symptoms include chronic pelvic pain, heavy periods and tiredness/fatigue, which have been associated with poorer quality of life and mental health. We aim to explore the impact of the COVID-19 pandemic on pain and fatigue symptoms and their interactions with the impact on mental health in people with endometriosis. This global cross-sectional online survey study collected data from 4717 adults with self-reported surgical/radiological diagnosis of endometriosis between May and June 2020. The survey included questions on the current status and changes of endometriosis symptoms (pelvic pain, tiredness/fatigue, and bleeding patterns), mental health, pain catastrophising, and the impact of the COVID-19 pandemic on the respondents’ lives. Compared to 6 months earlier, Respondents reported a marked worsening of their endometriosis symptoms (endometriosis-associated pain (39.3%; 95% CI: 37.7, 40.5), tiredness/fatigue (49.9%; 95% CI: 48.4, 51.2) and bleeding patterns (39.6%; 95% CI: 38.2, 41)) and mental health (38.6%; 95% CI: 37.2, 39.9). Those with a pre-existing mental health diagnosis (38.8%) were more likely to report their symptoms worsening. Worsening of pain and tiredness/fatigue was significantly correlated with worsening of mental health (P < 0.001). The relationship between changes in mental health and (a) change in pain and (b) change in fatigue was found to be weakly mediated by pain catastrophising scores (pain: B = 0.071, lower limit of confidence interval (LLCI) = 0.060, upper limit of confidence interval (ULCI) = 0.082, tiredness/fatigue: B = 0.050, LLCI = 0.040, ULCI = 0.060). This study demonstrates that stressful experiences impact the physical and mental health of people with endometriosis. The findings highlight the need to consider psychological approaches in the holistic management of people with endometriosis.
Lay summary
Endometriosis is a chronic condition in which tissue similar to that of the lining of the womb grows outside it. It affects around 10% of women globally, and the symptoms often include persistent pelvic pain, heavy periods and tiredness/fatigue. These symptoms are associated with impaired mental health and life quality. This study used an online questionnaire to assess the experiences of people with endometriosis during the first months of the pandemic. Results from 4717 adults revealed that pelvic pain, tiredness/fatigue and bleeding worsened in more than 39% of the participants. Poor mental health was also exacerbated and associated with worsening in tiredness/fatigue. Further analysis revealed that this relationship could be partially explained by ‘pain catastrophising’, which measures how participants think about their pain. Our results suggest that stressful experiences like the pandemic negatively impact the already burdened mental health of people with endometriosis, who could benefit from psychological interventions.
