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R de Koning Department of Gynaecology, Leiden University Medical Centre, Leiden, The Netherlands
Nederlandse Endometriose Kliniek, Reinier de Graaf Gasthuis, Delft, The Netherlands

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A E P Cantineau Department of Obstetrics and Gynaecology, University of Groningen, University Medical Centre Groningen, Groningen, The Netherlands

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K van der Tuuk Department of Obstetrics and Gynaecology, University of Groningen, University Medical Centre Groningen, Groningen, The Netherlands

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B De Bie Endometriosis Foundation of the Netherlands (Endometriose Stichting), Sittard, The Netherlands

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H Groen Department of Epidemiology, University of Groningen, University Medical Centre Groningen, Groningen, The Netherlands

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M E van den Akker-van Marle Department of Biomedical Data Sciences, Leiden University Medical Centre, Leiden, The Netherlands

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A W Nap Department of Obstetrics and Gynaecology, Radboud University Medical Centre, Nijmegen, The Netherlands

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J W M Maas Department of Gynaecology and Grow-school of Oncology and Reproduction, Maastricht University, Maastricht, The Netherlands

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F W Jansen Department of Gynaecology, Leiden University Medical Centre, Leiden, The Netherlands

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A R H Twijnstra Department of Gynaecology, Leiden University Medical Centre, Leiden, The Netherlands

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M D Blikkendaal Department of Gynaecology, Leiden University Medical Centre, Leiden, The Netherlands
Nederlandse Endometriose Kliniek, Reinier de Graaf Gasthuis, Delft, The Netherlands

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Currently, the optimal treatment to increase the chance of pregnancy and live births in patients with colorectal endometriosis and subfertility is unknown. Evidence suggests that that both surgery and in vitro fertilisation (IVF) or intracytoplasmic sperm injection (ICSI) are effective in improving the live birth rate (LBR) among these women. However, the available evidence is of low quality, reports highly heterogeneous results, lacks direct comparison between both treatment options, and does not assess whether a combination strategy results in a higher LBR compared to IVF/ICSI-only treatment. Additionally, the optimal timing of surgery within the treatment trajectory remains unclear. The primary objective of the TOSCA study is to assess the effectiveness of surgical treatment (potentially combined with IVF/ICSI) compared to IVF-/ICSI-only treatment to increase the chance of an ongoing pregnancy resulting in a live birth in patients with colorectal endometriosis and subfertility, measured by cumulative LBR. Secondary objectives are to assess and compare quality of life and cost-effectiveness in both groups. Patients will be followed for 40 months after inclusion or until live birth. The TOSCA study is expected to be completed in 6 years.

Trial registration number

The TOSCA trial is registered as ‘Cost-Effectiveness of Surgical Excision of Colorectal Endometriosis Compared to ART Treatment Trajectory (TOSCA)’ in the Clinical Trials Register (NCT No. NCT05677269, https://clinicaltrials.gov/ct2/show/NCT05677269)

Date of first patient enrolment

The first patient was included in February 2023.

Lay summary

Treating bowel endometriosis in people with fertility problems is difficult, and at the moment, there is no consensus on the best way to increase the chances of pregnancy. This makes it hard for gynaecologists to advise people when to have either IVF/ICSI or surgery, particularly in patients with fewer pain symptoms, as the benefits of surgery to enhance fertility have to be balanced against the potential risk of side effects. Surgery can improve fertility and pain symptoms, but it may delay people trying to conceive which means the reserve of eggs in the ovaries will reduce with time. IVF/ICSI also seems a viable option, but having the surgery first may increase the chances of conception (both naturally and/or after IVF/ICSI). The TOSCA study aims to determine whether surgery for bowel endometriosis leads to an increased birth rate and better patient reported outcome measures compared to IVF/ICSI alone.

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Maria Handzhiyska Department of Research, Nadezhda Women’s Health Hospital, Sofia, Bulgaria

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Rumiana Ganeva Department of Research, Nadezhda Women’s Health Hospital, Sofia, Bulgaria

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Dimitar Parvanov Department of Research, Nadezhda Women’s Health Hospital, Sofia, Bulgaria

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Margarita Ruseva Department of Research, Nadezhda Women’s Health Hospital, Sofia, Bulgaria

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Petar Eftimov Department of Cell and Developmental Biology, Faculty of Biology, SU St. Climent Ohridski, Sofia, Bulgaria

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Vilyana Georgieva Department of Andrology, Nadezhda Women’s Health Hospital, Sofia, Bulgaria

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Denitsa Velikova Department of Andrology, Nadezhda Women’s Health Hospital, Sofia, Bulgaria

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Georgi Stamenov Department of Obstetrics and Gynecology, Nadezhda Women’s Health Hospital, Sofia, Bulgaria

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The objective of this study was to compare the motility, morphology, and levels of DNA fragmentation of spermatozoa subjected to conventional swim-up or cumulus matrix (CM) sperm selection. Semen samples were collected from 60 normozoospermic men at a private hospital between December 2021 and March 2022. After liquefaction, semen samples were separated into two portions – one part was subjected to conventional swim-up preparation, and the remaining spermatozoa were subjected to CM selection. The CM was obtained by mechanical isolation from healthy donor oocytes. Semen analysis and evaluation of sperm were performed according to the WHO 6th Edition Laboratory Manual and Kruger’s strict criteria, respectively. Sperm DNA fragmentation (SDF, %) of the two preparations was evaluated using the Halosperm G2 detection Kit (Halotech, Madrid, Spain). Wilcoxon rank-sum test was used to compare the characteristics of spermatozoa obtained by the two preparations. Spermatozoa selected by CM showed significantly better rapidly progressive motility (43.5% vs 30.6%, respectively, P < 0.001), a higher percentage of morphologically normal forms (14.0% vs 9.0%, respectively, P < 0.05), and lower levels of SDF (26.0% vs 45.0%, P < 0.05) compared to those prepared by conventional swim-up. Moreover, the incidence of multiple sperm defects was considerably lower in the samples that underwent CM selection compared to those that did not (30.0% vs 49.0%, respectively, P < 0.05).The selection by CM significantly increases sperm motility and reduces morphologically abnormal spermatozoa and DNA fragmentation rates compared to the conventional swim-up preparation. The application of this selection technique may increase the chances of successful IVF outcomes.

Lay summary

There are various techniques for selecting high-quality sperm with better shape, mobility, and DNA quality. However, the success of assisted reproduction techniques remains relatively unchanged. In this study, we describe an innovative method that uses the ingredients of a natural coat surrounding the egg (cumulus matrix) to enhance sperm selection procedures. Using this cumulus matrix as a barrier through which sperm cells pass, we mimic natural sperm–egg interactions and are able to select sperm with better characteristics compared to conventional methods. This new sperm selection procedure could lead to increased assisted reproduction success rates.

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Caitriona Brennan Department of Pediatrics, University of California San Diego, La Jolla, California, USA
Division of Biological Sciences, University of California San Diego, La Jolla, California, USA

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Kristina Chan Department of Pediatrics, University of California San Diego, La Jolla, California, USA
Department of Bioengineering, University of California, San Diego, La Jolla, California, USA

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Tanya Kumar Medical Scientist Training Program, University of California San Diego, La Jolla, California, USA

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Erica Maissy Division of Gastroenterology, University of California San Diego, La Jolla, California, USA
Biomedical Sciences Graduate Program, University of California San Diego, La Jolla, California, USA

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Linda Brubaker Department of Obstetrics, Gynecology and Reproductive Sciences, University of California San Diego, La Jolla, California, USA

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Marisol I Dothard Department of Pediatrics, University of California San Diego, La Jolla, California, USA
Biomedical Sciences Graduate Program, University of California San Diego, La Jolla, California, USA

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Jack A Gilbert Department of Pediatrics, University of California San Diego, La Jolla, California, USA
Center for Microbiome Innovation, University of California San Diego, La Jolla, California, USA

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Katharine E Gilbert Department of Pediatrics, University of California San Diego, La Jolla, California, USA

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Amanda L Lewis Department of Obstetrics, Gynecology and Reproductive Sciences, University of California San Diego, La Jolla, California, USA

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Varykina G Thackray Department of Obstetrics, Gynecology and Reproductive Sciences, University of California San Diego, La Jolla, California, USA
Center for Microbiome Innovation, University of California San Diego, La Jolla, California, USA

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Amir Zarrinpar Department of Bioengineering, University of California, San Diego, La Jolla, California, USA
Medical Scientist Training Program, University of California San Diego, La Jolla, California, USA
Division of Gastroenterology, University of California San Diego, La Jolla, California, USA
Department of Obstetrics, Gynecology and Reproductive Sciences, University of California San Diego, La Jolla, California, USA
Center for Microbiome Innovation, University of California San Diego, La Jolla, California, USA
Jennifer Moreno Department of Veterans Affairs Medical Center, La Jolla, California, USA
Institute of Diabetes and Metabolic Health, University of California San Diego, La Jolla, California, USA

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Rob Knight Department of Pediatrics, University of California San Diego, La Jolla, California, USA
Department of Bioengineering, University of California, San Diego, La Jolla, California, USA
Center for Microbiome Innovation, University of California San Diego, La Jolla, California, USA
Department of Computer Science and Engineering, University of California, San Diego, La Jolla, California, USA
Halıcıoğlu Data Science Institute, University of California San Diego, La Jolla, California, USA

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Graphical abstract

Abstract

Although numerous studies have demonstrated the impact of microbiome manipulation on human health, research on the microbiome’s influence on female health remains relatively limited despite substantial disease burden. In light of this, we present a selected review of clinical trials and preclinical studies targeting both the vaginal and gut microbiomes for the prevention or treatment of various gynecologic conditions. Specifically, we explore studies that leverage microbiota transplants, probiotics, prebiotics, diet modifications, and engineered microbial strains. A healthy vaginal microbiome for females of reproductive age consists of lactic acid-producing bacteria predominantly of the Lactobacillus genus, which serves as a protective barrier against pathogens and maintains a balanced ecosystem. The gut microbiota’s production of short-chain fatty acids, metabolism of primary bile acids, and modulation of sex steroid levels have significant implications for the interplay between host and microbes throughout the body, ultimately impacting reproductive health. By harnessing interventions that modulate both the vaginal and gut microbiomes, it becomes possible to not only maintain homeostasis but also mitigate pathological conditions. While the field is still working toward making broad clinical recommendations, the current studies demonstrate that manipulating the microbiome holds great potential for addressing diverse gynecologic conditions.

Lay summary

Manipulating the microbiome has recently entered popular culture, with various diets thought to aid the microbes that live within us. These microbes live in different locations of our body and accordingly help us digest food, modulate our immune system, and influence reproductive health. The role of the microbes living in and influencing the female reproductive tract remains understudied despite known roles in common conditions such as vulvovaginal candidiasis (affecting 75% of females in their lifetime), bacterial vaginosis (25% of females in their lifetime), cervical HPV infection (80% of females in their lifetime), endometriosis (6–10% of females of reproductive age), and polycystic ovary syndrome (10–12% of females of reproductive age). Here, we review four different approaches used to manipulate the female reproductive tract and gastrointestinal system microbiomes: microbiota transplants, probiotics, prebiotics, and dietary interventions, and the use of engineered microbial strains. In doing so, we aim to stimulate discussion on new ways to understand and treat female reproductive health conditions.

Open access
Kaltrina Krasniqi Division of Biomedical Sciences, Warwick Medical School, University of Warwick, Coventry, UK

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Naomi Black Division of Biomedical Sciences, Warwick Medical School, University of Warwick, Coventry, UK
University Hospitals Coventry and Warwickshire, Coventry, UK

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Erin J Williams MRC Centre for Reproductive Health & The Roslin Institute, University of Edinburgh, College of Medicine and Veterinary Medicine, Edinburgh, UK

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Osvaldo Bogado Pascottini Department of Internal Medicine, Reproduction and Population Medicine, Faculty of Veterinary Medicine, Ghent University, Merelbeke, Belgium

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Sarah Thornton Hook Norton Veterinary Group, White Hill Surgery, Hook Norton, UK

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Siobhan Quenby Division of Biomedical Sciences, Warwick Medical School, University of Warwick, Coventry, UK
University Hospitals Coventry and Warwickshire, Coventry, UK

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Joshua Odendaal Division of Biomedical Sciences, Warwick Medical School, University of Warwick, Coventry, UK
University Hospitals Coventry and Warwickshire, Coventry, UK

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Chronic endometritis (CE) in humans is asymptomatic inflammation of the endometrium, associated with poor reproductive outcomes. Similarly, asymptomatic endometrial inflammation in cows, termed subclinical endometritis (SCE), is associated with adverse reproductive outcomes. While the pathophysiology and treatment options for CE in humans remain poorly defined, the well-known financial implications of SCE in dairy cows have attracted intensive research. We performed a systematic review to determine potential areas of interest in human CE research, by analysing emergent themes that arose in studies of SCE in cows. A literature search for studies of subclinical endometritis in cows published between 1990 and November 2021 was performed across Embase, Medline, Scopus and CINAHL. Studies of symptomatic or clinical endometritis were excluded. A thematic analysis across two broad themes was explored: i) diagnostic methods of SCE and ii) pathophysiology of SCE. In total, 51 bovine studies were included. Twelve studies reported on diagnostic methodology. The primary emergent theme was the use of cytology for the diagnosis of SCE. Cytological analysis has a lower sensitivity than histopathology but is less invasive and more specific than alternative techniques such as ultrasound, vaginoscopy or metabolic markers. The subthemes related to pathophysiology were identified as the type of endometritis, metabolic stress, artificial insemination, infective causes and altered cellular pathways. Despite the lack of symptoms, cellular pathways of inflammation including NF-κB, MAPK and inflammasomes were found to be activated. The key themes related to the diagnosis and pathophysiology of SCE in cows identified in this systematic review highlight potential areas for future research into human CE.

Lay summary

Long-term or chronic endometritis (CE) is a condition associated with inflammation in the womb lining. People with CE commonly experience recurrent miscarriages and subfertility. The cause of CE is poorly understood, and as such there are no specific treatments. Comparatively, a form of CE (i.e. subclinical endometritis (SCE)) has been extensively researched in dairy cows due to its financial impact. A systematic review of cow studies was carried out and key themes around cause and diagnosis of SCE in cows were identified and analysed. In total, 44 studies were included. Six main themes around the way SCE is diagnosed were found, and examining cells (i.e. cytology) was found to be more sensitive and practical than other techniques. Six themes were also found for causes of SCE, notably difficult delivery, metabolic stress and infection. This study shows potential areas for future research into human SCE and provides insight into the causes of disease within humans.

Open access
Michael L Power Center for Species Survival, Smithsonian’s National Zoo and Conservation Biology Institute, Washington, District of Columbia, USA

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Carly R Muletz-Wolz Center for Conservation Genomics, Smithsonian’s National Zoo and Conservation Biology Institute, Washington, District of Columbia, USA

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Sally L Bornbusch Center for Conservation Genomics, Smithsonian’s National Zoo and Conservation Biology Institute, Washington, District of Columbia, USA
Department of Nutrition Science, Smithsonian’s National Zoo and Conservation Biology Institute, Washington, District of Columbia, USA

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Graphical abstract

Abstract

Milk is an ancient, fundamental mammalian adaptation that provides nutrition and biochemical communication to offspring. Microbiomes have been detected in milk of all species studied to date. In this review, we discuss: (a) routes by which microbes may enter milk; (b) evidence for proposed milk microbiome adaptive functions; (c) variation in milk microbiomes across mammals; and (d) future research directions, including suggestions for how to address outstanding questions on the viability and functionality of milk microbiomes. Milk microbes may be sourced from the maternal gastrointestinal tract, oral, skin, and mammary gland microbiomes and from neonatal oral and skin microbiomes. Given the variety of microbial sources, stochastic processes strongly influence milk microbiome assembly, but milk microbiomes appear to be influenced by maternal evolutionary history, diet, environment, and milk nutrients. Milk microbes have been proposed to colonize the neonatal intestinal tract and produce gene and metabolic products that influence physiology, metabolism, and immune system development. Limited epidemiological data indicate that early-life exposure to milk microbes can result in positive, long-term health outcomes. Milk microbiomes can be modified by dietary changes including providing the mother with probiotics and prebiotics. Milk replacers (i.e. infant formula) may benefit from supplementation with probiotics and prebiotics, but data are lacking on probiotics’ usefulness, and supplementation should be evidence based. Overall, milk microbiome literature outside of human and model systems is scarce. We highlight the need for mechanistic studies in model species paired with comparative studies across mammals to further our understanding of mammalian milk microbiome evolution. A broader study of milk microbiomes has the potential to inform animal care with relevance to ex situ endangered species.

Lay summary

Milk is an ancient adaptation that supports the growth and development of mammalian neonates and infants. Beyond its fundamental nutritional function, milk influences all aspects of neonatal development, especially immune function. All kinds of milks so far studied have contained a milk microbiome. In this review, we focus on what is known about the collection of bacterial members found in milk microbiomes. Milk microbiomes include members sourced from maternal and infant microbiomes and they appear to be influenced by maternal evolutionary history, diet, milk nutrients, and environment, as well as by random chance. Once a neonate begins nursing, microbes from milk colonize their gut and produce byproducts that influence their physiology, metabolism, and immune development. Empirical data on milk microbiomes outside of humans and model systems are sparse. Greater study of milk microbiomes across mammals will expand our understanding of mammalian evolution and improve the health of animals under human care.

Open access
Francesca Hearn-Yeates EXPPECT Edinburgh and Centre for Reproductive Health, University of Edinburgh, Institute for Regeneration and Repair, Edinburgh, UK

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Andrew W Horne EXPPECT Edinburgh and Centre for Reproductive Health, University of Edinburgh, Institute for Regeneration and Repair, Edinburgh, UK

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Siobhain M O’Mahony Department of Anatomy and Neuroscience, University College Cork, Cork, Ireland
APC Microbiome Ireland, University College Cork, Cork, Ireland

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Philippa T K Saunders EXPPECT Edinburgh and Centre for Reproductive Health, University of Edinburgh, Institute for Regeneration and Repair, Edinburgh, UK

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Graphical abstract

Abstract

Endometriosis is a chronic inflammatory condition affecting one in ten women and those assigned female at birth, defined by the presence of endometrial-like tissue outside the uterus. It is commonly associated with pain, infertility, and mood disorders, and is often comorbid with other chronic pain conditions, such as irritable bowel syndrome. Recent research has identified a key role for the microbiota–gut–brain axis in health and a range of inflammatory and neurological disorders, prompting an exploration of its potential mechanistic role in endometriosis. Increased awareness of the impact of the gut microbiota within the patient community, combined with the often-detrimental side effects of current therapies, has motivated many to utilise self-management strategies, such as dietary modification and supplements, despite a lack of robust clinical evidence. Current research has characterised the gut microbiota in endometriosis patients and animal models. However, small cohorts and differing methodology have resulted in little consensus on the data. In this narrative review, we summarise research studies that have investigated the role of gut microbiota and their metabolic products in the development and progression of endometriosis lesions, before summarising insights from research into co-morbid conditions and discussing the reported impact of self-management strategies on symptoms of endometriosis. Finally, we suggest ways in which this promising field of research could be expanded to explore the role of specific bacteria, improve access to ‘microbial’ phenotyping, and develop personalised patient advice for reduction of symptoms such as chronic pain and bloating.

Lay Summary

Endometriosis is a chronic condition affecting one in ten women and those assigned female at birth, defined by the presence of tissue, similar to the womb lining, growing outside the womb. Symptoms include pelvic pain, period pain, pain during sex and when going to the toilet, digestive disturbance and bloating, infertility, depression, and anxiety. Standard treatments, including surgery and hormone-altering drugs, often have negative side effects. Many women with endometriosis use self-management strategies to control their symptoms, including changing their diet or taking supplements. Although some reports suggest such strategies are helpful, there is limited high-quality evidence to support their use. Here, we discuss how dietary adaptations could be impacting endometriosis-associated symptoms via changes to the bacteria within the gut. Gut bacteria communicate with the brain and influence inflammation throughout the body. Therefore, altering the gut bacteria through dietary changes can potentially benefit a variety of endometriosis-associated symptoms.

Open access
Ibrahim Banaru Abubakar Department of Family Medicine, Ahmadu Bello University Teaching Hospital, Zaria, Nigeria

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Hafsat Banaru Abubakar Department of Family Medicine, Abubakar Tafawa Balewa University Teaching Hospital, Bauchi, Nigeria

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Nigeria has the largest population in Africa, a high fertility rate, and unmet needs for family planning. Family planning is a key strategy for sustainable development. A good knowledge of factors that determine contraceptive uptake is imperative for policy formulation. A nationally representative secondary dataset of 41,821 women aged 15–49 years who participated in the 2018 Nigeria Demographic and Health Survey was analyzed. Multivariate logistic regression was used to examine the association between various factors and the current use of modern contraceptives. The respondents’ average age was 35.9 ± 7.9 years. Overall, contraceptive prevalence was 16.6% for traditional methods and 12.2% for modern methods. Predictors of an increase in modern contraception use were age 40–44 (aOR = 1.07, 95% CI: 0.75–1.53); being a working-class woman (aOR = 1.15, 95% CI: 0.99–1.33); living in an urban area (aOR = 1.14, 95% CI: 0.97–1.33); living in the South West (aOR = 1.36, 95% CI: 1.03–1.79); increasing wealth (aOR = 0.78, 95% CI: 0.66–0.93); and health insurance (aOR = 1.22, 95% CI: 0.89–1.68). Couple dynamics influencing modern contraceptive use were joint decision (aOR = 2.16, 95% CI: 1.81–2.59), self-decision on health care (aOR = 1.34, 95% CI: 1.06–1.70), and earning more than a partner (aOR = 1.14, 95% CI: 0.78–1.66). There are significant variations in contraceptive uptake attributable to socioeconomic and political inequalities, requiring a holistic approach to mitigate barriers and improve contraceptive uptake.

Lay summary

This study examined modern contraceptive use among 41,821 Nigerian women aged 15–49 using data from the 2018 Nigeria Demographic and Health Survey. The average age of the participants was 36 years. The findings showed that 12.2% of women used modern contraceptive methods, while 16.6% used traditional methods. Factors influencing modern contraceptive use included being aged 40–44, being employed, living in urban areas, residing in the South West region, having higher wealth, and having health insurance. Couple dynamics also played a role, with joint decision-making, self-decision on health care, and higher earnings than a partner being associated with increased contraceptive use. The study highlights the importance of addressing socioeconomic and political disparities to improve access to and use of contraceptives for Nigerian women, ultimately contributing to sustainable development.

Open access

Oogonial stem cells: the unexpected superheroes

The time has come for stem cell technologies to be used in fertility studies

Rita L Sousa Gamete Research Centre, Department of Veterinary Sciences, University of Antwerp, Antwerp, Belgium

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Shiuli Bhattacharyya UCL, Department of Medical School, London, UK

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The rights of transgender and intersex people have become a contentious issue in our current political climate. Whether it be the rights of intersex athletes such as Caster Semenya (who identifies as a woman) to compete in elite sport, or the rights of transgender women to use women’s only spaces, there is an increasingly fierce debate as to the legitimacy of people’s gender and sexual identities and what parameters should be used to define them. A common argument accepted by most in our society is that while gender may be a spectrum, sex is an inalienable binary.

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