Clinical research and reviews
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This study examined the status of oxidative stress in 599 couples undertaking in vitro fertilization (IVF) treatment and its association with reproductive hormones, smoking, and outcomes. Oxidative stress biomarkers such as malondialdehyde, 8-hydroxy-2-deoxyguanosine, hydrogen peroxide (H2O2), catalase (CAT), and total antioxidant capacity (TAC) were determined in follicular fluid and seminal plasma. Tail moment (TM) was used to evaluate DNA damage in the sperm and granulosa cells. Reproductive hormones in serum and cotinine (COT) in urine, follicular fluid, and seminal plasma samples were determined. Separate multivariate linear regression was used to assess associations between levels of each oxidative stress biomarker and each hormone and smoking parameter (modeled as natural log-transformed). The findings indicate that some oxidative stress and DNA damage biomarkers played a role in disrupting certain reproductive hormones in women and their male partners either by overproducing reactive oxygen species or reducing antioxidant defense capacity. Although women were nonsmokers, COT levels > 50 and 10 µg/L in urine and follicular were observed in 5.7 and 1.7%, respectively. Levels of follicular fluid COT were positively associated with H2O2 and TM. We used log-binomial multivariate regression to estimate relative risks for the association between oxidative stress/DNA damage and IVF binary outcomes (fertilization rate > 50%, biochemical pregnancy, clinical pregnancy, and live birth). An increase in the CAT levels of follicular fluid was associated with a 48 and 41% decrease in the risk of poor fertilization rate (≤50%) and unsuccessful live birth, respectively. After the models were adjusted for hormonal factors, the associations remained the same, except that the elevated TAC in follicular fluid became significantly associated with a decrease of 42% in the risk of poor fertilization rate (≤50%). The higher antioxidant activity (CAT and TAC) in follicular fluid might positively impact specific IVF outcomes.
Lay summary
Oxidative stress occurs when antioxidant molecules are insufficient in the body to destroy free radicals that can damage the cells, proteins and DNA, causing different health conditions, including infertility. The role of oxidative stress in female infertility has not received as much attention as male infertility, and research is still limited. This study explored whether the overproduction of free radicals can impact the success of in vitro fertilization (IVF) treatment using several biological markers such as hydrogen peroxide, catalase, and total antioxidant capacity. Our findings revealed that the high antioxidant levels in the fluid surrounding the egg were linked with a high fertilization rate. Additionally, oxidative stress status in couples was associated negatively with several reproductive hormones and smoking status. Biomarkers of oxidative stress and DNA damage might have potential applications in evaluating IVF patients’ clinical characteristics such as causes of infertility, hormonal profile, fertilization rate, implantation and live birth.
Search for other papers by Camila N Ortiz in
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Department of Internal Medicine, Ponce Health Sciences University, Ponce, Puerto Rico, USA
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Endometriosis is a complex disease characterized by inflammation and the growth of endometrial- like glands and stroma outside the uterine cavity. The pathophysiology of endometriosis is not entirely understood, however, with a prevalence of ~10% of women in their reproductive years, the disease symptoms significantly affect the quality of life of millions of women globally. Metabolomic studies have previously identified specific metabolites that could be a signature of endometriosis. This approach could potentially be used as a non-invasive tool for early diagnosis and provide a better understanding of endometriosis pathophysiology. This review aims to provide insight as to how endometriosis affects the metabolome by reviewing different studies that have used this approach to design follow-up studies. The search query included the term 'endometriosis' in combination with 'metabolomics', 'lipidomics', or 'sphingolipidomics' published between 2012 and 2020. We included studies in humans and animal models. Most studies reported differences in the metabolome of subjects with endometriosis in comparison to healthy controls and used samples taken from serum, endometrial tissue, follicular fluid, urine, peritoneal fluid, or endometrial fluid. Statistically significant metabolites contributed to group separation between patients and healthy controls. Reported metabolites included amino acids, lipids, organic acids, and other organic compounds. Differences in methods, analytical techniques, and the presence of confounding factors can interfere with results and interpretation of data. Metabolomics seems to be a promising tool for identifying significant metabolites in patients with endometriosis. Nonetheless, more investigation is needed in order to understand the significance of the study results.
Lay summary
Endometriosis is a chronic disease affecting the quality of life in one out of every ten women during their reproductive years, causing pain and infertility. It is characterized by inflammation and growth of tissue like the endometrium (uterus lining) outside the uterine cavity. Studies have searched for a predictor of endometriosis-associated changes by observing small molecules necessary for metabolism on a large scale (metabolomics). Metabolomics could serve to resolve one of the biggest challenges that patients with endometriosis face: a delay in diagnosis. In this review, the authors summarize identified potential biomarkers from various bodily fluids and tissues that are characteristic of metabolic processes observed in endometriosis. Biomarkers include cell growth, cell survival, high energy demand, oxidative stress, and fatty acid levels. A metabolomics approach offers promise as a non-invasive tool to identify significant metabolite changes in patients with endometriosis, potentially leading to earlier diagnoses and new opportunities for back-translational strategies.
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MRC Centre for Reproductive Health, Queen’s Medical Research Institute, University of Edinburgh, Edinburgh, UK
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Endometriosis is a chronic neuroinflammatory pain condition affecting ~180 million women worldwide. Surgical removal or hormonal suppression of endometriosis lesions only relieves pain symptoms in some women and symptomatic relapse following treatment is common. Identifying factors that contribute to pain is key to developing new therapies. We collected peritoneal fluid samples and clinical data from a cohort of women receiving diagnostic laparoscopy for suspected endometriosis (n = 52). Peritoneal fluid immune cells were analysed by flow cytometry and data compared with pain scores determined using the pain domain of the Endometriosis Health Profile Questionnaire (EHP-30) in order to investigate the association between peritoneal immune cells and pain symptoms. Pain scores were not different between women with or without endometriosis, nor did they differ according to disease stage; consistent with a poor association between disease presentation and pain symptoms. However, linear regression and correlation analysis demonstrated that peritoneal macrophage abundance correlated with the severity of pelvic pain. CD14high peritoneal macrophages negatively correlated with pain scores whereas CD14low peritoneal macrophages were positively correlated, independent of diagnostic outcome at laparoscopy. Stratification by pain subtype, rather than endometriosis diagnosis, resulted in the most robust correlation between pain and macrophage adundance. Pain score strongly correlated with CD14high (P = 0.007) and CD14low (P = 0.008) macrophages in patients with non-menstrual pain and also in patients who reported dysmennorhea (CD14high P = 0.021, CD14low P = 0.019) or dysparunia (CD14high P = 0.027, CD14low P = 0.031). These results provide new insight into the association between peritoneal macrophages and pelvic pain which may aid the identification of future therapeutic targets.
Lay summary
Endometriosis is a common condition where cells similar to those that line the womb are found elsewhere in the body. It is associated with inflammation and pain in the pelvis and affects ~180 million women worldwide. Current treatments are not effective for all patients and we, therefore, need to understand what causes pain in order to develop new treatments. We investigated the types of immune cells present within the pelvis of women undergoing investigation for suspected endometriosis. Disease diagnosis and stage (I–IV) was recorded along with pain score determined by questionnaire. We characterised the immune cells present and compared them to disease stage and pain score. We found that pelvic pain was linked to the abundance of immune cells but, surprisingly, not to disease stage. These findings suggest that immune cells are closely associated with pain severity in endometriosis and may be good targets for future endometriosis treatments.
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Recently, fertility services have started resuming since COVID-19 was declared a pandemic, but there remains significant uncertainty in the way this care will be delivered in the United Kingdom. The objective of our study was to explore the impact of COVID-19 on individuals using fertility services in the United Kingdom. The study was conducted in two phases between May 2020 and July 2020: an online questionnaire involving 1212 participants and subsequent individual semi-structured telephone interviews with 15 participants. Through thematic analysis, we learned from the questionnaire findings that 74% of individuals identified as White British, 21% as Black and Minority Ethnic (BAME) and 2.6% as male. Ninety-six per cent of individuals from the questionnaire explained that COVID-19 had a ‘negative impact’ on their fertility treatment, namely ‘delay in care’. Eighty-two per cent of participants discussed concerns about the ‘uncertainty’ they felt about fertility services; these included the ‘unknown impact of COVID-19 on pregnancy outcomes’, the ‘unknown impact on general gynaecology services’ and the ‘unknown impact of COVID-19 on fertility success’. Through semi-structured telephone interviews with 15 participants, we learned about the ‘cultural pressures’ individuals from BAME backgrounds faced in relation to care. Participants were mindful about the ‘pressures on the service’ when reopening, and therefore ‘advancing maternal age’, ‘socio-economic background’ and ‘previous unsuccessful fertility treatment’ were the main factors individuals considered important when ‘prioritising’ fertility care. Our findings can be used by fertility service providers to appreciate the patient perspective when considering the reopening of fertility services nationally and internationally.
Lay summary
The impact of COVID-19 on patients seeking or undergoing fertility treatment is not entirely known. Many patients have had their treatment postponed during the pandemic. As fertility services begin to recommence, it is important to understand how the pandemic has affected this group of patients. In addition, it is vital to appreciate and understand the patient’s voice in order to ensure services take into account the patients’ concerns as they begin to offer certain fertility treatments. Our study was conducted in two phases and involved an online questionnaire and individual interviews with people. We found that people were worried about services restarting and how care would be prioritised. People also discussed some of the perceived barriers to seeking fertility healthcare. Our findings highlight the importance of understanding the patient’s voice when recommencing fertility services.
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Today periodontal health is considered as an integral part of systemic health itself and no longer as a single factor. The literature recognizes that the presence of periodontal disease can represent a risk factor for numerous systemic conditions such as heart disease and diabetes. In recent years, we have witnessed a progressive interest regarding the influence exerted by this condition on reproduction, as well as the possible repercussions on conception possibilities. Upon analyzing a limited number of studies available for the correlation between periodontal disease and female infertility, it could be inferred that this condition can be equated to the presence of a real outbreak of infection and therefore exert its influence, not only through bacterial translocation in the bloodstream, causing the systemic dissemination of pathogens, but also through the production of cytokines and immunoglobulins by inflammatory mediators. This situation limits bacterial growth, but it could cause damage to the fetus, to the reproductive system, and could hinder conception attempts. Although further research is needed to better clarify the mechanism underlying the possible correlation between periodontal disease and female infertility, the present article aims to review all the available literature on this topic.
Lay summary
In recent years, interest regarding the influence of gum disease on conception has increased. Since serious gum disease (periodontitis) can be compared to an outbreak of infection, studies suggest that the bacteria that mediate inflammation do not remain confined only to the gum tissue, but can enter the bloodstream and spread, thus spreading the infection and having a whole-body effect. This situation could cause damage to the developing baby, to the reproductive system and could hinder conception attempts. Constant maintenance of oral health is definitely necessary. It is important for the professionals involved (gynecologists, obstetricians, dentists, etc.) to communicate and collaborate on these issues. Dentists could advise on the correct hygienic maintenance not only to pregnant women, but also to those who are planning a pregnancy in order to avoid the occurrence of unfavorable conditions.
Obstetrics and Gynecology, Showa University, Shinagawa-ku, Tokyo, Japan
Fertility Clinic Tokyo, Shibuya-ku, Tokyo, Japan
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Abstract
Purpose
Following reports of an increase in implantation and pregnancy continuation rates by a higher percentage of Lactobacillus in the intrauterine microbiota, it has received attention in infertility treatment. This study aimed to examine Japanese women for intrauterine microbiota.
Methods
The clinical background factors in women that influence the abundance of Lactobacillus in the bacterial microbiota were examined. We included 147 patients (31 and 116 in the follicular and luteal phase, respectively), from June 2018 to June 2020, who underwent their first intrauterine microbiota test and had not used antibiotics for at least 4 weeks before the test. In the luteal phase, we compared the background factors of women in cases with 90% or more and less than 90% of Lactobacillus. Differences in the intrauterine microbiota were examined during the follicular and luteal phases.
Results
The proportion of Lactobacillus tended to be low among women aged 36 years and older with a history of childbirth (P = 0.0631). Some bacteria were only detected during the follicular and luteal phases, and the bacterial microbiota may change during the menstrual cycle.
Conclusion
Bacterial microbiota in the uterus may differ between the follicular and luteal phases. Furthermore, it was shown that the rate of Lactobacillus may be lower in women (older than 36 years) who had given birth, indicating that intrauterine microbiological testing may be considered for these women in clinical practice.
Lay summary
Good implantation and pregnancy continuation rates have been reported when the proportion of the bacteria Lactobacillus is high in the uterus (intrauterine) bacterial population (microbiota). In this study, we assessed whether the clinical background of Japanese women (age, history of pregnancy and childbirth, and presence of gynecological or hormonal disorders) affect the proportion of intrauterine microbiota. Intrauterine samples were collected and sequenced to evaluate the intrauterine microbiota and the composition ratio of each bacterium. Comparing the percentage of Lactobacillus in the latter phase of the menstrual cycle with the clinical background, it was found that the percentage tended to be lower in women with a history of childbirth. We compared the intrauterine microbiota between the first phase and latter phase of the menstrual cycle and revealed that it may differ between the two phases. Advances in the development of criteria for assessing intrauterine microbiota are expected.
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The role that lifestyle factors play in fertility issues has generated some amount of interest and questions among stakeholders. This review aims to highlight the impact of lifestyle behaviors on the fertility potential of an individual and what can be done to prevent or improve reproductive outcomes. Relevant published articles on the effect of lifestyle behaviors were obtained from Medline, Pubmed and Google scholar search engines for the study. The review of the literature indicates a negative impact of modifiable lifestyle factors such as fat-rich diets, delayed childbearing/age of starting family, smoking, alcohol misuse, sexual behavior, anxiety/depression and perception/beliefs were associated with fertility. The ensuing stress precipitates social behaviors such as excessive alcohol and caffeine consumption, tobacco smoking, misuse of recreational drugs/medications, which increases the risk of sexually transmitted diseases and infection leading to infertility. Practical recommendations to modify lifestyle behaviors and the impact of misconception of Assisted Reproductive Technology in the treatment of infertility are discussed. The need to make appropriate behavioral changes to stem the tide of infertility in Nigeria is imperative. More reproductive health education is needed to create the necessary awareness of the etiologies of infertility and the importance of in vitro fertilization treatment as a means of conceiving ‘natural’ babies is suggested.
Lay summary
Scientific evidence has suggested that modifiable lifestyle factors (consumption fat-rich diets, delayed childbearing/age of starting family, smoking, alcohol misuse, sexual behavior, anxiety/depression and perception/beliefs) play important roles in the general health and wellbeing of individuals including fertility. Evidence exists of an association between lifestyle behaviors and infertility in both men and women. Understanding the various processes through which modifiable lifestyle behaviors impair fertility will help to assist in the management of affected individuals. We conducted a comprehensive review of published studies to assess how lifestyle factors inhibit fertility and practical ways to ameliorate them. This review also deals with the misconception of Assisted Reproductive Technology in the treatment of infertility. The need to make appropriate behavioral changes to stem the tide of infertility in Nigeria is imperative. More reproductive health education is needed to create the necessary awareness of the causes of infertility and the importance of in vitro fertilization in the treatment of infertility.
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Altered gut microbiota (dysbiosis), inflammation and weight gain are pivotal to the success of normal pregnancy. These are features of metabolic syndrome that ordinarily increase the risk of type 2 diabetes in non-pregnant individuals. Though gut microbiota influences host energy metabolism and homeostasis, the outcome (healthy or unhealthy) varies depending on pregnancy status. In a healthy pregnancy, the gut microbiota is altered to promote metabolic and immunological changes beneficial to the mother and foetus but could connote a disease state in non-pregnant individuals. During the later stages of gestation, metabolic syndrome-like features, that is, obesity-related gut dysbiotic microbiota, increased insulin resistance, and elevated pro-inflammatory cytokines, promote energy storage in adipose tissue for rapid foetal growth and development, and in preparation for energy-consuming processes such as parturition and lactation. The origin of this gestation-associated host–microbial interaction is still elusive. Therefore, this review critically examined the host–microbial interactions in the gastrointestinal tract of pregnant women at late gestation (third trimester) that shift host metabolism in favour of a diabetogenic or metabolic syndrome-like phenotype. Whether the diabetogenic effects of such interactions are indeed beneficial to both mother and foetus was also discussed with plausible mechanistic pathways and associations highlighted.
Lay summary
In non-pregnant women, increased blood glucose, fat accumulation, and prolonged immune response lead to obesity and diabetes. However, during the later stages of pregnancy, the changes in the body’s metabolism described previously do not lead to disease, instead pregnancy facilitates the storage of sufficient energy in fat cells for rapid growth and development of the foetus. The excess energy stores also prepares the mother for labour and breastfeeding. This review examines the role of the normal bacteria in the digestive tract in this beneficial energy accumulation and transfer between the mother and foetus without leading to obesity, diabetes and hypertension in pregnancy.
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Fifteen percent of couples are globally estimated to be infertile, with up to half of these cases attributed to male infertility. Reactive oxidative species (ROS) are known to damage sperm leading to impaired quantity and quality. Although not routinely assessed, oxidative stress is a common underlying pathology in infertile men. Antioxidants have been shown to improve semen analysis parameters by reducing ROS and facilitating repair of damage caused by oxidative stress, but it remains unclear whether they improve fertility. Carnitines are naturally occurring antioxidants in mammals and are normally abundant in the epididymal luminal fluid of men. We conducted a systematic review and meta-analysis to evaluate the safety and efficacy of carnitine supplementation for idiopathic male infertility. We searched ClinicalKey, ClinicalTrials.gov, Cochrane Central Register of Controlled Trials (CENTRAL), EMBASE, MEDLINE, PubMed and ScienceDirect for relevant studies published from 1 January 2000 to 30 April 2020. Of the articles retrieved, only eight randomised controlled trials were identified and included. Analysis showed that carnitines significantly improve total sperm motility, progressive sperm motility and sperm morphology, but without effect on sperm concentration. There was no demonstrable effect on clinical pregnancy rate in the five studies that included that outcome, although patient numbers were limited. Therefore, the use of carnitines in male infertility appears to improve some sperm parameters but without evidence of an increase in the chance of natural conception.
Lay summary
Although male infertility affects 1:15 men, there is no obvious reason in the vast majority of cases. Reactive oxidative species (ROS) are highly active molecules containing oxygen and are natural byproducts of normal metabolism. However, high concentrations of ROS have been shown to damage sperm, which negatively impacts a couple’s ability to conceive. Carnitines are natural antioxidants found in the body that counterbalance the damaging effects of ROS. We conducted a comprehensive review of published studies to assess whether carnitine supplements are safe and effective in improving sperm quality and pregnancy rates. Our analysis shows that carnitines improve sperm swimming and production of normal-shaped sperm cells but do not affect sperm count or pregnancy rates, although there are only a few studies and scientific evidence is limited. Whilst it is possible that carnitines may benefit male infertility, more evidence is required regarding chances of pregnancy after carnitine therapy.
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Complete Fertility, Princess Anne Hospital, Southampton, UK
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