Physical activity, obesity and eating habits can influence assisted reproduction outcomes

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Physical activity, obesity and eating habits can influence assisted reproduction outcomes
  517 ISSN  1745-5057 Women's Health  (2010) 6 (4), 517–52410.2217/WHE.10.40 © 2010 Future Medicine Ltd by females can be found on miscarriage, gesta-tional age at delivery and on embryotoxic effect after AR treatment [6] . Furthermore, previous studies indicate that a high caffeine intake by a  women during pregnancy is accompanied by a higher incidence of smoking and higher alcohol consumption [7] . Women who consume high amounts of alco-hol may take longer to fall pregnant [8] , have increased rates of spontaneous miscarriages and worse pregnancy outcomes [9] . In contrast,  women who are wine consumers present a shorter waiting time to pregnancy in comparison to nonwine drinkers [8] . The effects of BMI on AR cycle’s outcomes  were recently reviewed. Although overweight,  women required higher doses of gonadotrophins, and showed lower likelihoods of pregnancy and an increased risk of miscarriage after IVF; the live birth rates are still controversial [10] . The aim of the present study was to evaluate the potential effect of women’s lifestyle (eating habits and physical activity) and obesity on AR treatment outcomes. Materials & methods Experimental design This cohort study included 436 patients under-going their first cycle of intracytoplasmic sperm injection (ICSI) between January 2005 and Lifestyle factors are known to affect fertility in both men and women, and there is increasing interest in investigating such factors. A combi-nation of reduced exercise, changes of dietary composition and increased energy intake have been contributing to a growing worldwide epi-demic of obesity, with serious impacts on several aspects of health [1] .Overweight and obesity are the result of a chronic imbalance between energy intake and energy expenditure, and despite the fact that energy intake has become more caloric, a paral-lel decline in the level of physical activity also exists, contributing to the obesity epidemic [2] . The deleterious effects of obesity on repro-ductive health include menstrual disorders and infertility [3] . Such disorders are probably related to multiple factors such as endocrine and meta-bolic functions, including the balance of sex steroids, insulin and leptin, which, in turn, may directly or indirectly affect ovarian function, fol-licular growth, implantation and development of a clinical pregnancy [4,5] . Although no consensus can be found on pre-vious studies, the consumption of specific food and drinks and some habits can impair repro-ductive outcomes. Alcohol and caffeine intake, as well as tobacco smoking could be important factors in the failure of assisted reproduction (AR). A powerful influence of caffeine intake RESEARCH ARTICLE Physical activity, obesity and eating habits can influence assisted reproduction outcomes Renata Cristina Ferreira 1 , Gabriela Halpern 1 , Rita de Cássia Savio Figueira 1 , Daniela Paes de Almeida Ferreira Braga 1,2 , Assumpto Iaconelli Jr 1,2  & Edson Borges Jr †1,2 Objective:  to determine if eating habits, physical activity and BMI can influence assisted reproduction outcomes. Material and Methods: this study analyzed 436 patients undergoing intracytoplasmic sperm injection cycles. Patients answered a questionnaire and regression analysis examined the relationship between lifestyle and BMI with the intracytoplasmic sperm injection cycles outcomes. Results:  no influence of lifestyle and obesity was observed on the number of oocytes recovered. Obesity reduced the normal fertilization rate (coefficient [Coef.]: -16.0; p = 0.01) and increased the risk of miscarriage (OR: 14.3; p = 0.03). Physical activity positively affected implantation (Coef.: 9.4; p = 0.009), increased the chance of pregnancy (OR: 1.83; p = 0.013) and tended to decrease the risk of miscarriage (OR: 0.30; p = 0.068). In addition, an inverse correlation was found between physical activity and BMI, and a direct correlation was found between soft-drink consumption and BMI. Conclusions:  eating habits, physical activity and obesity could affect clinical outcomes of assisted reproduction. 1 Fertility – Assisted Fertilization Center,  Av. Brigadeiro Luis Antônio, 4545, São Paulo, 01401–002, Brazil  2 Sapientiae Institute – Educational & Research Center on Assisted Reproduction, R. Vieira Maciel, 62. São Paulo, 04503–040, Brazil †  Author for correspondence:Tel.: +55 11 30188181 Fax: +55 11 3018  Keywords • assisted reproduction• eating habits   • ICSI   • intracytoplasmic sperm injection • miscarriage   • obesity   • physical activity   • pregnancy   part of   518 future science group RESEARCH ARTICLE – Ferreira, Halpern, Figueira et al. October 2007, in a private assisted reproduc-tion center. This study was approved by the local Institutional Review Board, and written informed consents were obtained from all patients, in which they agreed to share the outcomes of their ICSI cycles for research purposes. The causes of infertility were male factors (35.6%), ovarian disorders (17.2%), idiopathic cause (13.0%), endometriosis (11.0%), tubal-uter-ine factors (8.0%), polycystic ovarian syndrome (5.0%) and a combination of various other causes (10.2%). The study included couples undergoing controlled ovarian stimulation and ICSI, who had completed the lifestyle questionnaire. The validated lifestyle questionnaire [11] , containing multiple choice questions, was com-pleted by the patients at the start of treatment. The women reported their (i) physical activity practices, and nutritional habits in terms of their consumption of (ii) caffeine-containing soft drinks, (iii) coffee, (iv) alcohol and (v) chocolate. The questionnaire was prepared by a nutritionist and based on the main nutritional habits observed on clinical routine of patients undergoing ICSI cycles in our center. Positive answers to the questionnaire were considered when patients reported: (i) practice of physical activity: at least 1 h of activity three-times a week, (ii) daily consumption of at least one glass of caffeine-containing soft drink, (iii) daily consumption of more than one cup of cof-fee, (iv) consumption of alcohol more than five-times a week, and (v) consumption of chocolate bars more than five-times a week.Patients were considered as obese with a BMI of ≥ 30.0 kg/m 2 , overweight with a BMI of ≥ 25.0 and <30.0 kg/m 2 , or nonoverweight with a BMI of <25.0 kg/m 2 . The outcomes of ICSI cycles  were retrospectively reviewed from the clinical database and correlated to the questionnaire answers regarding lifestyles and obesity. Controlled ovarian stimulation & laboratory procedures  Women were submitted to pituitary down-regulation using a gonadotropin-releasing hor-mone agonist (Lupron Kit™, Abbott S.A Societé Française des Laboratoires, Paris, France) fol-lowed by ovarian stimulation with recombinant follicle-stimulating hormone ([FSH]; Gonal-F ® , Merck Serono, Geneve, Switzerland). Follicular dynamics was followed by ultra-sound and dose adjustments were performed if necessary. When at least one follicle of 18 mm diameter or larger or two follicles of 16mm diameter or larger were observed, recombinant human chorionic gonadotropin (r-hCG) (250 µg; Ovidrel™, Merck Serono, Geneve, Switzerland)  was administered to induce final follicular matu-ration. A total of 35 h after r-hCG administra-tion, oocytes were collected by transvaginal ultra-sound. The recovered oocytes were assessed for their nuclear status, and those in metaphase II (MII) were submitted to ICSI f ollowing routine procedures [12] . Normal fertilization, indicated by the pres-ence of two clearly distinct pronuclei, was assessed 18 h after ICSI (it excludes abnormal fertilizations such as the presence of only one, or more than two pronuclei). Embryo quality  was evaluated under an inverted microscope (Eclipse TE 300; Nikon ® , Tokyo, Japan) and the following parameters were recorded: number and symmetry of blastomeres, fragmentation percentage, presence of multinucleation and defects in the zona pellucida and cytoplasm. One to three high-quality embryos, when available,  were transferred per patient on the second or third day of development. When no high-quality embryos were available the cycle was cancelled.Implantation rate was defined as the number of gestational sacs divided by the number of embryos transferred per patient. Clinical preg-nancy was defined as the presence of a gestational sac with heartbeat visualized by ultrasound 4–6 weeks after embryo transfer. Miscarriage  was considered when spontaneous loss of a p regnancy before 24 weeks’ gestation occurred. Data analysis The ICSI outcomes analyzed in this study  were specifically chosen to engage all aspects of treatment, including the number of oocytes recovered (representing the response to ovarian stimulation), the fertilization and implanta-tion rates (reflecting oocyte and embryo quality respectively), and the clinical outcomes, which included clinical pregnancy and miscarriage. The general characteristics of the groups were expressed as the mean ± standard deviation (SD) for numerical variables, and proportions (%)  were used for categorical variables. Prior to the multivariate analyses, univari-ate analyses were performed to identify which variable would affect the ICSI outcomes. For this analyses the predicted variables were BMI, e ating habits and social habitsMultiple linear or logistic regression analysis  were conducted to assess the influence of obes-ity, eating habits and physical activity on the outcomes of ICSI cycles. Regression analysis  was adjusted for variables considered potential  519 future science group Women's Health  (2010) 6 (4) Physical activity & diet can influence assisted reproduction outcomes – RESEARCH ARTICLE confounders of the association between the factors evaluated and ICSI outcomes (wom-en’s age, dose of FSH administered, number of transferred embryos, cause of infertility for all analyses and endometrium thickness for c linical outcomes analysis).  A Pearson correlation coefficient was also calculated to establish the association between variables.The power test was performed according to the sample size, standard deviation and differ-ence between groups taking into account the implantation rate. The result was higher than 0.8.Results were considered to be significant at the 5% critical   level (p ≤  0.05). Data analysis  was carried out using SPSS   (version 15) s tatistical   software. Results The causes of infertility were equally distributed among the groups (T   ABLE  1) . The general char-acteristics of patients and their classification according to BMI are shown in T   ABLE  2 . Our data demonstrated the influence of age on both BMI (coefficient [Coef.]: 0.107; p = 0.002) and dose of FSH administered (Coef.: 50.15; p < 0.001). Of the patients, five were over 44 years of age. One alternative would be to exclude these patients from the analysis; however, instead all the r egression analyses were maternal-age adjusted.Regarding the patients eating habits, we observed that 31.5% of the patients consume coffee, 17.6% consume caffeine-containing soft drinks, 9.2% consume chocolate and 5.1% con-sume alcohol. On the other hand, 36.3% of the patients practice physical activity. Even though there were no correlations between BMI and coffee (Coef.: = 0.011; p = 0.813), caffeine-con-taining soft drinks (Coef.: = 0.058; p = 0.231), alcohol (Coef.: = -0.051; p = 0.290), or chocolate (Coef.: = -0.010; p = 0.830) consumptions, we observed that patients that practiced physical activity had lower BMI (Pearson correlation: r =-0.118; p = 0.014), and those who consumed caffeine-containing soft drinks had a higher probability for obesity (logistic regression analy-sis: OR: 2.67, CI 95%: 1.0–7.0; p = 0.045). The cycle’s characteristics are shown in T   ABLE  3 .In a further analysis, we evaluated the influence of obesity, eating habits and physical activity on ICSI outcomes. The number of oocytes recovered  was not influenced by any variable included in the model. However, obesity adversely influenced the normal fertilization rate and positively influenced the chance of miscarriage. In addition, physical activity had a positive effect on implantation rate, increasing the chance of pregnancy in nearly 80% of patients, and decreasing the chance of m iscarriage (T   ABLE  4) . Discussion The impact of obesity on the outcomes of AR cycles has been supported by many studies and has also been recently reviewed [10] . Several stud-ies verified an adverse effect of obesity on IVF out-comes [5,13,14] . However, other studies have found no significant differences on clinical pregnancy between obese and nonoverweight women  [15–17] . It is well known that BMI is closely related to lifestyle factors, such as eating habits and physi-cal activity. In this study we aimed to investigate the influences of caffeine, caffeine-containing soft drinks, chocolate and alcohol consump-tions, physical activity and obesity on ICSI cycles outcome.Recent estimates in the USA highlight the prevalence of obesity (overweight or obese) in 61.8% of women   [18] . However, considering the population evaluated in this study, only 22.2% of women were in such categories. The difference between the prevalence of  American and Brazilian or Spanish overweight-obese women is likely due to the different eating Table 1. Distribution of the causes of infertility among the weight groups. Cause of infertilityNormal (%)Overweight (%)Obese (%) Endometriosis 6.5 4.7 7.9Unexplained infertility 12.9 4.7 10.5Male factor 35.1 38.1 36.1Ovarian factor 16.8 4.7 13.1Tubal factor 7.0 14.3 9.2Polycystic ovarian syndrome 4.1 14.3 3.5Associated factors 17.6 19.0 19.7  p > 0.05.  520 future science group RESEARCH ARTICLE – Ferreira, Halpern, Figueira et al. habits. The low percentage of women who con-sumed caffeine-containing soft drinks, chocolate and alcohol in our study supports this hypothesis. In our study, no influence of unhealthy eat-ing habits was observed on clinical outcomes of ICSI cycles. However, patients who consumed caffeine-containing soft drinks had a higher probability of being obese, which supports the relationship of eating habits and obesity.  A recent study demonstrated a marked inter-action between BMI and age, and a significant influence of BMI on oocyte recovery, fertiliza-tion, implantation, pregnancy and live birth rates of IVF cycles [19] . In the present study, no influence of obesity was found on oocyte recovery rates, likely owing to the adjustments p erformed on dose of FSH administered.The relationship between oocyte quality and obesity remains a matter of debate. Attention has been given to the cause of poor fertility outcomes in obese women, seeking to determine whether impaired outcomes are due to an ovarian effect, endometrial effect or a combined effect. While some studies demonstrated that obese women have a higher risk of nonrecurrent miscarriages,  which points to oocyte quality as the main fac-tor for poor reproductive performance [15,20,21] ; others did not find an association between the quality of oocytes and obesity [14,22,23] .In the present study, the relationship between BMI, eating habits and physical activity on the outcomes of ICSI was evaluated. Oocyte dimor-phisms were not evaluated. However, it is well known that intracytoplasmic and extracyto-plasmic anomalies developing during the matu-ration process may lead to fertilization failure [24,25]  and developmental impairment of the embryo despite normal fertilization [24,26,27] .The interaction between obesity and preg-nancy loss is probably not caused by the IVF procedure itself, since obesity also increases the miscarriage rate in ovodonation cycles [13] . In addition, previous studies have shown that obesity is an independent cause of miscarriage in spontaneous pregnancies [21] . The mechanism underlying obesity-related pregnancy loss may involve endocrine and biochemical factors that may affect ovarian function and endometrial receptivity [22,28] .Indeed, a recent study showed that a BMI of >30 is an independent factor for poor pregnancy outcome. Therefore, the evidence of endometrial compromise is evident in obese women [29] .By contrast, in a previous report, 6500 IVF cycles and more than 80,000 oocytes were ana-lyzed. Implantation, pregnancy and live birth rates were significantly lower as BMI increased. In addition, FSH dose was also adjusted and Table 2. General characteristics of patients regarding age, BMI and BMI categories. Mean ±  SDRange General characteristics Maternal age (years)35.3 ±  4.823–48BMI (kg/m 2 )23.0 ±  3.518.0–46.0 BMI categoriesNumber (%)Mean ± SDRange Normal (BMI 18.0–24.5 kg/m 2 )339 (77.8)21.6 ±  1.818.0–24.9Overweight (BMI ≥ 25.0 and <30.0 kg/m 2 )76 (17.4)26.9 ±  1.525.0–29.8Obese (BMI ≥ 30.0 kg/m 2 )21 (4.8)33.0 ±  3.630.1–46.1 Table 3. General characteristics of intracytoplasmic sperm injection cycles. General characteristics Follicle-stimulating hormone (total dose administered [IU])2376.9 ±  691.3Number of follicles aspirated17.7 ±  14.2Number of oocytes recovered11.5 ±  9.0Fertilization rate (%)74.9 ±  7.5Implantation rate (%)20.9 ±  .17.0Pregnancy rate (%)31.4Endometrial thickness (mm)11.8 ±  2.5Number of embryos transferred per patient2.0 ±  0.9  521 future science group Women's Health  (2010) 6 (4) Physical activity & diet can influence assisted reproduction outcomes – RESEARCH ARTICLE no differences appeared in number of retrieved oocytes among the BMI groups, although more FSH was needed in the obese group to obtain this result. Moreover, mean age was similar among BMI groups [30] . A significant poorer outcome was observed in surrogate mothers who received donated ova and nonseverely altered sperm samples when BMI  was higher than 35 [31] . A higher rate of early pregnancy loss in obese  women had been described [22,28] . It is important to note that miscarriage, as a consequence of obesity in women undergoing IVF, is an addi-tional potential complication. This emphasizes the necessity of weight reduction before the beginning of fertility treatments [28,32] , especially in younger patients who are not at risk of an age-related decline in fertility [19] .  We observed an inverse correlation between BMI and physical activity. Furthermore, practic-ing physical activity had an independent effect on ICSI outcomes, as woman who practiced physical activity had higher implantation rates, increased chance of becoming pregnant and a lower probability of miscarriage. However, despite the fact that obesity did not influence the implantation and clinical pregnancy rates,  whether or not the benefit of physical activity on implantation and pregnancy rates is mediated by BMI reduction is still to be elucidated.The US Center for Disease Control and Prevention (CDC) recommends 30 min of physical activity on most days of the week [33] .  Although exercise is known to improve several health aspects, the relationship between exer-cise and fertility is complex. Physical activity can impact reproductive function through its ability to regulate energy balance, influencing the hormonal milieu, which in turn may favo-rably or unfavorably affect assisted reproductive outcomes. Previous studies have shown that intense physical activity practiced by female athletes is linked to anovulation and infertility due to lower levels of estrogen and progesterone, which sug-gest an absence of follicular development, ovula-tion and luteal function [34] . On the other hand, physical activity performed aiming to improve health, may promote changes on energy balance status, which in turn is tightly coupled with the reproductive system [35] . In addition, exercise leading to weight loss in obese women has been suggested to improve ovulation and subsequent fertility [36–38] .Studying the benefits of physical activity for nonathletes is complex due to the difficulty of quantifying physical activity in terms of fre-quency, intensity, modality and duration. Thus, studies evaluating the effect of exercise for health recommendations specifically on AR outcomes are scarce.In a previous study evaluating the influence of exercise on AR treatment, no contribution of physical activity was found to influence IVF outcomes [39] . On the other hand, we found that regular physical activity increased implantation rates, improved the chance of becoming pregnant to 80%, and reduced the risk of miscarriage by 70%. In this study, physical activity was consid-ered when performed at least three-times a week, independently of modality, duration or intensity.In summary, our findings demonstrate that obesity impaired oocyte quality and clinical outcomes of women undergoing ICSI cycles. Furthermore, BMI is inversely related to physi-cal activity, which in turn may independently lead to many benefits on clinical outcomes such as implantation, clinical pregnancy and mis-carriage. Thus, patients should be encouraged to regularly practice physical activity aiming to decrease the BMI in obese patients, result-ing in better clinical outcomes. This study also Table 4. Effect of obesity and practicing physical activity on the intracytoplasmic sperm injection cycles outcomes. Linear regression analysis † ObesityPracticing physical activity Mean value (%)Coefficientp-valueCoefficientp-value Normal fertilization rate 68.8 -16.0 0.010 1.6 0.553Implantation rate 20.3 1.6 0.852 9.4 0.009 Logistic regression analysis † Obesity Practicing physical activity Mean value (%)95% CIORp-value95% CIORp-value Clinical pregnancy 31.4 0.3 – 3.2 1.02 0.976 1.1–2.9 1.83 0.013Miscarriage 14.8 1.3–157.0 14.3 0.030 0.08–1.1 0.30 0.068 † Regression analyses maternal age-adjusted.
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