Food intake and social habits in male patients and its relationship to intracytoplasmic sperm injection outcomes

Food intake and social habits in male patients and its relationship to intracytoplasmic sperm injection outcomesDaniela Paes de Almeida Ferreira Braga, D.V.M., M.Sc.,a,b Gabriela Halpern, M.Sc.,a Rita de C
assia S. Figueira, M.Sc.,a Amanda S. Setti, B.Sc.,b Assumpto Iaconelli Jr., M.D.,a and Edson Borges Jr., M.D., Ph.D.a,b a Fertility-Assisted Fertilization Centre and b Sapientiae Institute-Educational and Research Centre in Assisted Reproduction, S ao Paulo,Brazil Objective: To investigate the influence of the male partner's lifestyle, including eating and social habits, on semen quality and intracytoplasmic sperminjection (ICSI) success.
Design: Observational study.
Setting: Private fertility clinic.
Patient(s): Two hundred fifty male patients undergoing ICSI cycles.
Intervention(s): We recorded dietary and social habits using a food frequency questionnaire adapted to meet specific study objectives. Evaluation ofsemen parameters and ICSI outcomes were performed.
Main Outcome Measure(s): Frequency of intake of food items and social habits were registered on a scale with five categories ranging from no con-sumption to repeated daily consumption.
Result(s): The sperm concentration was negatively influenced by body mass index (BMI) and alcohol consumption and was positively influenced bycereal consumption and the number of meals per day. The sperm motility was also negatively influenced by BMI, alcohol consumption, and smokinghabit, whereas it was positively influenced by the consumption of fruits and cereals. The consumption of alcohol had a negative influence on the fer-tilization rate. The consumption of red meat as well as being on a weight loss diet had a negative impact on the implantation rate. In addition, the con-sumption of red meat and being on a weight loss diet had an effect on the pregnancy chance.
Conclusion(s): Couples seeking assisted reproduction treatments must be advised about the drastic effect of both the male and female lifestyle on treat-ment success. (Fertil SterilÒ 2012;97:53–9. Ó2012 by American Society for Reproductive Medicine.)Key Words: Food intake, feeding habits, male infertility, intracytoplasmic sperm injection, lifestyle Lifestyle factors and nutritional disordersareprobablyrelatedtomulti- and nonessential functions. In times status are known to be critical de- ple factors, such as endocrine and met- of deprivation, it is necessary to ration terminants of normal reproduc- abolic functions, including the balance available oxidizable substrates in favor tive function A combination of of sex steroids, insulin, and leptin, of essential functions that are required reduced exercise, changes in dietary which, in turn, may directly or indi- to sustain life. Reproduction is expend- composition, and increased energy in- rectly affect ovarian function, follicular able at least in the short term and can take have contributed to a growing growth, implantation, and the develop- be deferred until times are more favor- worldwide epidemic in obesity, with seri- ment of a clinical pregnancy .
able. For example, menstrual cycles re- ous impacts on several aspects of health, However, eating disorders leading turn in some female athletes when including reproductive system health .
to weight loss are also associated with energy expenditure is reduced such as The deleterious effects of obesity a reduced frequency or the cessation after an injury .
on reproductive health include men- of ovulation. Food is used as a source Besides the deleterious effects of strual disorders and infertility. These of energy for a variety of essential overweight and underweight status onreproductive function, it has been sug- Received April 19, 2011; revised September 30, 2011; accepted October 11, 2011; published online gested that the consumption of specific November 10, 2011.
foods and drinks and some women's D.P.d.A.F.B. has nothing to disclose. G.H. has nothing to disclose. R.d.C.S.F. has nothing to disclose.
A.S.S. has nothing to disclose. A.I. has nothing to disclose. E.B. has nothing to disclose.
social habits can affect reproductive Daniela Paes de Almeida Ferreira Braga and Gabriela Halpern equally contributed to this manuscript.
outcomes. Alcohol and caffeine intake Reprint requests: Edson Borges Jr., M.D., Ph.D., Fertility–Assisted Fertilization Centre, Avenue Brigade- ao Paulo, SP, Brazil 01401-002 (E-mail: as well as tobacco smoking , could be important factors in Fertility and Sterility® Vol. 97, No. 1, January 2012 0015-0282/$36.00 the failure of assisted reproduction Copyright 2012 American Society for Reproductive Medicine, Published by Elsevier Inc.
doi: techniques (ART).
VOL. 97 NO. 1 / JANUARY 2012 ORIGINAL ARTICLE: ANDROLOGY Currently there is an increasing interest in investigating once a month, 2) 1–3 times per month, 3) once per week, 4) factors that can affect ART outcomes, and the impact of life- 2–4 times/week, and 5) every day.
style on female fertility has been well documented. However, The questionnaires were completed by the same inter- the influence of food intake and other social habits on male viewer, and a different questionnaire recorded information reproduction has been poorly investigated.
on exercising, weight loss diet, number of meals per day, Although the success rates of intracytoplasmic sperm in- and smoking habit. In addition the BMI was measured.
jection (ICSI) were thought to be independent of basic sperm Exercising was recorded in a scale of: 1) less than 1 hour parameters , recent reports have suggested that per week, 2) 1 hour per week, 3) 2 hours per week, 4) 3 hours repeated failures after ICSI may be caused by the effect of per week, 5) 4 hours per week, 6) 5 hours per week or more.
sperm-derived factors on preimplantation embryo develop- The smoking habit was recorded as the number of cigarette ment However, whether these sperm-derived factors, re- smoked per day and the BMI was measured by the weight/ ferred to as paternal effects, are affected by social and eating height2 and expressed as kilograms per meter squared.
habits is unknown. Therefore, the goal of the present studywas to investigate the influence of the male partner's lifestyle,including the effects of eating and social habits on semen Semen Preparation quality and ICSI success.
All semen samples were collected in the laboratory after 5days of ejaculatory abstinence. After liquefaction for 30 min-utes at room temperature, the semen samples were evaluated MATERIALS AND METHODS according to the threshold values established by the World Health Organization in 1999 (concentration R20
The study included 250 male patients undergoing ICSI cycles 106/mL, total count R40
106, and progressive motility in a private assisted reproduction center. All patients com- >50%) using a Makler counting chamber. Typical morphol- pleted a questionnaire with multiple choice questions before ogy was evaluated according to Kruger criteria the beginning of the treatment. Men were asked about the fre- Density gradient centrifugation technique was used for quency of consumption of many food items and were asked sperm preparation. All procedures were conducted under ster- about their social habits.
ile conditions. Using a sterile pipette 1.0 mL of the ‘‘lower The effects of dietary and social habits on basic sperm pa- layer'' (90% isolate; Irvine Scientific) was transferred into rameters were evaluated. In addition, the influence of dietary a conical centrifuge tube. Using a new sterile pipette 1.0 mL and social habits on fertilization, pregnancy (PR), implanta- of the ‘‘upper layer'' (50% isolate; Irvine Scientific) was gently tion, and miscarriage rates was investigated. In addition, dispensed on top of the lower layer. A liquefied 2.0-mL semen the female smoking habit and the female body mass index sample was then placed on top of the upper layer and the tube (BMI) were included in the analysis, as these variables could was centrifuged for 20 minutes at 330
g and this process influence the results.
was repeated using additional tubes until the whole ejaculated Pregnancy was defined as the presence of fetal heart ac- sample was processed. The upper and lower layers were tivity by ultrasound at 6–7 weeks of gestation, and implanta- carefully aspirated without disturbing the pellet. Using tion was defined as the presence of a gestational sac a transfer pipette, 1.0 mL of N-2-hydroxyethylpiperazine- visualized on ultrasound at 4–6 weeks after ET. Miscarriage N0-2-ethanesulfonic acid (HEPES)-buffered modified human was considered when the spontaneous loss of a pregnancy oc- tubal fluid (HTF; Irvine Scientific) medium was added and curred before 24 weeks of gestation.
the resuspended pellet was centrifuged for 7 minutes at 330 A written informed consent was obtained from those pa-
g. The washing procedure was repeated. The supernatant tients who agreed to share the outcomes of their own cycles was then removed and the pellet suspended in a volume of for research purposes. The study was approved by the local In- 0.5 mL of modified HTF medium. Sperm count and motility stitute Review Board.
were estimated in the recovered fractions.
Food Consumption and Social Habits Frequency Controlled Ovarian Hyperstimulation and Laboratory Procedures All patients were interviewed face-to-face by the same pro- Controlled ovarian hyperstimulation (COH) was achieved by fessional before the beginning of the treatment. The modified long-term pituitary down-regulation using a GnRH agonist validated questionnaire contained multiple choice ques- (Lupron Kit; Abbott S.A. Societ
e Franc¸aise des Laboratoires).
tions about the average frequency of consumption of food This was followed by ovarian stimulation with recombinant items during the past year.
FSH (Gonal-F; Serono).
The food categories investigated in the present study were Follicular dynamics were followed by transvaginal ultra- cereals, vegetables, legumes, fruits, red and pork meat, sound examination to follow the follicular growth, starting on chicken, fish, dairy products, sweet foods, alcoholic drinks, day 4 of gonadotropin administration. When adequate follic- caffeine-containing soft drinks, and coffee. The frequency ular growth and serum E2 levels were observed, recombinant of food consumption was registered on a scale with five hCG (Ovidrel; Serono) was administered to trigger final follic- values, ranging from no consumption to repeated daily con- ular maturation. Oocytes were collected 35 hours after hCG sumption. The specific categories were: 1) never or less than administration by transvaginal ultrasound ovum pick-up.
VOL. 97 NO. 1 / JANUARY 2012 Fertility and Sterility® Description of the average of basic semen parameters, frequency of consumption of food and social habits, and ICSI outcomes among the studiedpopulation.
Sperm concentration % Kruger normal cells Yes: 53.2%; no: 46.8% Fertilization rate % fertilized oocyte Implantation rate % gestational sacs % of pregnant women Note: Values expressed as percentage or average  SD. BMI ¼ body mass index; ICSI ¼ intracytoplasmic sperm injection.
Braga. Lifestyle and assisted reproduction. Fertil Steril 2012.
The recovered oocytes were assessed for their nuclear status.
The oocytes in metaphase II were submitted to ICSI following routine procedures The patients' characteristics are as follows (mean  SD): ma- Sperm samples were collected by masturbation within 3– ternal age, 32.3  4.4 years; paternal age, 38.4  9.3 years; 5 days of ejaculatory abstinence. Before semen preparation total dose of FSH administered for ovarian stimulation, for sperm injection, the sperm concentration, sperm motility, 2,230  712 UI; number of aspirated follicles, 13.4  9.3; and sperm morphology according to Kruger strict criteria number of retrieved oocytes, 9.8  3.4. The patients' ethnic- were recorded. Normal fertilization, which was indicated by ity is as follows: white (82.0%), Asian (5.2%), Hispanic the presence of two clearly distinct pronuclei, was assessed (2.0%), black (4.0%), other or mixed (2.8%), and unknown 18 hours after ICSI. After 3 days in culture, 1–3 embryos or not stated (4.0%). The average of basic semen parameters, were transferred per patient.
frequency of consumption of food and social habits, andICSI outcomes among the studied population are described Statistical Analysis To study the influence of social and eating habits on preg-nancy and miscarriage outcomes, binary logistic regressions Influence of Food Intake and Social Habits on Basic were performed. To study the influence of social and eating habits on sperm concentration, percentage of motile sperma- The sperm concentration was negatively influenced by BMI tozoa, sperm morphology, fertilization rate, and implantation and alcohol consumption and was positively influenced by rate, linear logistic regressions were conducted. All regression cereal consumption and number of meals per day. The sperm analysis was adjusted for maternal and paternal age, the motility was also negatively influenced by BMI, alcohol con- number of retrieved oocytes, number of transferred embryos sumption, and smoking habit, whereas sperm motility was and endometrium thickness and FSH dose, maternal smoking, positively influenced by the consumption of fruits and ce- and female BMI, as these variables would be considered po- reals. The sperm morphology was not affected by any food tential confounders of the association between the factor consumption or social habit ().
evaluated and the ICSI outcomes.
The results were expressed as odds ratios (OR) with a 95% Influence of Food Intake and Social Habits on ICSI confidential interval (CI) or regression coefficients (RC) anda P value. The results were considered to be significant at the 5% critical level (P< .05). Data analysis was carried out The male consumption of alcohol and coffee and the female using the Minitab (version 14) Statistical Program.
smoking habit had a negative influence on the fertilization VOL. 97 NO. 1 / JANUARY 2012 ORIGINAL ARTICLE: ANDROLOGY The main challenge for the success of ICSI is to produce viable Linear regression analysis of eating and social habits that may affect embryos that have high implantation potential. Implantation the sperm concentration, sperm motility, and sperm morphology.
and early postimplantation development are conditioned by Response variable Predictor variable the viability of each embryo transferred, which, in turn, de- pends on the biological quality of the oocyte and the sperma- Sperm concentration tozoon at the given embryo 's origin. Consequences of the actions of sperm-derived factors on preimplantation embryo development, referred to as paternal effects, have been shown to be responsible for repeated failures of assisted reproduction However, although there is an increasing interest in in- vestigating social and eating habits that may affect reproduc- tion outcomes in women, the influence of such habits in male reproduction is still poorly understood. The present study in- vestigated whether the consumption of specific foods and so- cial habits may influence semen quality and ICSI outcomes.
Our data suggest that both semen quality and ICSI outcomes may be influenced by specific food intake and social habits.
Smoking habits and alcohol consumption were shown to be involved in sperm quality and fertilization function im- pairment. Several studies have suggested that human semen quality and fertility have been declining during the past de- cades . Deterioration in seminal samples has been related to environmental and occupational pollutants, changes in lifestyles, exposure to toxins, and dietary habits Concerning lifestyle, smoking habits may be antioxidants, which places their sperm at additional risk of oxidative damage whereas excessive alcohol consumption may cause an increase in systemic oxidative In recent years, oxidative stress and the role of reactive oxygen species in the pathophysiology of human sperm func- tion and male infertility have been explored intensively. Sper- matozoa, from the moment that they are produced in the testes to when they are ejaculated into the female reproduc- tive tract, are constantly exposed to oxidizing environments, and oxidative stress has been recognized as one of the most important causes of male infertility .
We also demonstrated that the consumption of grains and fruits and the number of meals per day are positively related to sperm quality. These findings are consistent with a higher intake of minerals, essential amino acids, and antioxidant vi- Note: BMI ¼ body mass index; RC ¼ regression coefficient.
Braga. Lifestyle and assisted reproduction. Fertil Steril 2012.
tamins, which would lead to the maintenance or improvementof semen quality .
The consumption of coffee was also related to decreased rate (). The consumption of red meat and female BMI fertilization capacity. Caffeine, a psychotropic drug , is had a negative impact on the implantation rate. Being on present naturally and is an additive in many foods and drugs.
a weight loss diet had also a negative influence on the implan- It has been reported that 80% of pregnant women consume tation rate; however, it was noted that this result was depen- caffeinated beverages which may have detrimental ef- dent on the female BMI fects on reproductive biology. In fact, caffeine has been impli- In addition, the consumption of red meat and female BMI cated as a risk factor for delayed conception had an effect on the chance of pregnancy, and being on Klonoff-Cohen et al. showed a significant association a weight loss diet had also a negative influence on the implan- between female but not male caffeine consumption and live tation rate; however, it was again dependent on the female births. Likewise, although a significant effect of caffeine in- BMI The miscarriage outcome was not influenced take on fertilization rates has been observed in the present by any food consumption or social habit study, the pregnancy, implantation and miscarriage rates VOL. 97 NO. 1 / JANUARY 2012 Fertility and Sterility® Linear regression analysis of eating and social habits that may affect Binary regression analysis of eating and social habits that may affect the fertilization and implantation rates.
the pregnancy and miscarriage outcome.
Response variable Predictor variable Response variable Predictor variable Fertilization rate Implantation rate Note: BMI ¼ body mass index; RC ¼ regression coefficient.
Note: BMI ¼ body mass index; CI ¼ confidence interval; OR ¼ odds ratio.
Braga. Lifestyle and assisted reproduction. Fertil Steril 2012.
Braga. Lifestyle and assisted reproduction. Fertil Steril 2012.
were not affected, suggesting that if there is a harmful effect loss diet, it is likely that the other is also experiencing food of caffeine on sperm fertilization potential, once fertilized, the deprivation, especially when they are overweight and the de- embryo development is not impaired.
creased chance of assisted fertilization treatment success in However, not only the fertilization but also the pregnancy these couples is due to the diminished quality oocyte rather and implantation rates were negatively affected in patients than the sperm.
who reported being on a weight loss diet. It is well known Although undernutrition is the dominant factor regulat- that the reproductive system is extremely sensitive to influ- ing reproductive activity under natural conditions, obesity ences from the external environment and the mechanisms re- is an important cause of subfertility in many modern societies sponsible for the adjustment of reproductive function involve Recently, Martini et al. suggested a deleterious effect the availability of calories of obesity on seminal quality, probably by alterations in the Women with anovulation associated with strenuous ex- function of the epididymis. This is consistent with our find- ercise or who are underweight have low levels of leptin, LH, ings that demonstrated a negative influence of BMI on sperm and E2. The frequency of gonadotropin pulses is too low to quality. However, in a recent systematic review with meta- sustain development of antral follicles to the point of ovula- analysis, MacDonald and colleagues failed to demon- tion . However, whether the mechanism by which repro- strate any evidence of an association between increased ductive function is impaired in men with food deprivation BMI and semen parameters.
also involves the endocrinologic system is still unknown. In Our evidence also suggests that successful pregnancy and the present study the effect of being on a weight loss diet implantation outcomes are decreased in patients reporting on implantation rate and PR were dependent on the female a more frequent intake of meat. This finding is consistent BMI, and it could be argued that partners usually share the with poor semen quality associated with a higher intake of- same habits. Therefore if one partner is undergoing a weight VOL. 97 NO. 1 / JANUARY 2012 ORIGINAL ARTICLE: ANDROLOGY xenoestrogens or certain anabolic steroids . The Kupker W, al-Hasani S, Schulze W, Kuhnel W, Schill T, Felberbaum R, et al.
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