Journal of Trace Elements in Medicine and Biology 29 (2015) 31–38

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Review

The role of selenium in human conception and pregnancy ∗ ´ Joanna Pieczynska , Halina Grajeta Department of Food Science and Dietetics, Wroclaw Medical University, Borowska 211, 50-556 Wrocław, Poland

a r t i c l e

i n f o

Article history: Received 11 December 2013 Accepted 11 July 2014 Keywords: Selenium Antioxidative activity Pregnancy Reproduction

a b s t r a c t Selenium (Se) is a trace element essential for the appropriate course of vital processes in the human body. It is also a constituent of the active center of glutathione peroxidase that protects cellular membranes against the adverse effects of H2 O2 lipid peroxides. Epidemiological surveys have demonstrated that selenium deficiency in the body may contribute to an increased risk for certain neoplasmic diseases (including colonic carcinoma, gastric carcinoma, pulmonary carcinoma and prostate carcinoma), as well as diseases of the cardiovascular, osseous and nervous systems. Apart from its cancer prevention and antioxidative activities, selenium protects the body against detrimental effects of heavy metals and determines the proper functioning of the immunological system. Furthermore, selenium plays a significant role in the undisturbed functioning of the reproductive system. Many studies have addressed correlations between its intake and fertility as well as disorders of procreation processes. Selenium deficiencies may lead to gestational complications, miscarriages and the damaging of the nervous and immune systems of the fetus. A low concentration of selenium in blood serum in the early stage of pregnancy has been proved to be a predictor of low birth weight of a newborn. A deficiency of this element may also cause infertility in men by causing a deterioration in the quality of semen and in sperm motility. For this reason, supplementation in the case of selenium deficiencies in the procreation period of both women and men is of utmost significance. © 2014 Elsevier GmbH. All rights reserved.

Contents Biochemical properties of selenium . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Selenium sources in the human diet . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Human selenium status . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Health impact of selenium . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Phospholipid peroxide glutathione peroxidase and thioredoxin reductase in spermatogenesis . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Selenoprotein P in the testes . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Selenium and testosterone . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Correlations between estrogen and selenium in menstruation cycle . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Selenium in ovulation . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Selenium and female infertility . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Selenium status in pregnancy . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Implications of selenium deficiencies on the fetus . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Selenium status in pregnancy-related complications . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Preeclampsia . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Pre-term delivery . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Miscarriages . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Cholestasis . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Gestational diabetes mellitus . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .

∗ Corresponding author. Tel.: +48 071 7840214l; fax: +48 071 7840206. ´ E-mail address: [email protected] (J. Pieczynska). http://dx.doi.org/10.1016/j.jtemb.2014.07.003 0946-672X/© 2014 Elsevier GmbH. All rights reserved.

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Thyroid dysfunction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Effect of tobacco, alcohol and polycyclic aromatic hydrocarbons on selenium status in pregnancy . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Conflict of interest . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .

Biochemical properties of selenium Selenium was discovered in the year 1817 by the Swedish chemist Jöns Jacob Berzelius. Initially, it had been perceived as a toxic element, but after 140 years, a study by Schwarz and Folt [1] demonstrated that Se is essential for human biology. Today, it is acknowledged as a trace element fundamental to human health. Selenium is absorbed from food in the form of inorganic compounds like selenites (Me2 SeO3 ) and selenates (Me2 SeO4 ) or organic links – selenomethionine (SeMet) and selenocysteine (SeCys). The absorption of selenium from organic compounds reaches 90–95%, whereas from inorganic links, it is lower by ca. 10% [2]. Its bioavailability increases when a diet is rich in low molecular weight proteins, vitamins (mainly A, C and E), and it decreases if a diet contains an increased concentration of heavy metals (cadmium, lead, arsenic and mercury) [3]. Selenium sources in the human diet For humans, a source of this microelement is foodstuff of both plant and animal origin, and marginally – drinking water. High quantities of selenium are provided by, among others, cereal products, seafood, haslets, eggs, yeast, tomatoes, asparagus, garlic, broccoli, nuts (especially Brazilian nuts), and turnip cabbage. Although more selenium is found in products of animal origin, the best sources of this element are wheat and other plant products owing to its better bioavailability [3]. The Se content of plant food depends mainly on the soil-type in which the plant was grown, but also on the agricultural use of pesticide, manure and phosphate fertilizers [4,5]. The health impacts of Se deficiency in human subjects can be related, however, to the level of Se in the environment if the local inhabitants are dependent on their direct surroundings for sustenance. In developed and well urbanized countries in which populations are less dependent on their proximate environment for food and drinking water, establishing a link is more difficult (Table 1). Human selenium status The nutritional status of selenium can be assessed by determining Se levels in blood (whole blood, erythrocyte, serum or plasma), urine, nails and hair. Serum or plasma selenium reflects short-term status as opposed to erythrocyte selenium which reflects long-term status [9]. There is a marked variation in Se intake and status from Table 1 Selenium content in food products from different countries (␮gSe/100 g) [6–8]. Food product

Denmark

Finland

Canada

Wheat bran Breakfast cereal cornflakes Bread white prepared with bread mixture Bread brown, wheat Cabbage white, raw Egg chicken, whole Oysters Herring salted Salmon smoked Liver chicken, raw Kidney pork, raw

2 5 4 4 1 17 36 46 16 49 150

9.5 2.9 2.9 5.7 1.5 24.9 3 22 26 135

77.6 15 17.3 28.8 0.3 34.2 33.8 36.5 22.2 54.6 190

35 36 36 36

one part of the world to another. Furthermore, it is often difficult to compare results because of variations in methodology in different laboratories. Because of variations in selenium status there are no accepted normal/optimal reference ranges. Usually, the recommended reference values are based on the evaluation of data from the literature in particular countries. An example might be the German Human Biomonitoring Commission which estimated reference values for selenium status: serum/plasma 50–120 ␮g/L; whole blood: females 60–120 ␮g/L and males 79–130 ␮g/L; erythrocytes per g hemoglobin females and males 0.2–0.6 ␮g (Table 2) [10]. Health impact of selenium This element, as a constituent of selenoproteins, activates anticarcinogenic factors, prevents diseases of the cardiovascular systems as well as exhibits anti-proliferative and anti-inflammatory activities [31,32]. Furthermore, it stimulates the immune system and acts antagonistically to such heavy metals as: arsenic, cadmium, lead and mercury [33–35]. Selenium deficiencies are mainly developed due to insufficient content in diet, but also as a result of disorders in its transport in biological fluids and in the improper synthesis of selenoproteins. They may also results from active disease [32,36]. As a component of enzymes, Se serves many important functions in the human body. The key one is its antioxidative function – it impairs adverse processes of lipids peroxidation and protects cells against damage to genetic material. The protective role of selenium results from its presence in glutathione peroxidase (GPx) and thioredoxin reductase (TrxRs), namely in the active center of antioxidative enzymes [37]. Phospholipid peroxide glutathione peroxidase and thioredoxin reductase in spermatogenesis Proper spermatogenesis requires two selenoproteins: phospholipid peroxide glutathione peroxidase – PHGPx and selenoprotein P. In the testes, selenium occurs mainly in the PHGPx form, namely in the form of one of the selenium-dependent antioxidative enzymes. TrxRs was additionally detected in the testes of mature male mice. Its high quantities may be observed in maturing spermatides, whereas its reduced expression – in mature semen [38]. Scientists have advanced a hypothesis that both selenoenzymes – TrxRs and PHGPx – together constitute a system capable for the formation of disulfide bridges that stabilize the protein ultrastructure of semen [39]. In turn, spermatic tubules have been shown to contain selenoprotein V, whose physiological role is still undefined, though it is speculated to play some role in the regulation of redox processes [40,41]. The testes are organs which are characterized by the highest expression of PHGPx in the body of mammals, exceeding even the expression of such key organs as the liver and kidneys. The most significant function of this enzyme includes the protection of plasmatic membranes of maturing spermatozoa against the attack of free radicals. Researches have shown, however, that not only the antioxidative properties of PHGPx are utilized in spermatozoa [42]. This protein constitutes ca. 50% of the material contained in the mitochondrial membrane of a spermatozoon and is enzymaticallyinactive therein. The structural function of selenoproteins may

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Table 2 Selenium status in healthy adult individuals from different countries. Country

Australia Belgium Chile Croatia Czech republic Finland France Greece Germany India Japan Korea Pakistan Poland Russia Sweden United Kingdom USA

Selenium assessment (technique)

Plasma (ICP-OES)a Serum (GFAAS) Plasma (AAS) Serum (AAS) Whole blood (HGAAS) Serum (ETAAS) Serum (ETAAS) Serum (ICP-MS) Serum (ICP-MS) Serum (GFAAS) Plasma (fluorimetry) Plasma (fluorimetry) Serum (ICP-MS) Whole blood (ICP-MS) Plasma (AAS) Serum (fluorimetry) Serum (fluorimetry) Serum (ICP-MS) Plasma (ICP-MS) Serum (ICP-MS)

Mean selenium concentration (␮gSe/L)

Reference

Men

Women

Total

– – – 72.7 (n = 123) 81.4 (n = 1781) 117.9 (n = 38) 90.0 (n = 5141) 90.5 (n = 296) – – 119.8 (n = 7) – 103.2 (n = 50) 92.0 (n = 56) 77.6 (65) – – 110.0 (n = 304) 66.3 (n = 589) –

– – 112.9 (n = 29) – 82.0 (n = 633) 113.1 (n = 70) 86.1 (n = 7876) 93.9 (n = 210) – – – 119.2 (n = 6) 120.8 (n = 50) 100.0 (56) 70.4 (n = 81) – 93.9 (n = 556) 109.0 (n = 362) 67.1 (n = 545) –

103.0 (n = 288)b 84.3 (n = 26) – – 81.9 (n = 2414) 115.5 (n = 108) 88.0 (n = 13,017) 91.8 (n = 406) 87.7 (n = 492) 90.8 (n = 196) – – 112.0 (n = 100) 96.0 (112) 72.5 (n = 146) 96.0 (n = 2462) – 109.0 (n = 666) 67.0 (n = 1134) 136.4 (n = 796)

[11] [12] [13] [14] [15] [16] [17] [18] [19] [20] [21] [22] [23] [24] [25] [26] [27] [28] [29] [30]

a ICP-MS, inductively coupled plasma mass spectrometry; AAS, atomic absorption spectrometry; ETAAS, electrothermal atomic absorption spectrometry; GFAAS, graphite furnace atomic absorption spectrometry; HGAAS, hydride generation atomic absorption spectrometry. b Mean (number of samples).

elucidate the reduced motility of spermatozoa caused by disorders in morphology of the spermatozoon mid-piece (the area between the head and the tail that contains multiple mitochondria generating energy necessary to propel the sperm cell) in the case of selenium deficiencies [38]. In addition, PHGPx may participate in chromatin organization. In a study on knockout mouse deprived of testicular PHGPx, disorders could be observed in chromatin condensation in the spermatozoa present in the head of the epididymis [43]. In spite of that, the spermatozoa were viable and capable of fertilization, whereas the chromatin defect was probably fixed in the process of sperm cell maturation in the epididymises. In other research, spermatozoa of a mouse fed a selenium-poor diet showed abnormal spermatozoon head morphology [44]. Complete deprivation of PHGPx synthesis (both mitochondrial, nuclear and cytosolic) in mice resulted in a significant increase of fetal mortality rate in homozygous mice. In addition, target silencing of gene expression for the mitochondrial isoform has led to severe damages in cerebellum development and has inducted apoptosis in the cerebral tissue, whereas the silencing of the nuclear form resulted in delayed heart development [45]. The appropriate supply of selenium and its positive impact on reproduction have been documented in studies with experimental animals. Results of surveys with human patients are, however, less explicit. Many scientists have linked a low concentration of PHGPx in patients suffering from oligoasthenozoospermis with reduced motility of spermatozoa and abnormalities in mitochondria morphology [46–48]. X-ray fluorescence microscopy may confirm their suspicions. This method can be used to visualize and quantify the tissue, cellular and subcellular topography of Se. Analyses using this method showed that PHGPx was present at high levels in the epididyma sperm [49]. This, however, has not been corroborated in other studies [50,51]. Differences in results could be due to different research material origin – from mice and men. As a result more exhaustive research is needed regarding male infertility and its correlation with deficiency of selenium or selenoproteins. Selenoprotein P in the testes The second significant component of the selenium pool in the testes is selenoprotein P. Its deficiency in a group of

knockout mice (deprived of this selenoprotein) has induced numerous disorders of the structure of the spermatozoa tail: improper mitochondrial membranes, disorders in the morphology of axonema microtubules, and improper morphology of the links of the central and main section of the spermatozoon. Symptoms of selenoprotein P deficiency were the same as in the second group in which mice were fed a diet poor in Se. The difference lay in the fact that selenium supplementation was contributing to an improvement in the status linked with diet-related deficiency, whereas not in the status caused by the lack of selenoprotein P. This enabled the conclusion that this protein is essential for selenium homeostasis and for functional development of spermatozoa [52]. Infertility in selenoprotein P knockout mice can be eliminated by transgenic expression of human selenoprotein P under the control of a hepatocyte-specific transthyrein promoter [53]. Most selenoprotein P is produced and secreted by the liver, although other tissues produce it as well. In a study conducted by Olson et al. [54] authors define the uptake mechanism and trafficking pathway by which selenoprotein P delivers its selenium to developing germ cells. They demonstrate that apolipoproteinE receptor 2 (ApoER2) is a selenoprotein P receptor and a component of the selenium delivery pathway to spermatogenic cells. Selenoprotein P is highly concentrated not only in the testes, but also in seminal fluid, likewise important to protection of sperm during storage, genital tract passage and final journey [55]. Selenium and testosterone Tests conducted on rats by Behne and co-workers [56,57] suggest that selenium may also influence the biosynthesis and secretion of testosterone. These authors have demonstrated that in the case of an insufficient supply of this element with diet, it is first delivered to testes and then to other tissues. A reduced level of Se was noted in the testes of hypophysectomized individuals. However, its level increased upon the administration of testosterone, which points to either an indirect or direct dependency of hormones responsible for spermatogenesis on the appropriate level of selenium in this organ. Furthermore, stimulation with luteinizing hormone-releasing hormone (LHRH) or chorionic gonadotropin (hCG) in individuals with selenium deficiency elicited a less

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affects the production of nitrogen oxide (NO), which plays a key role in the activity of ovaries. Selenium reduced NO production induced by bovine folliculotropic hormone (bFSH), in cells of both large and small follicles, although the most tangible differences were observed in the latter [66]. Selenium and female infertility

Fig. 1. Plasma selenium concentration during menstrual cycle.

significant increase in the serum concentration of testosterone, than in Se adequate males. It is also speculated that deficiency of this element causes some changes in the receptors of the luteinizing hormone (LH) on Leydig cells, thus affecting testosterone secretion [58].

In one of the sparse human studies, Paszkowski’s group [67] observed a lower selenium concentration in the follicular fluid of women with unexplained infertility, compared to women who were infertile due to other reasons. Simultaneously, no differences were demonstrated in either selenium concentration in the serum or GPx concentration in the serum and the follicular fluid between the analyzed groups of women. According to these authors, the results obtained suggest that the antioxidative activity of GPx in the follicular microenvironment may play a certain role in the process of gametogenesis and fertilization. Selenium status in pregnancy

Correlations between estrogen and selenium in menstruation cycle Despite sparse information on the relationship between female sex hormones and selenium status, research conducted with healthy women point to a correlation between estrogen content and selenium content as well as GPx activity depending on the phase of the menstruation cycle [59,60]. Both selenium concentration in the serum and GPx activity in the serum and erythrocytes are at their lowest in the early follicular phase, whereas they are at their the highest in the pre-ovulation phase, and then decrease in the middle luteal phase. These changes are concurrent with jumps in the concentration of 17-␤-estradiol during the menstruation cycle [59,60]. Such correlations were, however, not observed with respect to selenium concentration in erythrocytes. Likewise, no correlations were noted between the activity of GPx and concentrations of progesterone and androgens during the cycle [59,60]. These results are indicatory of the regulating effect of estradiol on the activity of GPx in erythrocytes during the menstruation cycle. These authors emphasize also the necessity of considering the phase of the menstruation cycle while evaluating the selenium status in women, though not all studies demonstrated a correlation between Se concentration in the plasma and the phase of the cycle [22,60]. This lack of correlation could be a result of not equal number of subjects in studied groups and different participants’ country origin (Japan, USA and Italy) (Fig. 1). Selenium in ovulation Although reduced fertility in women is often linked with insufficient body saturation with selenium, its role in this process still remains unknown. Perhaps it is due to the fact that selenium is a co-factor of antioxidative enzymes that are responsible for the neutralization, elimination and prevention of synthesis of reactive oxygen species (ROS) [61,62]. Through ROS, the oxidative stress affects oocytes. It has been observed that the first meiotic division in these cells is induced by an increase in ROS concentrations, and that it is inhibited by antioxidants. This allows for the presumption that ROS secretion, regulated by a pre-ovulation ovarian follicle, is a significant promoter in the course of ovulation and requires maintaining a gentle balance between ROS and antioxidants [63,64]. Investigations on bovine granular cells enveloping the primordial ovarian follicle have demonstrated that selenium had a significant effect on their proliferation and enhanced the stimulating action of gonadotropins in these cells [65]. This element also

Pregnancy is an exceptional condition of enhanced demand for various nutrients. Physiological changes proceeding in the body of a pregnant woman caused, for example, by a high concentration of progesterone, include a reduced bioavailability of some dietary components and an increased demand for them owing to a developing fetus. Deficiencies of mineral elements and vitamins in this period may contribute to the occurrence of perinatal complications, fetus necrobiosis, congenital organ defects in the child and impairment of the immune system functioning in a fetus [68–70]. During pregnancy, the concentration of selenium in the blood ˛ decreases significantly. Wasowicz et al. [71] assayed its level in the blood of 64 women during delivery and compared it with selenium concentration in the blood of non-pregnant women. Se concentration was observed to decrease significantly during pregnancy, in the pregnant women it accounted for 35 ␮g/L, whereas in the non-pregnant women, 59 ␮g/L, on average. Similar results were obtained by Zachara et al. [72], who additionally showed a drop in GPx activity in mother’s plasma. Mihailovic´ et al. [73] determined concentrations of selenium and malondialdehyde (MDA) and the activity of GPx in the blood of pregnant women in particular trimesters of pregnancy. A significant decrease in the level of selenium was noted in the second and the third trimester of pregnancy and during delivery. Concurrently, a decline was observed in the activity of GPx in the first trimester. Throughout the two subsequent trimesters it maintained a similar level of activity as in the first trimester, whereas during delivery it slightly increased. Furthermore, changes in selenium homeostasis during pregnancy are probably, due to an increased demand for oxygen in the body of mother and a developing fetus. Enhanced production of ROS and the intensity of lipid oxidation processes are then observed. The assurance of the appropriate antioxidative protection to the fetus is indispensable due to enhanced oxygen transformations taking place during delivery and in the early postnatal period [73,74]. Another reason behind the boosted demand for selenium in pregnant women may be an increased mass of erythrocytes in the fetus [75]. The estimated average requirements (EAR) and recommended dietary allowances (RDA) for selenium have been stipulated at levels which assure the optimal concentration of GPx in blood serum, however due to the aforementioned reasons during pregnancy, the RDA for this element is increased and ranges from 55 ␮g/day to 60 ␮g/day [51].

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Implications of selenium deficiencies on the fetus Deficiency of selenium in pregnant women may lead to dysfunctions in the nervous system of a developing fetus. Cengiz et al. [76] demonstrated a positive correlation between a low concentration of this element in the serum of pregnant women and the occurrence of neural tube defects, especially anencephaly and rachischisis (a type of birth defect that causes abnormal formation of the spinal column), in their progeny. It ought to be emphasized, however, that the development of the nervous system defects is affected by many factors, with selenium deficiency during pregnancy being only one of them [77,78]. Selenium status in pregnancy-related complications Preeclampsia Maternal selenium status may contribute to the incidence of the preeclamptic state (EPH gestosis). Conflicting results have been found in research examining the serum concentrations of selenium in preeclamptic women. Some studies have observed a reduction in concentrations of selenium in plasma or serum [79,80], and others have reported an increased selenium concentration in preeclamp´ tic woman than in normal pregnant women [81,82]. Gromadzinska et al. [81] observed higher concentrations of selenium and activity of GPx in serum of women with preeclampsia and with the risk of premature delivery. It is speculated to be a consequence of the action of mechanisms protecting the body against the occurrence of oxidative stress. Circulating lipid peroxides may lead to damage of the placenta, which causes retardation of fetus growth. They additionally lead to an increased content of thromboxane, a reduced content of prostacyclins, and damage of vascular endothelium cells, resulting in an improper blood flow in the placenta [80].

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miscarriage than in the women with a normal course of pregnancy as well as woman in the control group. A lower concentration of selenium in women with RPL compared to women with miscarriage may be due to a chronic deficiency of this element in their diet. Cholestasis Authors of some studies point also to a correlation between selenium deficiency and the incidence of cholestasis in pregnant women. The pregnant women with cholestasis were characterized by a lower selenium concentration in the blood and by a lower activity of GPx in erythrocytes than the healthy pregnant women. In patients with intrahepatic cholestasis of pregnancy the low concentration of selenium (possibly disturbed function of the microsomal cytochrome P-450 system, also controlled by selenium) and the reduced activity of glutathione peroxidase, may lead to the formation of free radicals, which could damage the hepatocytes and reduce excretion of bile [89,90]. Gestational diabetes mellitus

Bogden et al. [83] examined 107 women with pre-term delivery and 126 women with planned delivery. Progeny of the female patients with extremely low selenium concentration in the serum was characterized by a significantly lower birth weight than the progeny of women with a higher selenium concentration during pregnancy. The difference in the birth weight was significant and reached 259 g. However, this study did not demonstrate any correlation between the low concentration of this element and pre-mature delivery.

Diabetes is one of the most common diseases developing in pregnant women. Due to insulin-resistance and the increased demand for insulin in the period of pregnancy, some women suffer from debilitated glucose tolerance, which may transform into gestational diabetes mellitus (GDM). Selenium is speculated to be essential for the proper glucose uptake, the regulation of the cellular absorption of glucose and reduction of insulin resistance. Contrary to those expectations, recent epidemiological and intervention studies revealed a surprising association between high plasma selenium levels and type 2 diabetes, hyperglycemia and dyslipidemia. It is tempting to speculate that selenoprotein P and/or low-molecular-weight selenium compounds may affect insulin induced signaling pathways related to carbohydrate and lipid metabolism. The epidemiological association between high plasma selenium levels and hyperglycemia might also be explained by a disturbance of selenium homeostasis as a side-effect of a dysregulated carbohydrate metabolism [91]. Tan et al. [92], after the examination of 234 pregnant women (98 with glucose intolerance, 46 with gestational diabetes, and the remainder with normal pregnancy), demonstrated a significantly lower selenium concentration in the blood of women with gestational pregnancy, compared to normal pregnant women. Corresponding results were showed in Al-Saleh et al. study [93].

Miscarriages

Thyroid dysfunction

Low concentrations of selenium and antioxidative enzymes may also elicit recurrent miscarriages [84,85]. Al-Kunani et al. [86] examined two groups of non-pregnant women. One group included 18 women after one or more normal deliveries, whereas the other group included 26 women with recurrent pregnancy losses (≥3). The study involved a comparison of selenium content in the hair and serum of women of both groups. Corresponding results were achieved in Kumar et al. [87] study which demonstrated a significantly lower concentration of Se in erythrocytes in women with RPL compared to normal women. However, Zachara et al. [88] determined the concentration of selenium and activity of GPx in the blood of 40 women ages 17–40, who had miscarried in the first or second trimester of pregnancy. In the above study, selenium concentration in whole blood or plasma was comparable between women with miscarriage and healthy women. The activity of GPx in erythrocytes and plasma was significantly lower, and the concentration of glutathione in erythrocytes was higher in patients after

Selenium, as a component of selenoproteins, plays a significant role in the biosynthesis of thyroid hormones. In women who are at the reproductive age, hypothyroidism has an indirect or direct impact on their fertility, course of pregnancy and the development of the child. The development of the central nervous system takes place in the first and second trimester of pregnancy and is determined most of all by the transport of the mother’s thyroid hormones through the placenta [94]. A hormone essential for the proper development of the organs of the fetus is triiodothyronine. Klinger et al. [95] assayed concentrations of selenium, thyroxin, thyreotropic hormone and triiodothyronine in the blood of 29 newborns born between weeks 26 and 28 of pregnancy, with a mean birth weight of 809 g. They did not, however, demonstrate any correlation between the selenium level and concentrations of the assayed thyroid hormones. Selenium plays an important role in the thyroid gland under normal physiological conditions and in the case of disease. In particular, pregnant women

Pre-term delivery

36

J. Pieczy´ nska, H. Grajeta / Journal of Trace Elements in Medicine and Biology 29 (2015) 31–38

Table 3 Selenium status in pregnancy-related complications. Selenium assessment (technique)

Country

Case subjects

Serum (fluorimetry)

Indonesia

Serum (AAS)b

South Wales

Red cells (fluorimetry)

India

Whole blood (AAS)

Yugoslavia

Whole blood (AAS)

Kuwait

Plasma (AAS)

Chile

Serum (AAS)

Finland

Plasma (GFAAS)

Iran

Toenail (INAA) (mg/kg)

United Kingdom

Serum (AAS)

United Kingdom

Whole blood (AAS)

Italy

Spontaneous miscarriage Spontaneous miscarriage Non-pregnant women with recurrent miscarriage Hypertensive pregnant women Diabetic pregnant women Intrahepatic cholestasis pregnant women Intrahepatic cholestasis pregnant women Pregnant women with preeclampsia Pregnant women with preeclampsia Pregnant women with preeclampsia Euthyroid pregnant women

a b

Selenium concentration (␮gSe/L)

Noncase subjects

Selenium concentration (␮gSe/L)

Reference

66.71 (n = 25)a

Normal pregnancies

76.36 (n = 46)

[97]

54.48 (n = 40)

Normal pregnancies

65.29 (n = 40)

[84]

150.55 (n = 20)

[87]

57.5 (n = 37)

[98]

119.55 (n = 20)

Healthy non-pregnant women

54.65 (n = 23)

Normotensive pregnant women

85.65 (n = 14)

Healthy pregnant women

102.65 (n = 17)

[93]

78.43 (n = 21)

Healthy pregnant women

92.22 (n = 98)

[89]

27.65 (n = 12)

Healthy pregnant women

41.65 (n = 12)

[90]

71.22 (n = 38)

Healthy pregnant women

80.27 (n = 38)

[79]

0.56 (n = 53)

Healthy pregnant women

0.62 (n = 53)

[80]

39.7 (n = 25)

Healthy pregnant women

58.4 (n = 25)

[99]

75.7 (n = 74)

Healthy pregnant women

76.8 (n = 81)

[96]

Mean (number of samples). AAS, atomic absorption spectrometry; GFAAS, graphite furnace atomic absorption spectrometry; INAA, instrumental neutron activation analysis.

with autoimmune thyroiditis (thyroid-peroxidase-antibody positive) are prone to develop hypothyroxinemia during pregnancy and thyroid dysfunction after delivery. In a study conducted by Negro et al. [96] after selenomethionine supplementation of pregnant woman (200 ␮g per day), thyroid inflammatory activity fell, and post-partum thyroid disease and permanent hypothyroidism were significantly reduced (Table 3). Effect of tobacco, alcohol and polycyclic aromatic hydrocarbons on selenium status in pregnancy The course of pregnancy is also negatively affected by tobacco smoking. Toxic substances present in tobacco smoke intensify oxidative transformations and exert adverse effects on fetus development. Frequent smoking and exposure to environmental tobacco smoke during pregnancy may cause reduced availability of selenium to fetus tissues, preterm delivery, preterm rupture of fetal membranes, reduced birth weight of the child, hypotrophy, and many other severe disorders in the period of intrauterine development [100,101]. A low concentration of selenium lowers the effectiveness of defense against detrimental factors and of the antioxidative defense of the body. Kantola et al. [102] demonstrated that the level of this element in the blood plasma of women in delivery and in the plasma of cord blood was significantly lower in women who smoke than in non-smokers. No effect was, however, noted of tobacco smoking on selenium concentration in the placenta. Another addiction implicated in the suppression of selenium transport to the fetus is alcohol consumption during pregnancy. Alcohol may cause damage to and reduce the weight of the placenta, through which selenium is transported to a developing child [103]. The proper amount of selenium in the bodies of a mother and a fetus may protect them against the carcinogenic and mutagenic activity of polycyclic aromatic hydrocarbons (PAH) present in tobacco smoke and exhaust fumes, as well as in smoked foods and those fried at high temperatures. Most PAHs induce the activity of P450-1A1 cytochrome (CYP1A1), which is responsible for the

formation of their toxic metabolites. This induction may also occur in the placenta, and the PAHs may inactivate enzymes present therein. This process is especially enhanced during pregnancy [104,105]. Other studies have demonstrated that selenates might inhibit the activity of CYP1A1. Huel et al. [106] examined 178 pregnant women and observed a lower concentration of selenium in the plasma of women at risk of preterm delivery than in women with a normal course of pregnancy. The patients at risk of preterm delivery were also noted to have a higher activity of CYP1A1 cytochrome. The results of this study suggest that the antioxidative activity of selenium may prevent preterm deliveries, affect the final outcome of cyclic compounds metabolism and protect the bodies of fetus and mother against their adverse effects. This review presents the potential influence of selenium status on many disorders relating to human reproduction and pregnancy. The limitation of many previous studies is the lack of correction for potential confounding factors such as include other nutritional deficiencies, dietary habits, general health of the participants, etc. Obtaining detailed and accurate dietary and medical data is essential in the designing of any future studies. In conclusion, though reliable evidence already exists to suggest that additional selenium intake would be beneficial in some of the aforementioned disorders in selenium-deficient women and men, results from future intervention trials can provide us with arguments for or against increasing selenium intake. Conflict of interest The authors declare that there are no conflicts of interest. References [1] Schwarz K, Foltz CM. Selenium as an integral part of “Factor 3” against dietary necrotic liver degeneration. J Am Chem Soc 1957;79(12):3292–329. [2] Finley JW. Bioavailability of selenium from foods. Nutr Rev 2006;64:146–51. [3] Navarro-Alarcon M, Cabrera-Vique C. Selenium in food and the human body: a review. Sci Total Environ 2008;400:115–41.

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