Potential pathways of pesticide action on erectile function – A contributory factor in male infertility

Sharath, 2013, Association of obesity with male infertility among infertile couples is not significant in Mysore, South India, Adv Stud Biol, 5, 319, 10.12988/asb.2013.3316 Brugh, 2004, Male factor infertility, Med Clin North Am, 88, 2367, 10.1016/S0025-7125(03)00150-0 Hirsh, 2003, Male subfertility, BMJ, 327, 669, 10.1136/bmj.327.7416.669 Read, 1999, Sexual problems associated with infertility, pregnancy and ageing, BMJ, 318, 587, 10.1136/bmj.318.7183.587 Beyond pesticides. Pesticide-induced diseases: birth/fetal effects. [Online] Avaliable from: http://www.beyondpesticides.org/health/birthdefects.php [Accessed on 10th March]. Soliman, 2008, Erectile dysfunction in workers chronically - exposed to pesticides and organic solvents in Damietta Governorate, Mansoura J Forensic Med Clin Toxicol, 16, 63, 10.21608/mjfmct.2008.54095 Cooper, 2010, World Health Organization reference values for human semen characteristics, Hum Reprod Update, 16, 231, 10.1093/humupd/dmp048 Leibovitch, 2005, The vicious cycling: bicycling related urogenital disorders, Eur Urol, 47, 277, 10.1016/j.eururo.2004.10.024 Costabile, 2001, Characterization of patients presenting with male factor infertility in an equal access, no cost medical system, Urology, 58, 1021, 10.1016/S0090-4295(01)01400-5 Masarani, 2006, Mumps orchitis, J R Soc Med, 99, 573, 10.1258/jrsm.99.11.573 Cavallini, 2006, Male idiopathic oligoasthenoteratozoospermia, Asian J Androl, 8, 143, 10.1111/j.1745-7262.2006.00123.x Zhang, 2007, Novel mutations in ubiquitin-specific protease 26 gene might cause spermatogenesis impairment and male infertility, Asian J Androl, 9, 809, 10.1111/j.1745-7262.2007.00305.x Andrology Australia. Male infertility. [Online] Available from: https://www.andrologyaustralia.org/reproductive-problems/male-infertility/[Accessed on 8th May, 2015]. Olooto, 2012, A review of female infertility; important etiological factors and management, J Microbiol Biotech Res, 2, 379 Scott, 2000, Hyperprolactinemia and erectile dysfunction, Rev Urol, 2, 39 Hruska, 2000, Environmental factors in infertility, Clin Obstet Gynecol, 43, 821, 10.1097/00003081-200012000-00014 Mendiola, 2008, Exposure to environmental toxins in males seeking infertility treatment: a case-controlled study, Reprod Biomed Online, 16, 842, 10.1016/S1472-6483(10)60151-4 Hauser, 2007, DNA damage in human sperm is related to urinary levels of phthalate monoester and oxidative metabolites, Hum Reprod, 22, 688, 10.1093/humrep/del428 Brydoy, 2007, Gonadal dysfunction and fertility problems in cancer survivors, Acta Oncol, 46, 480, 10.1080/02841860601166958 Lee, 2007, Effect of di (n-butyl) phthalate on testicular oxidative damage and antioxidant enzymes in hyperthyroid rats, Environ Toxicol, 22, 245, 10.1002/tox.20259 Gaur, 2007, Effect of cigarette smoking on semen quality of infertile men, Singap Med J, 48, 119 Akhter, 2012, Evaluation of female infertility, J Med, 13, 200 Expert group on commissioning NHS infertility provision, 2009 Momoh, 2007, Resistant pattern of urinary tract infection bacterial isolates to selected quinolones, Benin J Postgrad Med, 9, 22 American Society for Reproductive Medicine, 2008, The management of infertility due to obstructive azoospermia, Fertil Steril, 90, 121, 10.1016/j.fertnstert.2008.08.096 Oger, 2003, Evaluating sperm DNA integrity: relationship between 8 hydroxyguanosine quantification and sperm chromatin structure assay, Zygote, 11, 367, 10.1017/S0967199403002442 Ozmen, 2007, DNA damage of human spermatozoa in assisted reproduction: origins, diagnosis, impacts and safety, Reprod Biomed Online, 14, 384, 10.1016/S1472-6483(10)60883-8 Momoh, 2011, Pathogenic bacteria-a probable cause of primary infertility among couples in Ekpoma, J Microbiol Biotech Res, 1, 66 Ochsendorf, 1999, Chlamydia trachomatis and male infertility: chlamydia-IgA antibodies in seminal plasma are C. trachomatis specific and associated with an inflammatory response, J Eur Acad Dermatol Venerol, 12, 143, 10.1111/j.1468-3083.1999.tb01005.x Wolf, 1995, The biologic significance of white blood cells in semen, Fertil Steril, 63, 1143, 10.1016/S0015-0282(16)57588-8 Nikiforos, 2003, Detection of herpes simplex virus, cytomegalovirus, and Epstein-Barr virus in the semen of men attending an infertility clinic, Fertil Steril, 79, 1566, 10.1016/S0015-0282(03)00370-4 Senanayake, 2008, Mumps: a resurgent disease with protean manifestation, Med J Aust, 189, 456, 10.5694/j.1326-5377.2008.tb02121.x Rosendahl, 2010, Dynamics and mechanisms of chemotherapy-induced ovarian follicular depletion in women of fertile age, Fertil Steril, 94, 156, 10.1016/j.fertnstert.2009.02.043 Carlsen, 1992, Evidence for decreasing quality of semen during the past 50 years, BMJ, 305, 609, 10.1136/bmj.305.6854.609 Auger, 1995, Decline in semen quality among fertile men in Paris during the past 20 years, Engl N. J Med, 332, 281, 10.1056/NEJM199502023320501 Adamopoulus, 1996, Seminal volume and total sperm number trends in men attending sub fertility clinics in the Greater Athens area during the period 1977-1993, Hum Reprod, 9, 1936, 10.1093/oxfordjournals.humrep.a019520 Irvine, 1996, Evidence of deteriorating semen quality in the United Kingdom: birth cohort study in 577 men in Scotland over 11 years, BMJ, 312, 467, 10.1136/bmj.312.7029.467 Becker, 1997, A meta-analysis of 61 sperm count studies revised, Fertil Steril, 67, 1103, 10.1016/S0015-0282(97)81446-X Swan, 1997, Have sperm densities declined? A reanalysis of global trend data, Environ Health Perspect, 105, 1228, 10.1289/ehp.971051228 Swan, 2000, The question of declining sperm density revisited: an analysis of 101 studies published 1934-1996, Environ Health Perspect, 108, 961, 10.1289/ehp.00108961 Aitken, 2004, Seeds of concern, Nature, 432, 48, 10.1038/432048a Skakkebaek, 2001, Testicular dysgenesis syndrome: an increasingly common developmental disorder with environmental aspects, Hum Reprod, 16, 972, 10.1093/humrep/16.5.972 Skakkebaek, 2006, Is human fecundity declining?, Int J Androl, 29, 2, 10.1111/j.1365-2605.2005.00573.x Jorgensen, 2006, Coordinated European investigations of semen quality: results from studies of Scandinavian young men are a matter of concern, Int J Androl, 29, 54, 10.1111/j.1365-2605.2005.00635.x Hauser, 2006, The environment and male fertility: recent research on emerging chemicals and semen quality, Semin Reprod Med, 24, 156, 10.1055/s-2006-944422 Swan, 2006, Does our environment affect our fertility? Some examples to help reframe the question, Semin Reprod Med, 24, 142, 10.1055/s-2006-944420 Cox, 2006, Unidentified inert ingredients in pesticides: implications for human and environmental health, Environ Health Perspect, 114, 1803, 10.1289/ehp.9374 Surgan, 2005, Toxicity tests: “inert” and active ingredients, Environ Health Perspect, 113, 657, 10.1289/ehp.113-a657c Toppari, 1996, Male reproductive health and environmental xenoestrogens, Environ Health Perspect, 104, 741, 10.1289/ehp.96104s4741 Ramazzini, 2009, Collegium ramazzini statement on the control of pesticides in the European Union, a call for action to protect human health, Am J Ind Med, 52, 176, 10.1002/ajim.20654 Ribas-Fito, 2006, Silent Invaders: pesticides, livelihoods and women's health, London: ZED Books, 2002, Int J Epidemiol, 35, 504, 10.1093/ije/dyl029 Department of Agriculture and Cooperation, 2010 Kuhar, 1991, The dopamine hypothesis of the reinforcing properties of cocaine, Trends Neurosci, 14, 299, 10.1016/0166-2236(91)90141-G Corrigall, 1992, The mesolimbic dopamine system is implicated in the reinforcing effects of nicotine, Psychopharmacology, 107, 285, 10.1007/BF02245149 Murphy, 1998, Function of cannabinoid receptors in the neuroendocrine regulation of hormone secretion, Neurobiol Dis, 5, 432, 10.1006/nbdi.1998.0224 Di Chiara, 2000, Role of dopamine in the behavioural actions of nicotine related to addiction, Euro J Pharmacol, 393, 295, 10.1016/S0014-2999(00)00122-9 Watkins, 2000, Neural mechanisms underlying nicotine addiction: acute positive reinforcement and withdrawal, Nicotine Tob Res, 2, 19, 10.1080/14622200050011277 Melman, 1999, The epidemiology and pathophysiology of erectile dysfunction, J Urol, 161, 5 Dehkhargani, 2011, Detrimental effect of atrazine on testicular tissue and sperm quality: implication for oxidative stress and hormonal alterations, Iran J Toxicol, 5, 426 Sasidhar, 2014, Chronic experimental feeding of imidachloroprid induced oxidative stress and amelioration with vitamin C and Withania somnifera in layer birds, Int J Sci Enviorn Technol, 3, 1679 Clair, 2012, A glyphosate-based herbicide induces necrosis and apoptosis in mature rat testicular cells in vitro, and testosterone decrease at lower levels, Toxicol Vitro, 26, 269, 10.1016/j.tiv.2011.12.009 Slimani, 2011, Pesticide exposure and reproductive biomarkers among male farmers from north-east Algeria, Ann Biol Res, 2, 290 Spassova, 2000, Acute effects of acephate and metamidophos on acetylcholinesterase activity, endocrine system and amino acid concentration in rats, Comp Biochem Physiol C Toxicol Pharmacol, 126, 79 Lue, 2001, Physiology of penile erection and pathophysiology of erectile dysfunction and priapism, 1167 Pohanka, 2012, Acetylcholinesterase inhibitors; a patent review (2008–present), Expert Opin Ther Pat, 22, 871, 10.1517/13543776.2012.701620 Mitsushima, 1994, GABA is an inhibitory neurotransmitter restricting the release of luteinizing hormone-releasing hormone before the onset of puberty, Proc Nat Aca Sci U. S. A, 91, 395, 10.1073/pnas.91.1.395 Terasawa, 2001, Neurobiological mechanisms of the onset of puberty in primates, Endocr Rev, 22, 111 Elayan, 2013, The Effect of carbofuran on testosterone serum concentration and histological change of Leydig cell in mice, IOSR J Pharm Biol Sci (IOSR-JPBS), 7, 01, 10.9790/3008-0760104 Mandal, 2011, Correlation of testicular toxicity and oxidative stress induced by chlorpyrifos in rats, Hum Exp Toxicol, 30, 1529, 10.1177/0960327110392400 Zalba, 2000, Vascular oxidant stress: molecular mechanisms and pathophysiological implications, J Physiol Biochem, 56, 57, 10.1007/BF03179777 Bal, 2012, Insecticide imidacloprid induces morphological and DNA damage through oxidative toxicity on the reproductive organs of developing male rats, Cell Biochem Funct, 30, 492, 10.1002/cbf.2826 Beckman, 1996, Nitric oxide, superoxide, and peroxynitrite: the good, the bad, and ugly, Am J Physiol, 271, 1424, 10.1152/ajpcell.1996.271.5.C1424 Kojda, 1999, Interactions between NO and reactive oxygen species: pathophysiological importance in atherosclerosis, hypertension, diabetes and heart failure, Cardiovasc Res, 43, 562, 10.1016/S0008-6363(99)00169-8 Warnholtz, 1999, Increased NADH oxidasemediated superoxide production in the early stages of atherosclerosis: evidence for involvement of the renin-angiotensin system, Circulation, 99, 2027, 10.1161/01.CIR.99.15.2027 Hink, 2001, Mechanisms underlying endothelial dysfunction in diabetes mellitus, Circ Res, 88, 14, 10.1161/01.RES.88.2.e14 Jones, 2002, Oxygen free radicals and the penis, Expert Opin Pharm, 3, 889, 10.1517/14656566.3.7.889 Tsai, 1994, Role of conformation of peroxynitrite anion (ONOO-) with its stability and toxicity, J Am Chem Soc, 116, 4115, 10.1021/ja00088a072 Zou, 1997, Tyrosine nitration as a mechanism of selective inactivation of prostacyclin synthase by peroxynitrite, Biol Chem, 378, 707, 10.1515/bchm.1997.378.7.707 Khan, 2001, The effect of nitric oxide and peroxynitrite on rabbit cavernosal smooth muscle relaxation, World J Urol, 19, 220, 10.1007/s003450000162 Ermak, 2002, Calcium and oxidative stress: from cell signalling to cell death, Mol Immunol, 38, 713, 10.1016/S0161-5890(01)00108-0 Bustos, 2003, Effect of a single dose of malathion on spermatogenesis in mice, Asian J Androl, 5, 105 Narayana, 2006, An organophosphate insecticide methyl parathion (0-0- dimethyl 0-4-nitrophenylphosphorothioate) induces cytotoxic damage and tubular atrophy in the testis despite elevated testosterone level in rats, J Toxicol Sci, 31, 177, 10.2131/jts.31.177 Swart, 1991, Effect of Lead and organophosphates on sperm morphology, Syst Biol Reprod Med, 26, 67 Costa, 2009, The endothelial-erectile dysfunction connection: an essential update, J Sex Med, 6, 2390 Katusic, 1989, Superoxide anion is an endothelium derived contracting factor, Am J Physiol, 257, 33 Mills, 1996, Androgen and penile erection: a review, J Androl, 17, 633 Kavlock, 1996, Research needs for the risk assessment of health and environmental effects of endocrine disruptors: a report of the U.S. EPA-sponsored workshop, Environ Health Perspect, 104, 715, 10.1289/ehp.96104s4715 Environmental protection agency, 2007, Draft list of initial pesticide active ingredients and pesticide inerts to be considered for screening under the federal food, drug, and cosmetic act; extension of comment period, Fed Regist, 72, 33486 Romano, 2010, Prepubertal exposure to commercial formulation of the herbicide and decreased testosterone serum level at puberty alters testosterone levels and testicular morphology, Arch Toxicol, 84, 309, 10.1007/s00204-009-0494-z Dallegrave, 2007, Pre- and postnatal toxicity of the commercial glyphosate formulation in Wistar rats, Arch Toxicol, 81, 665, 10.1007/s00204-006-0170-5 Akingbemi, 2000, A metabolite of methoxychlor, 2,2-bis(p-hydroxyphenyl)-1,1, 1-trichloroethane, reduces testosterone biosynthesis in rat leydig cells through suppression of steady-state messenger ribonucleic acid levels of the cholesterol side-chain cleavage enzyme, Biol Reprod, 62, 571, 10.1095/biolreprod62.3.571 Institute of Science in Society. Glyphosate/Roundup & human male infertility. ISIS Report 19/03/14 [Online] Available at: http://www.i-sis.org.uk/Glyphosate_Roundup_and_Human_Male_Infertility.php. [Accessed on 10th November, 2014]. Afifi, 1991, Influence of on testicular and epididymal organs, testosterone, plasma level and their tissue residues in rats, Dtsch Tierarztl Wochenschr, 98, 419 Walsh, 2000, Roundup inhibits steroidogenesis by disrupting steroidogenic acute regulatory (StAR) protein expression, Environ Health Perspect, 108, 769, 10.1289/ehp.00108769 Chapin, 1990, The interaction of Sertoli and Leydig cells in the testicular toxicity of tri-o-cresyl phosphate, Toxicol Appl Pharmacol, 104, 483, 10.1016/0041-008X(90)90170-Y Padungtod, 1998, Reproductive hormone profile among pesticide factory workers, J Occup Environ Med, 40, 1038, 10.1097/00043764-199812000-00002 Ngoula, 2007, Effects of pirimiphos-methyl (an organophosphate insecticide) on the fertility of adult male rats, Afr Health Sci, 7, 3 Evamarie, 1999, Disruption of male sex hormones with regard to pesticides: pathophysiological and regulatory aspects, Toxicol Lett, 107, 225, 10.1016/S0378-4274(99)00051-X Zvara, 1995, Nitric oxide mediated erectile activity is a testosterone dependent event: a rat erection model, Int J Impot Res, 7, 209 Stuehr, 1999, Mammalian nitric oxide synthases, BBA-Bioenergetics, 1411, 217, 10.1016/S0005-2728(99)00016-X Forstermann, 1995, Isoforms of nitric oxide synthase, Biochem Pharmacol, 50, 1321, 10.1016/0006-2952(95)00181-6 Bansal, 2010, Garlic- potential substitute to synthetic aphrodisiacs for erectile dysfunction, J Pharm Res, 3, 3072 Masters, 1996, Neuronal nitric oxide synthase, a modular enzyme formed by convergent evolution: structure studies of a cysteine thiolate-liganded heme protein that hydroxylates L-arginine to produce NO as a cellular signal, FASEB J, 10, 552, 10.1096/fasebj.10.5.8621055 Burnett, 1993, Immuno histochemical localization of nitric oxide synthase in the autonomic innervation of the human penis, J Urol, 150, 73 Bush, 1992, Nitric oxide is a potent relaxant of human and rabbit corpus cavernosum, J Urol, 147, 1650 Ignarro, 1990, Nitric oxide and cyclic GMP formation upon electrical field stimulation cause relaxation of corpus cavernosum smooth muscle, Biochem Biophys Res Commun, 170, 843, 10.1016/0006-291X(90)92168-Y Holmquist, 1991, Effects of the nitric oxide synthase inhibitor NGnitro-L-arginine on the erectile response to cavernous nerve stimulation in the rabbit, Acta Physiol Scand, 143, 299, 10.1111/j.1748-1716.1991.tb09236.x Kim, 1991, A nitric oxide-like factor mediates nonadrenergicnoncholinergic neurogenic relaxation of penile corpus cavernosum smooth muscle, J Clin Invest, 88, 112, 10.1172/JCI115266 Burnett, 1992, Nitric oxide: a physiologic mediator of penile erection, Science, 257, 401, 10.1126/science.1378650 Rajifer, 1992, Nitric oxide as a mediator of relaxation of the corpus cavernosum in response to nonadrenergic, noncholinergic neurotransmission, N Engl J Med, 326, 90, 10.1056/NEJM199201093260203 Burnett, 1997, Nitric oxide in the penis: physiology and pathology, J Urol, 157, 320 Seftel, 1996, Nitric oxide relaxes rabbit corpus cavernosum smooth muscle via a potassium-conductive pathway, Biochem Biophys Res Commun, 219, 382, 10.1006/bbrc.1996.0242 Traish, 1999, Effects of castration and androgen replacement on erectile function in a rabbit model, Endocrinology, 140, 1861, 10.1210/endo.140.4.6655 Okamura, 1994, Colocalization of NADPH-diaphorase and estrogen receptor immunoreactivity in the rat ventromedial hypothalamic nucleus: stimulatory effects of estrogen on NADPH-diaphorase activity, Endocrinol, 135, 1705, 10.1210/endo.135.4.7925135 Pu, 1996, Evidence that gonadal steroids modulate nitric oxide efflux in the medial preoptic area: effects of N-methyl-Daspartate and correlation with Luteinizing hormone secretion, Endocrinol, 137, 1949, 10.1210/endo.137.5.8612535 Sullivan, 1999, Nitric oxide and penile erection: Is erectile dysfunction another manifestation of vascular disease?, Cardivasc Res, 43, 658, 10.1016/S0008-6363(99)00135-2 Boston University School of Medicine. Male genital anatomy. [Online] Available from: http://www.bumc.bu.edu/sexualmedicine/physicianinformation/male-genital-anatomy/[Accessed on 10th January, 2004]. Najafi, 2010, The effect of chronic exposure with imidacloprid insecticide on fertility in mature male rats, Int J Fertil Steril, 4, 9 Lacono, 1994, Microstructural disorders of tunica albuginea in patients affected by impotence, Eur Urol, 26, 233, 10.1159/000475386 Lacono, 1995, Scanning electron microscopy of the tunica albuginea of the corpora cavernosa in normal and impotent subjects, Urol Res, 23, 221, 10.1007/BF00393302 Shafik, 2007, On the pathogenesis of penile venous leakage: role of the tunica albuginea, BMC Urol, 7, 14, 10.1186/1471-2490-7-14 Zhang, 2011, Oxidative stress: role in acetamiprid-induced impairment of the male mice reproductive system, Agricul Sci China, 10, 786, 10.1016/S1671-2927(11)60063-1