Impaired reproductive function of male rats infected with Toxoplasma gondii
A. Abdoli
Department of Parasitology, Faculty of Medical Sciences, Tarbiat Modares University, Tehran, Iran
Search for more papers by this authorA. Dalimi
Department of Parasitology, Faculty of Medical Sciences, Tarbiat Modares University, Tehran, Iran
Search for more papers by this authorM. Movahedin
Department of Anatomy, Faculty of Medical Sciences, Tarbiat Modares University, Tehran, Iran
Search for more papers by this authorA. Abdoli
Department of Parasitology, Faculty of Medical Sciences, Tarbiat Modares University, Tehran, Iran
Search for more papers by this authorA. Dalimi
Department of Parasitology, Faculty of Medical Sciences, Tarbiat Modares University, Tehran, Iran
Search for more papers by this authorM. Movahedin
Department of Anatomy, Faculty of Medical Sciences, Tarbiat Modares University, Tehran, Iran
Search for more papers by this authorThis study was presented in 11th Royan International Congress on Reproductive Biomedicine, 15–17 September, 2010; Tehran, Iran.
Summary
Toxoplasmosis is one of the classical conditions known to have an adverse effect on female reproductive functions, but a few investigations into male reproductive parameters have been performed. This work was carried out to study the effects of Toxoplasma gondii on reproductive function in male rats. Male rats were infected with the RH strain of T. gondii tachyzoites, and following every 10 days from 10 to 70 postinfection (PI), the percentage of body weight to testis weight ratio as well as epididymal sperm parameters (number, motility, viability, and morphology rates), serum testosterone (ST), intratesticular testosterone (ITT), serum lactate dehydrogenase (SLDH), intratesticular lactate dehydrogenase and fructose in seminal vesicles and coagulating glands were measured. The results of the study showed sperm motility, viability and concentration rates were significantly decreased temporary after infection up to 70 days. Sperm abnormality was also increased during these days. In addition, temporary alteration in ST, ITT, SLDH, intratesticular LDH and fructose in seminal vesicle and coagulating gland was observed PI. These findings suggest that toxoplasmosis can cause impermanent impairment on the reproductive parameters of male rats.
References
- Adiga SK, Jagetia GC (1999) Effect of teniposide (Vm-26) on the cell survival, micronuclei induction and lactate dehydrogenase activity on V79 cells. Toxicology 138: 29–41.
- Arantes TP, Lopes ZWD, Ferreira RM, Pinto Pieroni JS, Pinto VMR, Sakamoto CA, da Costa AJ (2009) Toxoplasma gondii: evidence for the transmission by semen in dogs. Exp Parasitol 123: 190–194.
- Barreto F, Hering F, Dall’oglio MF, Martini Filho D, Campagnari JC, Srougi M (2008) Testicular toxoplasmosis: a rare case of testicular mass. Actas Urol Esp 32: 666–668.
- Bradford MM (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72: 248–254.
- Bustos-Obregon E, Esponda P, Sarabia L (2006) Effect of flutamide in mouse spermatogenesis and on the function of seminal vesicle and prostate. Int J Morphol 24: 171–174.
10.4067/S0717-95022006000300008 Google Scholar
- Carpino A, De Sanctis V, Siciliano L, Maggiolini M, Vivacqua A, Pinamonti A, Sisci D, Ando S (1997) Epididymal and sex accessory gland secretions in transfusion-dependent beta-thalassemic patients: evidence of an impaired prostatic function. Exp Clin Endocrinol Diabetes 105: 169–174.
- Crider SR, Horstman WG, Massey GS (1998) Toxoplasma orchitis: report of a case and a review of the literature. Am J Med 85: 421–424.
- Daryani A, Hosseini AZ, Dalimi A (2003) Immune responses against excreted/secreted antigens of Toxoplasma gondii tachyzoites in the murine model. Vet Parasitol 113: 123–134.
- De Lamirande E, Jiang H, Zini A, Kodama H, Gagnon C (1997) Reactive oxygen species and sperm physiology. Rev Reprod 2: 48–54.
- Decker T, Lohmann-Matthes ML (1988) A quick and simple method for the quantitation of lactate dehydrogenase release in measurements of cellular cytotoxicity and tumor necrosis factor (TNF) activity. J Immunol Methods 115: 61–69.
- Dubey JP (2010) Toxoplasmosis of Animals and Humans, 2nd edn. CRC Press, Boca Raton, FL, USA.
- Dubey JP, Frenkel Jk (1998) Toxoplasmosis of rats: a review, with considerations of their value as an animal model and their possible role in epidemiology. Vet Parasitol 77: 1–32.
- Dubey JP, Sharma SP (1980) Prolonged excretion of Toxoplasma gondii in semen of goats. Am J Vet Res 41: 794–795.
- Dubey JP, Shen SK, Kwok OCH, Frenkel JK (1999) Infection and immunity of the RH strain of Toxoplasma gondii in rats and mice. J Parasitol 85: 657–662.
- Flegr J, Lindova J, Kodym P (2008) Sex-dependent Toxoplasmosis-associated differences in testosterone concentration in humans. Parasitology 135: 427–431.
- Ganesh Kumar S, Narayana K, Bairy KL, D’Souza UJA, Paul Samuel P, Gopalakrishna K (2006) Dacarbazine induces genotoxic and cytotoxic germ cell damage with concomitant decrease in testosterone and increase in lactate dehydrogenase concentration in the testis. Mutat Res 607: 240–252.
- Garcia MF, Regadera J, Mayer R, Sanchez S, Nistal M (1996) Protozoan infections in the male genital tract. J Urol 156: 340–349.
- Haskel Ll, Fusco MJ, Ares L, Sublay B (1989) Case report: disseaminated Toxoplasmosis presenting as symptomatic orchitis and nephrotic syndrome. Am J Med Sci 298: 185–190.
- Janitschke K, Nurnberger F (1975) Studies on the significant of sexual intercourse for the transmission of Toxoplasma gondii (In German with English abstract). Zentralbl Bakteriol Orig A 231: 323–332.
- Jones J, Lopez A, Wils NM (2003) Congenital Toxoplasmosis. Am Fam Physician 67: 2131–2138.
- Lan-Chun W, Qiao Qing W, Zhang C (2008) Dynamic change of content of fructose in semen of male rabbits infected with Toxoplasma gondii (In Chinese with English abstract). J Xinxiang Med College 25: 73–76.
- Lecomte V, Chumpitazi BFF, Pasquier B, Ambroise-Thomas P, Santoro F (1992) Brain-tissue cysts in rats infected with the RH strain of Toxoplasma gondii. Parasitol Res 78: 267–269.
- Lewis-Jones DI, Aird IA, Biljan MM, Kingsland CR (1996) Effects of sperm activity on zinc and fructose concentration in seminal plasma. Hum Reprod 11: 2465–2467.
- Liu SG, Qin C, Yao Z, Wang D (2006) Study on the transmission of Toxoplasma gondii by semen in rabbits. Chin J Parasitol Parasit Dis 24: 166–170.
- Lopes WDZ, Costa AJ, Santana LF, dos Santos RS, Rossanese WM, Lopes WCZ, Costa GHN, Sakamoto CA, dos Santos TR (2009a) Aspects of Toxoplasma infection on the reproductive system of experimentally infected rams (Ovis aries). J Parasitol Res 2009:602803.
10.1155/2009/602803 Google Scholar
- Lopes WDZ, Costa AJ, Souza FA, Rodrigues JDF, Costa GHN, Soares VE, Silva GS (2009b) Semen variables of sheep (Ovis aries) experimentally infected with Toxoplasma gondii. Anim Reprod Sci 111: 312–319.
- Lu J, Chen F, Xu HR, Huang Y, Lu N (2007) Standardization and quality control for determination of fructose in seminal plasma. J Androl 28: 207–213.
- Manivannan B, Bhande SS, Panneerdoss S, Sriram S, Lohiya NK (2005) Safety evaluation of long-term vas occlusion with styrene maleic anhydride and its non-invasive reversal on accessory reproductive organs in langurs. Asian J Androl 7: 195–204.
- Miller CM, Boulter NR, Ikin RJ, Smith NC (2009) The immunobiology of the innate response to Toxoplasma gondii. Int J Parasitol 39: 23–39.
- Mosher WD, Pratt WF (1991) Fecundity and infertility in the United States: incidence and trends. (Editorial) Fertil Steril 56: 192–193.
- Moura AB, Costa AJ, Filho SJ, Paim BB, Pinto FR, Di Mauro DC (2007) Toxoplasma gondii in semen of experimentally infected swine. Pesq Vet Bras 27: 430–434.
- Nouri SH, Azarmi Y, Movahedin M (2009) Effect of growth hormone on testicular dysfunction induced by methotrexate in rats. Andrologia 41: 105–110.
- Oktenli C, Doganci L, Ozgurtas T, Araz RE, Tanyuksel M, Musabak U, Sanisoglu SY, Yesilova Z, Erbil MK, Inal A (2004) Transient hypogonadotrophic hypogonadism in males with acute Toxoplasmosis: suppressive effect of interleukin-1b on the secretion of GnRH. Human Reprod 19: 859–866.
- Patton PE, Battaglia DE (2005) Office Andrology. Humana Press Inc., Totowa, NJ, USA.
10.1007/978-1-59259-876-2 Google Scholar
- Pellati D, Mylonakis I, Bertoloni G, Fiore C, Andrisani A, Ambrosini G, Armanini D (2008) Genital tract infections and infertility. Eur J Obstet Gynecol Reprod Biol 140: 3–11.
- Prandota J (2010) Neuropathological changes and clinical features of autism spectrum disorder participants are similar to that reported in congenital and chronic cerebral Toxoplasmosis in humans and mice. Res Autism Spectr Disord 4: 103–118.
- Rui Y, Qiang X, Mingzhe J (2009) Effect of abnormal gonadal hormone secretion caused by Toxoplasma gondii in male fertility descent (In Chinese with English abstract). Mod Prev Med 36: 4130–4132.
- Sanocka D, Kurpisz M (2004) Reactive oxygen species and sperm cells. Reprod Biol Endocrinol 2: 12. Available at: http://www.rbej.com/content/2/1/12.
- Santana NMA, Paniaqua R, Palacios J (1986) Testicular Toxoplasmosis in two men with the acquired immune deficiency syndrome. Arch Pathol Lab Med 110: 744–746.
- Santana LF, da Costa AJ, Pieroni J, Lopes WDZ, Santos RS, de Oliveira GP, de Mendonça RP, Sakamoto CAM (2010) Detection of Toxoplasma gondii in the reproductive system of male goats. Rev Bras Parasitol Vet 19: 179–182.
- Scarpelli L, Lopes WDZ, Migani M, Bresciani KDS, Costa AJ (2009) Toxoplasma gondii in experimentally infected Bos taurus and Bos indicus semen and tissues. Pesq Vet Bras 29: 59–64.
- Schoenfeld C, Amelar RD, Dubin L, Numeroff M (1979) Prolactin, fructose, and zinc levels found in human seminal plasma. Fertil Steril 32: 206–208.
- Seed J, Chapin RE, Clegg ED, Dostal LA, Foote RH, Hurtt ME, Klinefelter GR, Makris SL, Perreault AD, Schrader S, Seyler D, Sprando R, Treinen KA, Rao Veeramachaneni DN, David Weise L (1996) Method for assessing sperm motility, morphology, and count in the rat, rabbit and dog: a consensus report. Reprod Toxicol 10: 237–244.
- Sharma RK, Agarwal A (1996) Role of reactive oxygen species in male infertility. Urology 48: 835–850.
- Shen L (2001) Pathology and pathogenetic study of the Toxoplasma gondii acute infection mice testis (In Chinese with English abstract). Chin J Zoonoses 17: 75–77.
- Sun LH, Fan F, Wang JJ, Gong J (2008) Acute Toxoplasma gondii infection affects the reproductive function of male mice (In Chinese with English abstract). Zhonghua Nan Ke Xue 14: 55–57.
- Suresh Babu PS, Nagendra K, Sarfaraz Navaz R, Ravindranath HM (2007) Congenital Toxoplasmosis presenting as hypogonadotropic hypogonadism. Indian J Pediatr 47: 577–579.
- Suzuki N, Piekarski G, Janssen P, Viswanathan R (1971) Biochemical observations of blood of rat Infected with Toxoplasma gondii. Res Bull Obihiro Univ 7: 15–25.
- Teale AJ, Blewett DA, Miller JK (1982) Experimentally induced toxoplasmosis in young rams: the clinical syndrome and semen secretion of Toxoplasma. Vet Rec 111: 53–55.
- Terpsidis KI, Papazahariadou MG, Taitzoglou IA, Papaioannou NG, Georgiadis MP, Theodoridis IT (2009) Toxoplasma gondii: reproductive parameters in experimentally infected male rats. Exp Parasitol 121: 238–241.
- Torrey EF, Yolken RH (2003) Toxoplasma gondii and schizophrenia. Emerg Infect Dis 9: 1375–1380.
- Vijay P, Yeshwanth R, Bairy KL (2008) The effect of sodium valproate on the biochemical parameters of reproductive function in male albino wistar rats. Indian J Pharmacol 40: 248–250.
- Voller A, Bidwell DE, Bartlett A, Fleck DG, Perkins M, Oldehin BA (1976) Microplate enzyme-immunoassay for Toxoplasma antibody. J Clin Pathol 29: 150–153.
- Weiss LM, Dubey JP (2009) Toxoplasmosis: a history of clinical observations. Int J Parasitol 39: 895–901.
- World Health Organization (2010) WHO Laboratory Manual for the Examination and Processing of Human Semen, 5th edn. WHO Press, Geneva, Switzerland.
- Xavier de Moraes EPB, Batista AM, Faria EB, Freire RL, Freitas AC, Ramos Silva MA, Braga VA, Mota RA (2010) Experimental infection by Toxoplasma gondii using contaminated semen containing different doses of tachyzoites in sheep. Vet Parasitol 170: 318–322.
- Xiangcai W, Wei Y, PinLe C, JiaMing Z (2000) The clinical experimental analysis of Toxoplasma gondii infection in the genital tract by polymerase chain reaction (In Chinese with English abstract). Chin J Zoonos 16: 70–72.
- Zhou YH, Lu J, Wang RB, Song LM, Shi F, Gao QF, Luo YF, Gu XF, Wang P (2002) Survey of infection of Toxoplasma gondii in infertile couples in Suzhou countryside (In Chinese with English abstract). Zhonghua Nan Ke Xue 8: 350–352.
- Zhou YH, Lu YJ, Wang R, Gao QF, Song L, Shi F, Luoya F, Gu F, Wang B (2003) Relations between anti-Toxoplasma IgG antibody in seminal plasma and NO level in infertile patients (In Chinese with English abstract). Chin J Zoonos 19: 98–100.
- Zhou YH, Shi H, Hu Y, Lu Y, Zhong X, Wang R, Gao Q, Shu Z (2004) Study on the damages on the reproductive system of male rats induced by Toxoplasma gondii infection and its regulatory mechanism (In Chinese with English abstract). Chin J Zoonos 20: 989–993.
- Zhou YH, Lu YJ, Diao YH, Xue R, Gao QF, Wang R, Shi F (2005) Study on correlation of semen anti-Toxoplasma IgG antibody with seminal quality and sperm motility in infertile males (In Chinese with English abstract). Chin J Schistosom Control 17: 45–48.
- Zhou YH, Fan H, Gao Q, Wang R (2007) Study on influence of Toxoplasma tachyzoites on human sperm motility parameters in vitro (In Chinese with English abstract). Chin J Schistosom Control 19: 43–45.