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Level of circulating steroid hormones in malaria and cutaneous leishmaniasis: a case control study

  • Farideh Esfandiari
  • Bahador SarkariEmail author
  • Habibollah Turki
  • Nasir Arefkhah
  • Najme Shakouri
Original Article
  • 5 Downloads

Abstract

Epidemiological and clinical studies have shown a great difference in the severity and prevalence of infectious diseases in men and women and various studies have shown that the key immunological factors are affected by sex-associated hormones. Considering the role of sex hormones in various infections, the current study aimed to determine the level of sex hormones in patients with cutaneous leishmaniasis (CL) and malaria and compare it with those of healthy controls. The survey was designed as a case–control study. Peripheral blood was collected from thirty male malaria patients, sixty patients (equal number of both sexes) with cutaneous leishmaniasis and ninety healthy subjects. Disease confirmations were done through microscopic examination of either peripheral blood smears, in case of malaria, or Giemsa-stained lesion imprint slides for CL. The level of testosterone, progesterone and estrogen were measured in malaria and CL patients along with healthy subjects, using an ELISA commercial kit. Age of participants was 18–35 years (mean 25.39 ± 4.70) for CL patients and 14–41 years (mean 27.63 ± 9.09) for malaria patients. Differences between the age of patients and the healthy subjects were insignificant. The level of testosterone in malaria patients (1.44 ± 0.12 ng/mL) was lower than control group (1.46 ± 0.06, ng/mL) but the differences were not statistically significant (p > .05). The concentration of testosterone in CL patients (1.49 ± 0.03 ng/mL) was higher than those of control group (1.46 ± 0.06 ng/mL), and the difference was statistically significant (p  = 0.05). Although the concentration of estrogen and progesterone in CL patients were lower than controls, still the differences were not statistically significant (p > 0.05). Findings of the current study demonstrated a significant difference in the serum level of testosterone in CL patients in comparison with the healthy subjects whereas such difference was not seen in malaria patients.

Keywords

Steroid hormones Malaria Cutaneous leishmaniasis 

Notes

Acknowledgements

The results described in this paper were part of MD thesis of Najme Shakouri. The study was financially supported by the office of vice-chancellor for research of Shiraz University of Medical Sciences (Grant No. 94-01-43-9603).

References

  1. Abdagalil MA, ElBagir NM (2009) Effect of falciparum malaria on some plasma proteins in males: with special reference to the levels of testosterone and cortisol. Afr J Biochem Res 3(11):349–355Google Scholar
  2. Alvar J, Vélez ID, Bern C, Herrero M, Desjeux P, Cano J, Jannin J, den Boer M, Team WLC (2012) Leishmaniasis worldwide and global estimates of its incidence. PLoS ONE 7(5):e35671CrossRefGoogle Scholar
  3. Baccan GC, Oliveira F, Sousa AD, Cerqueira NA, Costa JML, Barral-Netto M, Barral A (2011) Hormone levels are associated with clinical markers and cytokine levels in human localized cutaneous leishmaniasis. Brain Behav Immun 25(3):548–554CrossRefGoogle Scholar
  4. Benten W, Wunderlich F, Mossmann H (1992) Testosterone-induced suppression of self-healing Plasmodium chabaudi malaria: an effect not mediated by androgen receptors? J Endocrinol 135(3):407–413CrossRefGoogle Scholar
  5. Benten W, Ulrich P, Kühn-Velten W, Vohr H, Wunderlich F (1997) Testosterone-induced susceptibility to Plasmodium chabaudi malaria: persistence after withdrawal of testosterone. J Endocrinol 153(2):275–281CrossRefGoogle Scholar
  6. Bernin H, Lotter H (2014) Sex bias in the outcome of human tropical infectious diseases: influence of steroid hormones. J Infect Dis 209(suppl_3):S107–S113CrossRefGoogle Scholar
  7. Bouman A, Heineman MJ, Faas MM (2005) Sex hormones and the immune response in humans. Hum Reprod Update 11(4):411–423CrossRefGoogle Scholar
  8. Cernetich A, Garver LS, Jedlicka AE, Klein PW, Kumar N, Scott AL, Klein SL (2006) Involvement of gonadal steroids and gamma interferon in sex differences in response to blood-stage malaria infection. Infect Immun 74(6):3190–3203CrossRefGoogle Scholar
  9. Cutolo M, Villaggio B, Seriolo B, Montagna P, Capellino S, Straub RH, Sulli A (2004) Synovial fluid estrogens in rheumatoid arthritis. Autoimmun Rev 3(3):193–198CrossRefGoogle Scholar
  10. Daily JP (2017) Malaria 2017: update on the clinical literature and management. Curr Infect Dis Rep 19(8):28CrossRefGoogle Scholar
  11. Davami MH, Motazedian MH, Sarkari B (2010) The changing profile of cutaneous leishmaniasis in a focus of the disease in Jahrom district, southern Iran. Ann Trop Med Parasitol 104(5):377–382CrossRefGoogle Scholar
  12. Escobedo G, Roberts CW, Carrero JC, Morales-Montor J (2005) Parasite regulation by host hormones: an old mechanism of host exploitation? Trends Parasitol 21(12):588–593CrossRefGoogle Scholar
  13. Faust Z, Laškarin G, Rukavina D, Szekeres-Bartho J (1999) Progesterone-induced blocking factor inhibits degranulation of natural killer cells. Am J Reprod Immunol 42(2):71–75PubMedGoogle Scholar
  14. Ferede G, Diro E (2017) Visceral leishmaniasis-malaria coinfection and their associated factors in patients attending metema hospital, Northwest Ethiopia: suggestion for integrated vector management. Malar Res Treat 2017:6816913PubMedPubMedCentralGoogle Scholar
  15. Folstad I, Karter AJ (1992) Parasites, bright males, and the immunocompetence handicap. Am Nat 139(3):603–622CrossRefGoogle Scholar
  16. Ghazeeri G, Abdullah L, Abbas O (2011) Immunological differences in women compared with men: overview and contributing factors. Am J Reprod Immunol 66(3):163–169CrossRefGoogle Scholar
  17. Giefing-Kröll C, Berger P, Lepperdinger G, Grubeck-Loebenstein B (2015) How sex and age affect immune responses, susceptibility to infections, and response to vaccination. Aging Cell 14(3):309–321CrossRefGoogle Scholar
  18. Hatam GR, Nejati F, Mohammadzadeh T, Shahriari Rad R, Sarkari B (2015) Population-based seroprevalence of malaria in Hormozgan Province, Southeastern Iran: a low transmission area. Malar Res Treat 2015:174570PubMedPubMedCentralGoogle Scholar
  19. Khosravani A, Sarkari B, Negahban H, Sharifi A, Toori MA, Eilami O (2012) Hepatitis B Infection among high risk population: a seroepidemiological survey in Southwest of Iran. BMC Infect Dis 12:378CrossRefGoogle Scholar
  20. Klein S (2004) Hormonal and immunological mechanisms mediating sex differences in parasite infection. Parasite Immunol 26(6–7):247–264CrossRefGoogle Scholar
  21. Klein PW, Easterbrook JD, Lalime EN, Klein SL (2008) Estrogen and progesterone affect responses to malaria infection in female C57BL/6 mice. Gend Med 5(4):423–433CrossRefGoogle Scholar
  22. Kurtis JD, Mtalib R, Onyango FK, Duffy PE (2001) Human resistance to Plasmodium falciparum increases during puberty and is predicted by dehydroepiandrosterone sulfate levels. Infect Immun 69(1):123–128CrossRefGoogle Scholar
  23. Legorreta-Herrera M, Mosqueda-Romo NA, Nava-Castro KE, Morales-Rodríguez AL, Buendía-González FO, Morales-Montor J (2015) Sex hormones modulate the immune response to Plasmodium berghei ANKA in CBA/Ca mice. Parasitol Res 114(7):2659–2669CrossRefGoogle Scholar
  24. Lezama-Davila C, Oghumu S, Satoskar A, Isaac-Marquez A (2007) Sex-associated susceptibility in humans with chiclero’s ulcer: resistance in females is associated with increased serum-levels of GM-CSF. Scand J Immunol 65(2):210–211CrossRefGoogle Scholar
  25. Lotter H, Helk E, Bernin H, Jacobs T, Prehn C, Adamski J, Gonzalez-Roldan N, Holst O, Tannich E (2013) Testosterone increases susceptibility to amebic liver abscess in mice and mediates inhibition of IFNgamma secretion in natural killer T cells. PLoS ONE 8(2):e55694CrossRefGoogle Scholar
  26. Mohammadzadeh T, Hatam G, Kalantari M, Sarkari B, Motazedian MH, Sadjjadi SM, Safari R (2014) Molecular and microscopic-based characterization of Plasmodium spp. in Fars and Hormozgan Provinces, South of Iran. J Trop Med 2014:935469CrossRefGoogle Scholar
  27. Muñoz G, Davies CR (2006) Leishmania panamensis transmission in the domestic environment: the results of a prospective epidemiological survey in Santander, Colombia. Biomedica 26:131–144CrossRefGoogle Scholar
  28. Pandey K, Singh D, Bimal S, Murti K, Das P (2014) Association of testosterone and cholesterol level in modulation of immunity and severity of disease in visceral leishmaniasis patients-a preliminary study. Am J Immunol 10(1):46CrossRefGoogle Scholar
  29. Pourmohammadi B, Motazedian MH, Handjani F, Hatam GH, Habibi S, Sarkari B (2011) Glucantime efficacy in the treatment of zoonotic cutaneous leishmaniasis. Southeast Asian J Trop Med Public Health 42(3):502–508PubMedGoogle Scholar
  30. Reithinger R, Mohsen M, Aadil K, Sidiqi M, Erasmus P, Coleman PG (2003) Anthroponotic cutaneous leishmaniasis, Kabul, Afghanistan. Emerg Infect Dis 9(6):727CrossRefGoogle Scholar
  31. Robinson DP, Klein SL (2012) Pregnancy and pregnancy-associated hormones alter immune responses and disease pathogenesis. Horm Behav 62(3):263–271CrossRefGoogle Scholar
  32. Sarkari B, Pedram N, Mohebali M, Moshfe AA, Zargar MA, Akhoundi B, Shirzadi MR (2010) Seroepidemiological study of visceral leishmaniasis in Booyerahmad district, south-west Islamic Republic of Iran. East Mediterr Health J 16(11):1133–1136CrossRefGoogle Scholar
  33. Sarkari B, Hatam G, Ghatee M (2012) Epidemiological features of visceral leishmaniasis in fars province, southern iran. Iran J Public Health 41(4):94–99PubMedPubMedCentralGoogle Scholar
  34. Sarkari B, Ahmadpour NB, Motazedian MH, Mirjalali H, Akhoundi M, Mohebali M, Hajjaran H (2016a) Inter- and intraspecific variations of leishmania strains isolated from patients with cutaneous and visceral leishmaniases in Fars Province, South of Iran. Iran J Med Sci 41(3):209–216PubMedGoogle Scholar
  35. Sarkari B, Naraki T, Ghatee MA, Abdolahi Khabisi S, Davami MH (2016b) Visceral leishmaniasis in southwestern Iran: a retrospective clinico-hematological analysis of 380 consecutive hospitalized cases (1999–2014). PLoS ONE 11(3):e0150406CrossRefGoogle Scholar
  36. Snider H, Lezama-Davila C, Alexander J, Satoskar AR (2009) Sex hormones and modulation of immunity against leishmaniasis. NeuroImmunoModulation 16(2):106–113CrossRefGoogle Scholar
  37. Travi BL, Osorio Y, Melby PC, Chandrasekar B, Arteaga L, Saravia NG (2002) Gender is a major determinant of the clinical evolution and immune response in hamsters infected with Leishmania spp. Infect Immun 70(5):2288–2296CrossRefGoogle Scholar
  38. Wunderlich F, Marinovski P, Peter W, Benten M, Schmitt-Wrede HP, Mossmann H (1991) Testosterone and other gonadal factor (s) restrict the efficacy of genes controlling resistance to Plasmodium chabaudi malaria. Parasite Immunol 13(4):357–367CrossRefGoogle Scholar

Copyright information

© Indian Society for Parasitology 2018

Authors and Affiliations

  1. 1.Department of Parasitology and Mycology, School of MedicineShiraz University of Medical SciencesShirazIran
  2. 2.Basic Sciences in Infectious Diseases Research CenterShiraz University of Medical SciencesShirazIran
  3. 3.Infectious and Tropical Diseases Research Center, Hormozgan Health InstituteHormozgan University of Medical SciencesBandar AbbasIran

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