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Erschienen in: Journal of Parasitic Diseases 1/2019

20.11.2018 | Original Article

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

verfasst von: Farideh Esfandiari, Bahador Sarkari, Habibollah Turki, Nasir Arefkhah, Najme Shakouri

Erschienen in: Journal of Parasitic Diseases | Ausgabe 1/2019

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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.
Literatur
Zurück zum Zitat 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):349–355 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):349–355
Zurück zum Zitat 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):e35671CrossRefPubMedPubMedCentral 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):e35671CrossRefPubMedPubMedCentral
Zurück zum Zitat 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):548–554CrossRefPubMed 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):548–554CrossRefPubMed
Zurück zum Zitat 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):407–413CrossRefPubMed 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):407–413CrossRefPubMed
Zurück zum Zitat 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):275–281CrossRefPubMed 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):275–281CrossRefPubMed
Zurück zum Zitat 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–S113CrossRefPubMed 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–S113CrossRefPubMed
Zurück zum Zitat Bouman A, Heineman MJ, Faas MM (2005) Sex hormones and the immune response in humans. Hum Reprod Update 11(4):411–423CrossRefPubMed Bouman A, Heineman MJ, Faas MM (2005) Sex hormones and the immune response in humans. Hum Reprod Update 11(4):411–423CrossRefPubMed
Zurück zum Zitat 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):3190–3203CrossRefPubMedPubMedCentral 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):3190–3203CrossRefPubMedPubMedCentral
Zurück zum Zitat 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):193–198CrossRefPubMed 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):193–198CrossRefPubMed
Zurück zum Zitat Daily JP (2017) Malaria 2017: update on the clinical literature and management. Curr Infect Dis Rep 19(8):28CrossRefPubMed Daily JP (2017) Malaria 2017: update on the clinical literature and management. Curr Infect Dis Rep 19(8):28CrossRefPubMed
Zurück zum Zitat 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):377–382CrossRefPubMed 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):377–382CrossRefPubMed
Zurück zum Zitat 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):588–593CrossRefPubMed 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):588–593CrossRefPubMed
Zurück zum Zitat 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):71–75PubMed 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):71–75PubMed
Zurück zum Zitat 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 2017:6816913PubMedPubMedCentral 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 2017:6816913PubMedPubMedCentral
Zurück zum Zitat Folstad I, Karter AJ (1992) Parasites, bright males, and the immunocompetence handicap. Am Nat 139(3):603–622CrossRef Folstad I, Karter AJ (1992) Parasites, bright males, and the immunocompetence handicap. Am Nat 139(3):603–622CrossRef
Zurück zum Zitat Ghazeeri G, Abdullah L, Abbas O (2011) Immunological differences in women compared with men: overview and contributing factors. Am J Reprod Immunol 66(3):163–169CrossRefPubMed Ghazeeri G, Abdullah L, Abbas O (2011) Immunological differences in women compared with men: overview and contributing factors. Am J Reprod Immunol 66(3):163–169CrossRefPubMed
Zurück zum Zitat 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):309–321CrossRefPubMedPubMedCentral 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):309–321CrossRefPubMedPubMedCentral
Zurück zum Zitat 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 2015:174570PubMedPubMedCentral 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 2015:174570PubMedPubMedCentral
Zurück zum Zitat 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 12:378CrossRefPubMedPubMedCentral 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 12:378CrossRefPubMedPubMedCentral
Zurück zum Zitat Klein S (2004) Hormonal and immunological mechanisms mediating sex differences in parasite infection. Parasite Immunol 26(6–7):247–264CrossRefPubMed Klein S (2004) Hormonal and immunological mechanisms mediating sex differences in parasite infection. Parasite Immunol 26(6–7):247–264CrossRefPubMed
Zurück zum Zitat 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):423–433CrossRefPubMedPubMedCentral 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):423–433CrossRefPubMedPubMedCentral
Zurück zum Zitat 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):123–128CrossRefPubMedPubMedCentral 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):123–128CrossRefPubMedPubMedCentral
Zurück zum Zitat 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):2659–2669CrossRefPubMed 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):2659–2669CrossRefPubMed
Zurück zum Zitat 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):210–211CrossRefPubMed 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):210–211CrossRefPubMed
Zurück zum Zitat 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):e55694CrossRefPubMedPubMedCentral 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):e55694CrossRefPubMedPubMedCentral
Zurück zum Zitat 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 2014:935469CrossRefPubMedPubMedCentral 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 2014:935469CrossRefPubMedPubMedCentral
Zurück zum Zitat Muñoz G, Davies CR (2006) Leishmania panamensis transmission in the domestic environment: the results of a prospective epidemiological survey in Santander, Colombia. Biomedica 26:131–144CrossRefPubMed Muñoz G, Davies CR (2006) Leishmania panamensis transmission in the domestic environment: the results of a prospective epidemiological survey in Santander, Colombia. Biomedica 26:131–144CrossRefPubMed
Zurück zum Zitat 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):46CrossRef 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):46CrossRef
Zurück zum Zitat 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):502–508PubMed 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):502–508PubMed
Zurück zum Zitat Reithinger R, Mohsen M, Aadil K, Sidiqi M, Erasmus P, Coleman PG (2003) Anthroponotic cutaneous leishmaniasis, Kabul, Afghanistan. Emerg Infect Dis 9(6):727CrossRefPubMedPubMedCentral Reithinger R, Mohsen M, Aadil K, Sidiqi M, Erasmus P, Coleman PG (2003) Anthroponotic cutaneous leishmaniasis, Kabul, Afghanistan. Emerg Infect Dis 9(6):727CrossRefPubMedPubMedCentral
Zurück zum Zitat Robinson DP, Klein SL (2012) Pregnancy and pregnancy-associated hormones alter immune responses and disease pathogenesis. Horm Behav 62(3):263–271CrossRefPubMedPubMedCentral Robinson DP, Klein SL (2012) Pregnancy and pregnancy-associated hormones alter immune responses and disease pathogenesis. Horm Behav 62(3):263–271CrossRefPubMedPubMedCentral
Zurück zum Zitat 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):1133–1136CrossRefPubMed 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):1133–1136CrossRefPubMed
Zurück zum Zitat Sarkari B, Hatam G, Ghatee M (2012) Epidemiological features of visceral leishmaniasis in fars province, southern iran. Iran J Public Health 41(4):94–99PubMedPubMedCentral Sarkari B, Hatam G, Ghatee M (2012) Epidemiological features of visceral leishmaniasis in fars province, southern iran. Iran J Public Health 41(4):94–99PubMedPubMedCentral
Zurück zum Zitat 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):209–216PubMed 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):209–216PubMed
Zurück zum Zitat 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):e0150406CrossRefPubMedPubMedCentral 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):e0150406CrossRefPubMedPubMedCentral
Zurück zum Zitat Snider H, Lezama-Davila C, Alexander J, Satoskar AR (2009) Sex hormones and modulation of immunity against leishmaniasis. NeuroImmunoModulation 16(2):106–113CrossRefPubMed Snider H, Lezama-Davila C, Alexander J, Satoskar AR (2009) Sex hormones and modulation of immunity against leishmaniasis. NeuroImmunoModulation 16(2):106–113CrossRefPubMed
Zurück zum Zitat 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):2288–2296CrossRefPubMedPubMedCentral 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):2288–2296CrossRefPubMedPubMedCentral
Zurück zum Zitat 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):357–367CrossRefPubMed 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):357–367CrossRefPubMed
Metadaten
Titel
Level of circulating steroid hormones in malaria and cutaneous leishmaniasis: a case control study
verfasst von
Farideh Esfandiari
Bahador Sarkari
Habibollah Turki
Nasir Arefkhah
Najme Shakouri
Publikationsdatum
20.11.2018
Verlag
Springer India
Erschienen in
Journal of Parasitic Diseases / Ausgabe 1/2019
Print ISSN: 0971-7196
Elektronische ISSN: 0975-0703
DOI
https://doi.org/10.1007/s12639-018-1055-2

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