Skip to main content
Top
Published in: BMC Infectious Diseases 1/2019

Open Access 01-12-2019 | Toxoplasmosis | Research article

Opportunistic parasitoses among Egyptian hemodialysis patients in relation to CD4+ T-cell counts: a comparative study

Authors: Amany I. Shehata, Faika Hassanein, Rashad Abdul-Ghani

Published in: BMC Infectious Diseases | Issue 1/2019

Login to get access

Abstract

Background

Some reports are available on the prevalence of opportunistic parasitoses among hemodialysis (HD) patients, yet there is a paucity of data on the association of CD4+ T-cell counts with such infections. Therefore, this study aimed to determine the prevalence of intestinal parasites and Toxoplasma gondii in relation to CD4+ counts among HD patients in Alexandria, Egypt.

Methods

A comparative cross-sectional study was conducted on 120 HD patients and 100 apparently healthy individuals between December 2014 and January 2016. Data and samples (stool and blood) were collected from the participants after obtaining their informed consent. Stool samples were examined for parasites after concentration and staining, EDTA-blood samples were used for CD4+ counting by flow cytometry, and sera were analyzed for anti-Toxoplasma IgM and IgG antibodies.

Results

A significantly higher prevalence rate of intestinal parasitoses was found among HD patients compared to apparently healthy individuals (52.5% vs. 12.0%, respectively), with absence of helminths. Cryptosporidium species (32.5%), B. hominis(24.2%) and microsporidia (11.7%) were the most frequent parasites among HD patients, while B. hominis (13.0%), Cryptosporidium species (11.0%) and G. lamblia (4.0%) were the most frequent parasites among their counterparts. Statistically significant differences in parasite infection rates between patients and their counterparts were found for Cryptosporidium species, B. hominis and microsporidia. However, parasite species were not significantly associated with diarrhea. On the other hand, the overall T. gondii seroprevalence rate among HD patients was significantly higher than that among their counterparts (33.3% vs. 8%, respectively). HD patients with CD4+ counts < 200 cells/μl were twice more exposed to intestinal parasitoses compared to those with counts ≥200 cells/μl, but the difference was not statistically significant. However, low CD4+ counts were significantly associated with higher rates of Cryptosporidium species, microsporidia and T. gondii.

Conclusions

Intestinal parasitoses and T. gondii infection rates are significantly higher among Egyptian HD patients compared to apparently healthy individuals, with Cryptosporidium species, B. hominis, microsporidia and T. gondii being the most frequent parasites. CD4+ counts < 200 cells/μl are significantly associated with Cryptosporidium species, microsporidia and T. gondii among HD patients. Therefore, regular screening of HD patients for opportunistic parasites is recommended.
Literature
1.
go back to reference Girndt M, Sester U, Sester M, Kaul H, Kohler H. Impaired cellular immune function in patients with end-stage renal failure. Nephrol Dial Transplant. 1999;14(12):2807–10.PubMedCrossRef Girndt M, Sester U, Sester M, Kaul H, Kohler H. Impaired cellular immune function in patients with end-stage renal failure. Nephrol Dial Transplant. 1999;14(12):2807–10.PubMedCrossRef
2.
go back to reference Eleftheriadis T, Antoniadi G, Liakopoulos V, Kartsios C, Stefanidis I. Disturbances of acquired immunity in hemodialysis patients. Semin Dial. 2007;20(5):440–51.PubMedCrossRef Eleftheriadis T, Antoniadi G, Liakopoulos V, Kartsios C, Stefanidis I. Disturbances of acquired immunity in hemodialysis patients. Semin Dial. 2007;20(5):440–51.PubMedCrossRef
3.
go back to reference Meijers RW, Litjens NH, de Wit EA, Langerak AW, van der Spek A, Baan CC, et al. Uremia causes premature ageing of the T cell compartment in end-stage renal disease patients. Immun Ageing. 2012;9(1):19.PubMedPubMedCentralCrossRef Meijers RW, Litjens NH, de Wit EA, Langerak AW, van der Spek A, Baan CC, et al. Uremia causes premature ageing of the T cell compartment in end-stage renal disease patients. Immun Ageing. 2012;9(1):19.PubMedPubMedCentralCrossRef
4.
go back to reference Meijers RW, Betjes MG, Baan CC, Litjens NH. T-cell ageing in end-stage renal disease patients: assessment and clinical relevance. World J Nephrol. 2014;3(4):268–76.PubMedPubMedCentralCrossRef Meijers RW, Betjes MG, Baan CC, Litjens NH. T-cell ageing in end-stage renal disease patients: assessment and clinical relevance. World J Nephrol. 2014;3(4):268–76.PubMedPubMedCentralCrossRef
5.
go back to reference Tetta C, Camussi G, Turello E, Salomone M, Aimo G, Priolo G, et al. Production of cytokines in hemodialysis. Blood Purif. 1990;8(6):337–46.PubMedCrossRef Tetta C, Camussi G, Turello E, Salomone M, Aimo G, Priolo G, et al. Production of cytokines in hemodialysis. Blood Purif. 1990;8(6):337–46.PubMedCrossRef
6.
go back to reference Morita Y, Yamamura M, Kashihara N, Makino H. Increased production of interleukin-10 and inflammatory cytokines in blood monocytes of hemodialysis patients. Res Commun Mol Pathol Pharmacol. 1997;98(1):19–33.PubMed Morita Y, Yamamura M, Kashihara N, Makino H. Increased production of interleukin-10 and inflammatory cytokines in blood monocytes of hemodialysis patients. Res Commun Mol Pathol Pharmacol. 1997;98(1):19–33.PubMed
7.
go back to reference Muniz-Junqueira MI, Braga Lopes C, Magalhaes CA, Schleicher CC, Veiga JP. Acute and chronic influence of hemodialysis according to the membrane used on phagocytic function of neutrophils and monocytes and pro-inflammatory cytokines production in chronic renal failure patients. Life Sci. 2005;77(25):3141–55.PubMedCrossRef Muniz-Junqueira MI, Braga Lopes C, Magalhaes CA, Schleicher CC, Veiga JP. Acute and chronic influence of hemodialysis according to the membrane used on phagocytic function of neutrophils and monocytes and pro-inflammatory cytokines production in chronic renal failure patients. Life Sci. 2005;77(25):3141–55.PubMedCrossRef
8.
go back to reference Borges A, Borges M, Fernandes J, Nascimento H, Sameiro-Faria M, Miranda V, et al. Apoptosis of peripheral CD4(+) T-lymphocytes in end-stage renal disease patients under hemodialysis and rhEPO therapies. Ren Fail. 2011;33(2):138–43.PubMedCrossRef Borges A, Borges M, Fernandes J, Nascimento H, Sameiro-Faria M, Miranda V, et al. Apoptosis of peripheral CD4(+) T-lymphocytes in end-stage renal disease patients under hemodialysis and rhEPO therapies. Ren Fail. 2011;33(2):138–43.PubMedCrossRef
9.
go back to reference Akgul SU, Ciftci HS, Temurhan S, Caliskan Y, Bayraktar A, Tefik T, et al. Association between HLA antibodies and different sensitization events in renal transplant candidates. Transplant Proc. 2017;49(3):425–9.PubMedCrossRef Akgul SU, Ciftci HS, Temurhan S, Caliskan Y, Bayraktar A, Tefik T, et al. Association between HLA antibodies and different sensitization events in renal transplant candidates. Transplant Proc. 2017;49(3):425–9.PubMedCrossRef
10.
11.
go back to reference Mohammadi Manesh R, Hosseini Safa A, Sharafi SM, Jafari R, Bahadoran M, Yousefi M, et al. Parasites and chronic renal failure. J Renal Inj Prev. 2014;3(4):87–90.PubMedPubMedCentral Mohammadi Manesh R, Hosseini Safa A, Sharafi SM, Jafari R, Bahadoran M, Yousefi M, et al. Parasites and chronic renal failure. J Renal Inj Prev. 2014;3(4):87–90.PubMedPubMedCentral
12.
go back to reference Gil FF, Barros MJ, Macedo NA, Junior CG, Redoan R, Busatti H, et al. Prevalence of intestinal parasitism and associated symptomatology among hemodialysis patients. Rev Inst Med Trop Sao Paulo. 2013;55(2):69–74.PubMedCrossRef Gil FF, Barros MJ, Macedo NA, Junior CG, Redoan R, Busatti H, et al. Prevalence of intestinal parasitism and associated symptomatology among hemodialysis patients. Rev Inst Med Trop Sao Paulo. 2013;55(2):69–74.PubMedCrossRef
13.
go back to reference Omrani VF, Fallahi S, Rostami A, Siyadatpanah A, Barzgarpour G, Mehravar S, et al. Prevalence of intestinal parasite infections and associated clinical symptoms among patients with end-stage renal disease undergoing hemodialysis. Infection. 2015;43(5):537–44.PubMedCrossRef Omrani VF, Fallahi S, Rostami A, Siyadatpanah A, Barzgarpour G, Mehravar S, et al. Prevalence of intestinal parasite infections and associated clinical symptoms among patients with end-stage renal disease undergoing hemodialysis. Infection. 2015;43(5):537–44.PubMedCrossRef
14.
go back to reference Evering T, Weiss LM. The immunology of parasite infections in immunocompromised hosts. Parasite Immunol. 2006;28(11):549–65.PubMedPubMedCentral Evering T, Weiss LM. The immunology of parasite infections in immunocompromised hosts. Parasite Immunol. 2006;28(11):549–65.PubMedPubMedCentral
15.
go back to reference El-Arbagy AR, Yassin YS, Boshra BN. Study of prevalence of end-stage renal disease in Assiut governorate, upper Egypt. Menoufia Med J. 2016;29:222–7.CrossRef El-Arbagy AR, Yassin YS, Boshra BN. Study of prevalence of end-stage renal disease in Assiut governorate, upper Egypt. Menoufia Med J. 2016;29:222–7.CrossRef
16.
go back to reference El-Kady AM, Fahmi Y, Tolba M, Hashim AA, Hassan AA. Cryptosporidium infection in chronic kidney disease patients undergoing hemodialysis in Egypt. J Parasit Dis. 2018;42(4):630–5.PubMedCrossRef El-Kady AM, Fahmi Y, Tolba M, Hashim AA, Hassan AA. Cryptosporidium infection in chronic kidney disease patients undergoing hemodialysis in Egypt. J Parasit Dis. 2018;42(4):630–5.PubMedCrossRef
17.
go back to reference Hamza H, El-Taweel H, Abou-Holw S, Khalil S, Wagdy E. Toxoplasma gondii seropositivity in renal patients: rate, pattern, predictors and related morbidity. J Egypt Soc Parasitol. 2015;45(1):7–15.PubMedCrossRef Hamza H, El-Taweel H, Abou-Holw S, Khalil S, Wagdy E. Toxoplasma gondii seropositivity in renal patients: rate, pattern, predictors and related morbidity. J Egypt Soc Parasitol. 2015;45(1):7–15.PubMedCrossRef
18.
go back to reference Ali MS, Mahmoud LA, Abaza BE, Ramadan MA. Intestinal spore-forming protozoa among patients suffering from chronic renal failure. J Egypt Soc Parasitol. 2000;30(1):93–100.PubMed Ali MS, Mahmoud LA, Abaza BE, Ramadan MA. Intestinal spore-forming protozoa among patients suffering from chronic renal failure. J Egypt Soc Parasitol. 2000;30(1):93–100.PubMed
20.
go back to reference Moura H, Schwartz DA, Bornay-Llinares F, Sodre FC, Wallace S, Visvesvara GS. A new and improved “quick-hot gram-chromotrope” technique that differentially stains microsporidian spores in clinical samples, including paraffin-embedded tissue sections. Arch Pathol Lab Med. 1997;121(8):888–93.PubMed Moura H, Schwartz DA, Bornay-Llinares F, Sodre FC, Wallace S, Visvesvara GS. A new and improved “quick-hot gram-chromotrope” technique that differentially stains microsporidian spores in clinical samples, including paraffin-embedded tissue sections. Arch Pathol Lab Med. 1997;121(8):888–93.PubMed
21.
go back to reference Garcia L, Smith J, Fritsche T. Selection and use of laboratory procedures for the diagnosis of parasitic infections of the gastrointestinal tract. Washington, DC: ASM Press; 2003. Garcia L, Smith J, Fritsche T. Selection and use of laboratory procedures for the diagnosis of parasitic infections of the gastrointestinal tract. Washington, DC: ASM Press; 2003.
22.
go back to reference Garcia L. Practical guide to diagnostic parasitology. Washington, DC: ASM Press; 2009. Garcia L. Practical guide to diagnostic parasitology. Washington, DC: ASM Press; 2009.
23.
go back to reference Young KH, Bullock SL, Melvin DM, Spruill CL. Ethyl acetate as a substitute for diethyl ether in the formalin-ether sedimentation technique. J Clin Microbiol. 1979;10(6):852–3.PubMedPubMedCentral Young KH, Bullock SL, Melvin DM, Spruill CL. Ethyl acetate as a substitute for diethyl ether in the formalin-ether sedimentation technique. J Clin Microbiol. 1979;10(6):852–3.PubMedPubMedCentral
24.
go back to reference Henriksen SA, Pohlenz JF. Staining of cryptosporidia by a modified Ziehl-Neelsen technique. Acta Vet Scand. 1981;22(3–4):594–6.PubMed Henriksen SA, Pohlenz JF. Staining of cryptosporidia by a modified Ziehl-Neelsen technique. Acta Vet Scand. 1981;22(3–4):594–6.PubMed
25.
go back to reference Garcia LS, Bruckner DA, Brewer TC, Shimizu RY. Techniques for the recovery and identification of Cryptosporidium oocysts from stool specimens. J Clin Microbiol. 1983;18(1):185–90.PubMedPubMedCentral Garcia LS, Bruckner DA, Brewer TC, Shimizu RY. Techniques for the recovery and identification of Cryptosporidium oocysts from stool specimens. J Clin Microbiol. 1983;18(1):185–90.PubMedPubMedCentral
26.
go back to reference World Health Organization. Bench aids for the diagnosis of intestinal parasites. Geneva: WHO; 1994. World Health Organization. Bench aids for the diagnosis of intestinal parasites. Geneva: WHO; 1994.
27.
go back to reference Picot J, Guerin CL, Le Van Kim C, Boulanger CM. Flow cytometry: retrospective, fundamentals and recent instrumentation. Cytotechnol. 2012;64(2):109–30.CrossRef Picot J, Guerin CL, Le Van Kim C, Boulanger CM. Flow cytometry: retrospective, fundamentals and recent instrumentation. Cytotechnol. 2012;64(2):109–30.CrossRef
28.
go back to reference Maini MK, Gilson RJ, Chavda N, Gill S, Fakoya A, Ross EJ, et al. Reference ranges and sources of variability of CD4 counts in HIV-seronegative women and men. Sex Transm Infect. 1996;72(1):27–31.CrossRef Maini MK, Gilson RJ, Chavda N, Gill S, Fakoya A, Ross EJ, et al. Reference ranges and sources of variability of CD4 counts in HIV-seronegative women and men. Sex Transm Infect. 1996;72(1):27–31.CrossRef
29.
go back to reference World Health Organization. Interim WHO clinical staging of HVI/AIDS and HIV/AIDS case definitions for surveillance: African region. No. WHO/HIV/2005.02. Geneva: WHO; 2005. World Health Organization. Interim WHO clinical staging of HVI/AIDS and HIV/AIDS case definitions for surveillance: African region. No. WHO/HIV/2005.02. Geneva: WHO; 2005.
30.
go back to reference Kato S, Chmielewski M, Honda H, Pecoits-Filho R, Matsuo S, Yuzawa Y, et al. Aspects of immune dysfunction in end-stage renal disease. Clin J Am Soc Nephrol. 2008;3(5):1526–33.PubMedPubMedCentralCrossRef Kato S, Chmielewski M, Honda H, Pecoits-Filho R, Matsuo S, Yuzawa Y, et al. Aspects of immune dysfunction in end-stage renal disease. Clin J Am Soc Nephrol. 2008;3(5):1526–33.PubMedPubMedCentralCrossRef
31.
go back to reference Lisowska KA, Debska-Slizien A, Jasiulewicz A, Heleniak Z, Bryl E, Witkowski JM. Hemodialysis affects phenotype and proliferation of CD4-positive T lymphocytes. J Clin Immunol. 2012;32(1):189–200.PubMedCrossRef Lisowska KA, Debska-Slizien A, Jasiulewicz A, Heleniak Z, Bryl E, Witkowski JM. Hemodialysis affects phenotype and proliferation of CD4-positive T lymphocytes. J Clin Immunol. 2012;32(1):189–200.PubMedCrossRef
32.
go back to reference Kulik RA, Falavigna DL, Nishi L, Araujo SM. Blastocystis sp. and other intestinal parasites in hemodialysis patients. Braz J Infect Dis. 2008;12(4):338–41.PubMedCrossRef Kulik RA, Falavigna DL, Nishi L, Araujo SM. Blastocystis sp. and other intestinal parasites in hemodialysis patients. Braz J Infect Dis. 2008;12(4):338–41.PubMedCrossRef
33.
go back to reference Karadag G, Tamer GS, Dervisoglu E. Investigation of intestinal parasites in dialysis patients. Saudi Med J. 2013;34(7):714–8.PubMed Karadag G, Tamer GS, Dervisoglu E. Investigation of intestinal parasites in dialysis patients. Saudi Med J. 2013;34(7):714–8.PubMed
34.
go back to reference Rasti S, Hassanzadeh M, Hooshyar H, Momen-Heravi M, Mousavi SGA, Abdoli A. Intestinal parasitic infections in different groups of immunocompromised patients in Kashan and Qom cities, Central Iran. Scand J Gastroenterol. 2017;52(6–7):738–41.PubMedCrossRef Rasti S, Hassanzadeh M, Hooshyar H, Momen-Heravi M, Mousavi SGA, Abdoli A. Intestinal parasitic infections in different groups of immunocompromised patients in Kashan and Qom cities, Central Iran. Scand J Gastroenterol. 2017;52(6–7):738–41.PubMedCrossRef
35.
go back to reference Barazesh A, Fouladvand M, Tahmasebi R, Heydari A, Fallahi J. The prevalence of intestinal parasites in hemodialysis patients in Bushehr, Iran. Hemodial Int. 2015;19(3):447–51.PubMedCrossRef Barazesh A, Fouladvand M, Tahmasebi R, Heydari A, Fallahi J. The prevalence of intestinal parasites in hemodialysis patients in Bushehr, Iran. Hemodial Int. 2015;19(3):447–51.PubMedCrossRef
36.
go back to reference Seyrafian S, Pestehchian N, Kerdegari M, Yousefi HA, Bastani B. Prevalence rate of Cryptosporidium infection in hemodialysis patients in Iran. Hemodial Int. 2006;10(4):375–9.PubMedCrossRef Seyrafian S, Pestehchian N, Kerdegari M, Yousefi HA, Bastani B. Prevalence rate of Cryptosporidium infection in hemodialysis patients in Iran. Hemodial Int. 2006;10(4):375–9.PubMedCrossRef
37.
go back to reference Chen TL, Chan CC, Chen HP, Fung CP, Lin CP, Chan WL, et al. Clinical characteristics and endoscopic findings associated with Blastocystis hominis in healthy adults. Am J Trop Med Hyg. 2003;69(2):213–6.PubMedCrossRef Chen TL, Chan CC, Chen HP, Fung CP, Lin CP, Chan WL, et al. Clinical characteristics and endoscopic findings associated with Blastocystis hominis in healthy adults. Am J Trop Med Hyg. 2003;69(2):213–6.PubMedCrossRef
38.
go back to reference Hayashi M, Inamori M, Goto K, Akiyama T, Fujita K, Ikeda I, et al. Blastocystis hominis infection in patient with regular dialysis. J Gastroenterol. 2006;41(6):605–6.PubMedCrossRef Hayashi M, Inamori M, Goto K, Akiyama T, Fujita K, Ikeda I, et al. Blastocystis hominis infection in patient with regular dialysis. J Gastroenterol. 2006;41(6):605–6.PubMedCrossRef
39.
go back to reference Rao K, Sekar U, Iraivan KT, Abraham G, Soundararajan P. Blastocystis hominis--an emerging cause of diarrhoea in renal transplant recipients. J Assoc Physicians India. 2003;51:719–21.PubMed Rao K, Sekar U, Iraivan KT, Abraham G, Soundararajan P. Blastocystis hominis--an emerging cause of diarrhoea in renal transplant recipients. J Assoc Physicians India. 2003;51:719–21.PubMed
40.
go back to reference Thagfan FA, Sanad MM, Al Olayan EM, Al Hoshani NI. Intestinal parasitic infections in relation to diarrhea and CD4 T-cell count among Saudi patients with chronic renal insufficiency. In: International Conference on Agricultural, Ecological and Medical Sciences (AEMS). Phuket: IICBEE; 2015. Thagfan FA, Sanad MM, Al Olayan EM, Al Hoshani NI. Intestinal parasitic infections in relation to diarrhea and CD4 T-cell count among Saudi patients with chronic renal insufficiency. In: International Conference on Agricultural, Ecological and Medical Sciences (AEMS). Phuket: IICBEE; 2015.
41.
go back to reference Strid H, Simrén M, Johansson AC, Svedlund J, Samuelsson O, Björnsson ES. The prevalence of gastrointestinal symptoms in patients with chronic renal failure is increased and associated with impaired psychological general well-being. Nephrol Dial Transplant. 2002;17:1434–9.PubMedCrossRef Strid H, Simrén M, Johansson AC, Svedlund J, Samuelsson O, Björnsson ES. The prevalence of gastrointestinal symptoms in patients with chronic renal failure is increased and associated with impaired psychological general well-being. Nephrol Dial Transplant. 2002;17:1434–9.PubMedCrossRef
42.
go back to reference Dong R, Guo ZY. Gastrointestinal symptoms in patients undergoing peritoneal dialysis: multivariate analysis of correlated factors. World J Gastroenterol. 2010;16:2812–7.PubMedPubMedCentralCrossRef Dong R, Guo ZY. Gastrointestinal symptoms in patients undergoing peritoneal dialysis: multivariate analysis of correlated factors. World J Gastroenterol. 2010;16:2812–7.PubMedPubMedCentralCrossRef
43.
go back to reference El-Diffrawy M, Neanaa H, Eissa M, Sadaka H, Nomir A. Study of parasitic infections in immunocompromised patients in Haematology Department at Main University Hospital, Alexandria. Exp Pathol Parasitol. 2002;10:85–92. El-Diffrawy M, Neanaa H, Eissa M, Sadaka H, Nomir A. Study of parasitic infections in immunocompromised patients in Haematology Department at Main University Hospital, Alexandria. Exp Pathol Parasitol. 2002;10:85–92.
44.
go back to reference Yazar S, Demirtas F, Yalcin S, Yaman O, Tokgoz B, Utas C, et al. Anti-Toxoplasma gondii antibodies in haemodialysis patients with chronic renal failure. Yonsei Med J. 2003;44(2):288–92.PubMedCrossRef Yazar S, Demirtas F, Yalcin S, Yaman O, Tokgoz B, Utas C, et al. Anti-Toxoplasma gondii antibodies in haemodialysis patients with chronic renal failure. Yonsei Med J. 2003;44(2):288–92.PubMedCrossRef
45.
go back to reference Ocak S, Duran N, Eskiocak AF, Aytac H. Anti-Toxoplasma gondii antibodies in hemodialysis patients receiving long-term hemodialysis therapy in Turkey. Saudi Med J. 2005;26(9):1378–82.PubMed Ocak S, Duran N, Eskiocak AF, Aytac H. Anti-Toxoplasma gondii antibodies in hemodialysis patients receiving long-term hemodialysis therapy in Turkey. Saudi Med J. 2005;26(9):1378–82.PubMed
46.
go back to reference Alvarado-Esquivel C, Liesenfeld O, Torres-Castorena A, Estrada-Martinez S, Urbina-Alvarez JD, Ramos-de la Rocha M, et al. Seroepidemiology of Toxoplasma gondii infection in patients with vision and hearing impairments, cancer, HIV, or undergoing hemodialysis in Durango, Mexico. J Parasitol. 2010;96(3):505–8.PubMedCrossRef Alvarado-Esquivel C, Liesenfeld O, Torres-Castorena A, Estrada-Martinez S, Urbina-Alvarez JD, Ramos-de la Rocha M, et al. Seroepidemiology of Toxoplasma gondii infection in patients with vision and hearing impairments, cancer, HIV, or undergoing hemodialysis in Durango, Mexico. J Parasitol. 2010;96(3):505–8.PubMedCrossRef
47.
go back to reference Foroutan M, Rostami A, Majidiani H, Riahi SM, Khazaei S, Badri M, et al. A systematic review and meta-analysis of the prevalence of toxoplasmosis in hemodialysis patients in Iran. Epidemiol Health. 2018;40:e2018016.PubMedPubMedCentralCrossRef Foroutan M, Rostami A, Majidiani H, Riahi SM, Khazaei S, Badri M, et al. A systematic review and meta-analysis of the prevalence of toxoplasmosis in hemodialysis patients in Iran. Epidemiol Health. 2018;40:e2018016.PubMedPubMedCentralCrossRef
48.
go back to reference Dorri M, Dabirzadeh M, Maroufi Y, Afshari M, Badri Chokamy M. Prevalence of anti-Toxoplasma IgG and IgM in hemodialysis patients comparing to healthy individuals in Sistan area. Iran J Nephropharmacol. 2017;6(2):106–9. Dorri M, Dabirzadeh M, Maroufi Y, Afshari M, Badri Chokamy M. Prevalence of anti-Toxoplasma IgG and IgM in hemodialysis patients comparing to healthy individuals in Sistan area. Iran J Nephropharmacol. 2017;6(2):106–9.
49.
go back to reference Ebrahim Zadeh A, Bamedi T, Etemadi S, Shahrakipour M, Saryazdipour K. Toxoplasmosis as a complication of transfusion in hemodialysis patients. Iran J Ped Hematol Oncol. 2014;4(1):22–5.PubMedPubMedCentral Ebrahim Zadeh A, Bamedi T, Etemadi S, Shahrakipour M, Saryazdipour K. Toxoplasmosis as a complication of transfusion in hemodialysis patients. Iran J Ped Hematol Oncol. 2014;4(1):22–5.PubMedPubMedCentral
50.
go back to reference Aufy SM, Mahgoub AM, Saadi MG, Adel Elmallawany M. Serological detection of Toxoplasma gondii in chronic renal failure patients and renal transplant recipients. J Egypt Soc Parasitol. 2009;39(3):943–50.PubMed Aufy SM, Mahgoub AM, Saadi MG, Adel Elmallawany M. Serological detection of Toxoplasma gondii in chronic renal failure patients and renal transplant recipients. J Egypt Soc Parasitol. 2009;39(3):943–50.PubMed
51.
go back to reference Saki J, Khademvatan S, Soltani S, Shahbazian H. Detection of toxoplasmosis in patients with end-stage renal disease by enzyme-linked immunosorbent assay and polymerase chain reaction methods. Parasitol Res. 2013;112(1):163–8.PubMedCrossRef Saki J, Khademvatan S, Soltani S, Shahbazian H. Detection of toxoplasmosis in patients with end-stage renal disease by enzyme-linked immunosorbent assay and polymerase chain reaction methods. Parasitol Res. 2013;112(1):163–8.PubMedCrossRef
52.
go back to reference Murat JB, Hidalgo HF, Brenier-Pinchart MP, Pelloux H. Human toxoplasmosis: which biological diagnostic tests are best suited to which clinical situations? Expert Rev Anti-Infect Ther. 2013;11(9):943–56.PubMedCrossRef Murat JB, Hidalgo HF, Brenier-Pinchart MP, Pelloux H. Human toxoplasmosis: which biological diagnostic tests are best suited to which clinical situations? Expert Rev Anti-Infect Ther. 2013;11(9):943–56.PubMedCrossRef
53.
go back to reference Montoya JG. Laboratory diagnosis of Toxoplasma gondii infection and toxoplasmosis. J Infect Dis. 2002;185(Suppl 1):S73–82.PubMedCrossRef Montoya JG. Laboratory diagnosis of Toxoplasma gondii infection and toxoplasmosis. J Infect Dis. 2002;185(Suppl 1):S73–82.PubMedCrossRef
54.
go back to reference Dhakal R, Gajurel K, Pomares C, Talucod J, Press CJ, Montoya JG. Significance of a positive Toxoplasma immunoglobulin M test result in the United States. J Clin Microbiol. 2015;53(11):3601–5.PubMedPubMedCentralCrossRef Dhakal R, Gajurel K, Pomares C, Talucod J, Press CJ, Montoya JG. Significance of a positive Toxoplasma immunoglobulin M test result in the United States. J Clin Microbiol. 2015;53(11):3601–5.PubMedPubMedCentralCrossRef
55.
go back to reference Nissapatorn V, Sawangjareon N. Toxoplasmosis: IgG avidity and its implication in serodiagnosis. Trends in immunolabelled and related techniques: IntechOpen; 2012. Nissapatorn V, Sawangjareon N. Toxoplasmosis: IgG avidity and its implication in serodiagnosis. Trends in immunolabelled and related techniques: IntechOpen; 2012.
56.
go back to reference Hedman K, Lappalainen M, Seppäiä I, Mäkelä O. Recent primary Toxoplasma infection indicated by a low avidity of specific IgG. J Infect Dis. 1989;159(4):736–40.PubMedCrossRef Hedman K, Lappalainen M, Seppäiä I, Mäkelä O. Recent primary Toxoplasma infection indicated by a low avidity of specific IgG. J Infect Dis. 1989;159(4):736–40.PubMedCrossRef
57.
go back to reference Sonaimuthu P, Fong MY, Kalyanasundaram R, Mahmud R, Lau YL. Sero-diagnostic evaluation of Toxoplasma gondii recombinant rhoptry antigen 8 expressed in E. coli. Parasit Vectors. 2014;7:297.PubMedPubMedCentralCrossRef Sonaimuthu P, Fong MY, Kalyanasundaram R, Mahmud R, Lau YL. Sero-diagnostic evaluation of Toxoplasma gondii recombinant rhoptry antigen 8 expressed in E. coli. Parasit Vectors. 2014;7:297.PubMedPubMedCentralCrossRef
58.
go back to reference Hajissa K, Zakaria R, Suppian R, Mohamed Z. Design and evaluation of a recombinant multi-epitope antigen for serodiagnosis of Toxoplasma gondii infection in humans. Parasit Vectors. 2015;8:315.PubMedPubMedCentralCrossRef Hajissa K, Zakaria R, Suppian R, Mohamed Z. Design and evaluation of a recombinant multi-epitope antigen for serodiagnosis of Toxoplasma gondii infection in humans. Parasit Vectors. 2015;8:315.PubMedPubMedCentralCrossRef
60.
go back to reference Nsagha DS, Njunda AL, Assob NJC, Ayima CW, Tanue EA, Kibu OD, et al. Intestinal parasitic infections in relation to CD4(+) T cell counts and diarrhea in HIV/AIDS patients with or without antiretroviral therapy in Cameroon. BMC Infect Dis. 2016;16:9.PubMedPubMedCentralCrossRef Nsagha DS, Njunda AL, Assob NJC, Ayima CW, Tanue EA, Kibu OD, et al. Intestinal parasitic infections in relation to CD4(+) T cell counts and diarrhea in HIV/AIDS patients with or without antiretroviral therapy in Cameroon. BMC Infect Dis. 2016;16:9.PubMedPubMedCentralCrossRef
61.
go back to reference Sucilathangam G, Palaniappan N, Sreekumar C, Anna T. Serological survey of toxoplasmosis in a district in Tamil Nadu: hospital-based study. Indian J Med Res. 2013;137(3):560–3.PubMedPubMedCentral Sucilathangam G, Palaniappan N, Sreekumar C, Anna T. Serological survey of toxoplasmosis in a district in Tamil Nadu: hospital-based study. Indian J Med Res. 2013;137(3):560–3.PubMedPubMedCentral
62.
go back to reference Anuradha B, Preethi C. Seroprevalence of Toxoplasma IgG antibodies in HIV positive patients in and around Khammam, Telangana state. J Clin Diagn Res. 2014;8(9):DL01–2.PubMedPubMedCentral Anuradha B, Preethi C. Seroprevalence of Toxoplasma IgG antibodies in HIV positive patients in and around Khammam, Telangana state. J Clin Diagn Res. 2014;8(9):DL01–2.PubMedPubMedCentral
63.
go back to reference Osunkalu VO, Akanmu SA, Ofomah NJ, Onyiaorah IV, Adediran AA, Akinde RO, Onwuezobe IA. Seroprevalence of Toxoplasma gondii IgG antibody in HIV-infected patients at the Lagos University teaching hospital. HIV AIDS (Auckl). 2011;3:101–5. Osunkalu VO, Akanmu SA, Ofomah NJ, Onyiaorah IV, Adediran AA, Akinde RO, Onwuezobe IA. Seroprevalence of Toxoplasma gondii IgG antibody in HIV-infected patients at the Lagos University teaching hospital. HIV AIDS (Auckl). 2011;3:101–5.
Metadata
Title
Opportunistic parasitoses among Egyptian hemodialysis patients in relation to CD4+ T-cell counts: a comparative study
Authors
Amany I. Shehata
Faika Hassanein
Rashad Abdul-Ghani
Publication date
01-12-2019
Publisher
BioMed Central
Published in
BMC Infectious Diseases / Issue 1/2019
Electronic ISSN: 1471-2334
DOI
https://doi.org/10.1186/s12879-019-4110-4

Other articles of this Issue 1/2019

BMC Infectious Diseases 1/2019 Go to the issue
Live Webinar | 27-06-2024 | 18:00 (CEST)

Keynote webinar | Spotlight on medication adherence

Live: Thursday 27th June 2024, 18:00-19:30 (CEST)

WHO estimates that half of all patients worldwide are non-adherent to their prescribed medication. The consequences of poor adherence can be catastrophic, on both the individual and population level.

Join our expert panel to discover why you need to understand the drivers of non-adherence in your patients, and how you can optimize medication adherence in your clinics to drastically improve patient outcomes.

Prof. Kevin Dolgin
Prof. Florian Limbourg
Prof. Anoop Chauhan
Developed by: Springer Medicine
Obesity Clinical Trial Summary

At a glance: The STEP trials

A round-up of the STEP phase 3 clinical trials evaluating semaglutide for weight loss in people with overweight or obesity.

Developed by: Springer Medicine

Highlights from the ACC 2024 Congress

Year in Review: Pediatric cardiology

Watch Dr. Anne Marie Valente present the last year's highlights in pediatric and congenital heart disease in the official ACC.24 Year in Review session.

Year in Review: Pulmonary vascular disease

The last year's highlights in pulmonary vascular disease are presented by Dr. Jane Leopold in this official video from ACC.24.

Year in Review: Valvular heart disease

Watch Prof. William Zoghbi present the last year's highlights in valvular heart disease from the official ACC.24 Year in Review session.

Year in Review: Heart failure and cardiomyopathies

Watch this official video from ACC.24. Dr. Biykem Bozkurt discusses last year's major advances in heart failure and cardiomyopathies.