YKL-40 as a novel diagnostic biomarker in Toxoplasmosis
Main Article Content
Keywords
Toxoplasmosis, Toxoplasma gondii, YKL-40, biomarkers, diagnosis.
Abstract
Toxoplasmosis is one of the most globally prevalent zoonotic infection caused by an obligate, intracellular parasite called Toxoplasma gondii. Toxoplasmosis actively triggers an acute immune response and inflammatory reactions, causes serious pathological changes in various tissues in the human body, and more evidently localizes in different nervous tissues of various body organs. The YKL-40 is a glycoprotein secreted by numerous cell types in different patterns associated with various pathological processes such as inflammatory reactions, tissue remodeling, fibrosis, and thought it is a disease-specific biomarker of neuroinflammation. Therefore, The current study aimed to determine if the YKL-40 is markedly increased in toxoplasmosis or not and if its level is different between the acute and chronic phases of the infection to determine if it can be used as a clinically useful biomarker in the diagnosis, determination of disease severity and follow up of toxoplasmosis. Accordingly, a total of eighty serum samples were collected from previously diagnosed female patients with toxoplasmosis of different ages. In addition, ten healthy female sera were used as a control. Patients were firstly divided into two groups (30 patients with acute infection and 50 patients with chronic infection) depending on the results of detecting the specific anti-Toxoplasma IgM and IgG by ELISA. The level of YKL-40 was then measured in the patients’ serum by ELISA. The statistical analysis of data clearly disclosed very highly significant differences (p <0.001) between the level of YKL-40 in the acute infection group and healthy controls, chronic infection group and healthy controls, and between the groups of acute and chronic infection. These findings lead to conclude that YKL-40 classify as a unique and sophisticated biomarker in the diagnosis of toxoplasmosis where it can vitally be used to detect the stage of the disease whether acute or chronic, beside its ability to detect the infection.
References
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13. Heij HAJPSGPS, Tumors, Trauma, Transplantation. Lymph Node Disorders. 2021:11-20.
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16. Clough B, Frickel E-MJTip. The toxoplasma parasitophorous vacuole: an evolving host–parasite frontier. 2017;33(6):473-88.
17. Tong WH, Pavey C, O’Handley R, Vyas A. Behavioral biology of Toxoplasma gondii infection. Parasites & Vectors. 2021;14(1):77.
18. Ortiz-Guerrero G, Gonzalez-Reyes RE, de-la-Torre A, Medina-Rincón G, Nava-Mesa MOJBs. Pathophysiological mechanisms of cognitive impairment and neurodegeneration by Toxoplasma gondii infection. 2020;10(6):369.
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21. Frickel E-M, Hunter CAJJoEM. Lessons from Toxoplasma: Host responses that mediate parasite control and the microbial effectors that subvert them. 2021;218(11):e20201314.
22. Laing C, Blanchard N, McConkey GAJTiI. Noradrenergic signaling and neuroinflammation crosstalk regulate Toxoplasma gondii-induced behavioral changes. 2020.
23. Bhadra R, Khan IA. Redefining Chronic Toxoplasmosis—A T Cell Exhaustion Perspective. PLOS Pathogens. 2012;8(10):e1002903.
24. Jiang T. The population genetics, ecology, and transmission of Toxoplasma gondii in North America. 2019.
25. Mévélec, M., Lakhrif, Z., & Dimier-Poisson, I. (2020). Key Limitations and New Insights in to the Toxoplasma gondii Parasite Stage Switching for Future Vaccine Development in Human, Livestock, and Cats. Fron. Cell. Infect. Microbiol, 10, 607198.
26. Robinson, Cory M., et al. "Cytokines involved in interferon-γ production by human macrophages." Journal of innate immunity 2.1 (2010): 56-65.
27. Petersen E. “Toxoplasmosis” Semin Fetal Neonatal Med, 12(3) : 214 – 223(2007).
28. Denkers, Eric Y., and Ricardo T. Gazzinelli. "Regulation and function of T-cell-mediated immunity during Toxoplasma gondii infection." Clinical microbiology reviews 11.4 (1998): 569-588.
29. Wang J-L, Li T-T, Elsheikha HM, Chen K, Cong W, Yang W-B, et al. Live Attenuated Pru: Δ cdpk2 Strain of Toxoplasma gondii Protects Against Acute, Chronic, and Congenital Toxoplasmosis. 2018;218(5):768-77.
30. Santana SS, Paiva VF, Carvalho FR, Barros HLS, Silva TL, Barros PSC, et al. A peptide originated from Toxoplasma gondii microneme 8 displaying serological evidence to differentiate recent from chronic human infection. 2021:102394.
31. Ybañez RHD, Ybañez AP, Nishikawa YJFiC, Microbiology I. Review on the current trends of toxoplasmosis serodiagnosis in humans. 2020;10:204.
32. Ripoll Pastor G. Chimeric synthetic peptides as diagnostic tools: a novel IgM-specific immunoassay for the diagnosis of toxoplasmosis: Driving innovation towards next generation IgM immunoassays 2021.
33. Robert-Gangneux F, Dardé M-L. Epidemiology of and Diagnostic Strategies for Toxoplasmosis. 2012;25(2):264-96.
34. Khan AH, Noordin RJEJoCM, Diseases I. Serological and molecular rapid diagnostic tests for Toxoplasma infection in humans and animals. 2020;39(1):19-30.
35. Khames M, Sihem S, Hizia H, Nguewa PJAoP. High toxoplasmosis seroprevalence among young pregnant women in Medea, Algeria. 2020;66(4):509-15.
36. Devakumar D, Bamford A, Ferreira MU, Broad J, Rosch RE, Groce N, et al. Infectious causes of microcephaly: epidemiology, pathogenesis, diagnosis, and management. 2018;18(1):e1-e13.
37. Robert-Gangneux F, Guegan HJP. Anti-Toxoplasma IgG assays: What performances for what purpose? A systematic review. 2021;28.
38. Teimouri A, Mohtasebi S, Kazemirad E, Keshavarz HJJocm. Role of Toxoplasma gondii IgG avidity testing in discriminating between acute and chronic toxoplasmosis in pregnancy. 2020;58(9):e00505-20.
39. Oudah, Narjis Abdul Rahman, Kareem S. Chead Al-Teea, and Ahmed A. Mohammed. "Using the Level of Serum YKL-40 as an Indicator to the Pathogenesis of Allergic Asthma and Helminths Infection." Indian Journal of Public Health Research & Development 10.10 (2019).
40. Zhao, Ting, et al. "Chitinase-3 like-protein-1 function and its role in diseases." Signal Transduction and Targeted Therapy 5.1 (2020): 1-20.
41. Salomon, Joanna, et al. "Chitinase-3-like protein 1 (ykl-40) reflects the severity of symptoms in atopic dermatitis." Journal of immunology research 2017 (2017).
42. Gurung R, Choong AM, Woo CC, Foo R, Sorokin VJIjoms. Genetic and epigenetic mechanisms underlying vascular smooth muscle cell phenotypic modulation in abdominal aortic aneurysm. 2020;21(17):6334.
43. Majewski, Sebastian, et al. "Longitudinal and comparative measures of serum chitotriosidase and YKL-40 in patients with idiopathic pulmonary fibrosis." Frontiers in immunology (2022): 421.
44. Lee, Chun Geun, and Jack A. Elias. "Role of breast regression protein-39/YKL-40 in asthma and allergic responses." Allergy, asthma & immunology research 2.1 (2010): 20-27.
45. Giraldo, Mónica, et al. "Fractionation of membrane components from tachyzoite forms of Toxoplasma gondii: differential recognition by immunoglobulin M (IgM) and IgG present in sera from patients with acute or chronic toxoplasmosis." Journal of clinical microbiology 38.4 (2000): 1453-1460.
46. Villard, O., et al. "Serological diagnosis of Toxoplasma gondii infection: recommendations from the French National Reference Center for Toxoplasmosis." Diagnostic Microbiology and Infectious Disease 84.1 (2016): 22-33.
47. Giraldo, Mónica, et al. "Immunoglobulin M (IgM)-glycoinositolphospholipid enzyme-linked immunosorbent assay: an immunoenzymatic assay for discrimination between patients with acute toxoplasmosis and those with persistent parasite-specific IgM antibodies." Journal of Clinical Microbiology 40.4 (2002): 1400-1405.
48. Fricker-Hidalgo, Hélène, et al. "How to estimate time of infection with Toxoplasma gondii in pregnant women. Use of specific IgG and IgM kinetics by 7 techniques on 691 sera." Diagnostic microbiology and infectious disease 96.4 (2020): 114987.
49. Kamal, Amany M., et al. "Seropositivity of toxoplasmosis in pregnant women by ELISA at Minia University Hospital, Egypt." The Korean journal of parasitology 53.5 (2015): 605.
50. Al-Kuraishy, Hayder M., et al. "Toxoplasmosis and risk of endothelial dysfunction: Role of oxidative stress and pro-inflammatory mediators." Arch. Clin. Infect. Dis 14 (2019): e95563.
51. Gandhi, Puneet, et al. "Circulatory YKL-40 & NLR: underestimated prognostic indicators in diffuse glioma." International Journal of Molecular and Cellular Medicine 7.2 (2018): 111.
52. Coriati, Adèle, et al. "Ykl-40 as a clinical biomarker in adult patients with cf: Implications of a chi3l1 single nucleotide polymorphism in disease severity." Journal of Cystic Fibrosis 20.6 (2021): e93-e99.
53. Mazur, Marzena, et al. "Chitinases and Chitinase-Like Proteins as Therapeutic Targets in Inflammatory Diseases, with a Special Focus on Inflammatory Bowel Diseases." International Journal of Molecular Sciences 22.13 (2021): 6966.
54. Pinteac, Rucsanda, Xavier Montalban, and Manuel Comabella. "Chitinases and chitinase-like proteins as biomarkers in neurologic disorders." Neurology-Neuroimmunology Neuroinflammation 8.1 (2021).
55. Jankowska-Konsur, Alina, et al. "Chitinase-3-like Protein 1 (YKL-40): A New Biomarker of Inflammation in Pyoderma Gangrenosum." Acta Dermato-Venereologica (2021).
56. Kwon, Yoowon, et al. "Serum YKL-40 Levels Are Associated with the Atherogenic Index of Plasma in Children." Mediators of inflammation 2020 (2020).
57. Heukels, Peter, et al. "Inflammation and immunity in IPF pathogenesis and treatment." Respiratory Medicine 147 (2019): 79-91.
58. Chandan, Kumari, Meenakshi Gupta, and Maryam Sarwat. "Role of host and pathogen-derived microRNAs in immune regulation during infectious and inflammatory diseases." Frontiers in Immunology (2020): 3081.
2. Pérez‐Grisales LJ, Cruz‐Moncada M, Peláez‐Sánchez R, Díaz‐Nieto JFJZ, Health P. Toxoplasma gondii infection in Colombia with a review of hosts and their ecogeographic distribution. 2021;68(1):38-53.
3. George C, Jeffery H, Lahra MJKsF, Pathology N. Infection of Mother and Baby. 2022:207-45.
4. El Bissati K, Levigne P, Lykins J, Adlaoui EB, Barkat A, Berraho A, et al. Global initiative for congenital toxoplasmosis: an observational and international comparative clinical analysis. 2018;7(1):1-14.
5. Mero WMSJZJoP, Sciences A. Seroprevalence of anti-Toxoplasma gondii antibodies among women of childbearing age in Zakho City, Kurdistan Region/Iraq. 2020;32(3):75-84.
6. Costa MJFGLd. Contribution for the knowledge of toxoplasmosis in Portugal. 2019.
7. Al-Tufaili RANJSRiP. Evaluation of commercial Linked immune-sorbent assay (ELISA) for detecting sero-prevalence of Toxoplasma gondii antibodies in Iraqi women. 2020;11(12):57-62.
8. Dubey J, Murata F, Cerqueira-Cézar C, Kwok OJTJoP. Epidemiologic and public health significance of Toxoplasma gondii infections in venison: 2009–2020. 2021;107(2):309-19.
9. Sharif A, Aliyu M, Yusuf M, Getso M, Yahaya H, Bala J, et al. Risk factors and mode of transmission of toxoplasmosis in Nigeria: a review. 2018;11(2):107-21.
10. Onduru OG, Rumisha SF, Munyeme M, Phiri AMJAhs. Evaluation of the level of awareness of congenital toxoplasmosis and associated practices among pregnant women and health workers in Tanzania’s Temeke district in Dar es Salaam. 2019;19(4):3027-37.
11. Ladeia WA, Martins FDC, Pinto-Ferreira F, Freire RL, Navarro IT. Detection of Toxoplasma Gondii in Meat. Detection and Enumeration of Bacteria, Yeast, Viruses, and Protozoan in Foods and Freshwater: Springer; 2021. p. 215-23.
12. Kalogeropoulos D, Sakkas H, Mohammed B, Vartholomatos G, Malamos K, Sreekantam S, et al. Ocular toxoplasmosis: a review of the current diagnostic and therapeutic approaches. 2021:1-27.
13. Heij HAJPSGPS, Tumors, Trauma, Transplantation. Lymph Node Disorders. 2021:11-20.
14. Healy CMJUDewuccc-lt-i-c-e-a-c-m. Cervical lymphadenitis in children: etiology and clinical manifestations. 2017.
15. Bargagli E, Prasse AJI, medicine e. Sarcoidosis: a review for the internist. 2018;13(3):325-31.
16. Clough B, Frickel E-MJTip. The toxoplasma parasitophorous vacuole: an evolving host–parasite frontier. 2017;33(6):473-88.
17. Tong WH, Pavey C, O’Handley R, Vyas A. Behavioral biology of Toxoplasma gondii infection. Parasites & Vectors. 2021;14(1):77.
18. Ortiz-Guerrero G, Gonzalez-Reyes RE, de-la-Torre A, Medina-Rincón G, Nava-Mesa MOJBs. Pathophysiological mechanisms of cognitive impairment and neurodegeneration by Toxoplasma gondii infection. 2020;10(6):369.
19. Dubey, J. P., Ferreira, L. R., Alsaad, M., Verma, S. K., Alves, D. A., Holland, G. N., & McConkey, G. A. (2016). Experimental toxoplasmosis in rats induced orally with eleven strains of Toxoplasma gondii of seven genotypes: tissue tropism, tissue cyst size, neural lesions, tissue cyst rupture without reactivation, and ocular lesions. PloS One, 11(5), e0156255.
20. Lori C., Kenneth H. E., Martha E. W. and Imtiaz A. “CD8 + T-Cell Immunity Against Toxoplasma gondii can be Induced but not Maintained in Mice lacking Conventional CD4+ T Cells” Infect Immunol, 70: 434-443(2002).
21. Frickel E-M, Hunter CAJJoEM. Lessons from Toxoplasma: Host responses that mediate parasite control and the microbial effectors that subvert them. 2021;218(11):e20201314.
22. Laing C, Blanchard N, McConkey GAJTiI. Noradrenergic signaling and neuroinflammation crosstalk regulate Toxoplasma gondii-induced behavioral changes. 2020.
23. Bhadra R, Khan IA. Redefining Chronic Toxoplasmosis—A T Cell Exhaustion Perspective. PLOS Pathogens. 2012;8(10):e1002903.
24. Jiang T. The population genetics, ecology, and transmission of Toxoplasma gondii in North America. 2019.
25. Mévélec, M., Lakhrif, Z., & Dimier-Poisson, I. (2020). Key Limitations and New Insights in to the Toxoplasma gondii Parasite Stage Switching for Future Vaccine Development in Human, Livestock, and Cats. Fron. Cell. Infect. Microbiol, 10, 607198.
26. Robinson, Cory M., et al. "Cytokines involved in interferon-γ production by human macrophages." Journal of innate immunity 2.1 (2010): 56-65.
27. Petersen E. “Toxoplasmosis” Semin Fetal Neonatal Med, 12(3) : 214 – 223(2007).
28. Denkers, Eric Y., and Ricardo T. Gazzinelli. "Regulation and function of T-cell-mediated immunity during Toxoplasma gondii infection." Clinical microbiology reviews 11.4 (1998): 569-588.
29. Wang J-L, Li T-T, Elsheikha HM, Chen K, Cong W, Yang W-B, et al. Live Attenuated Pru: Δ cdpk2 Strain of Toxoplasma gondii Protects Against Acute, Chronic, and Congenital Toxoplasmosis. 2018;218(5):768-77.
30. Santana SS, Paiva VF, Carvalho FR, Barros HLS, Silva TL, Barros PSC, et al. A peptide originated from Toxoplasma gondii microneme 8 displaying serological evidence to differentiate recent from chronic human infection. 2021:102394.
31. Ybañez RHD, Ybañez AP, Nishikawa YJFiC, Microbiology I. Review on the current trends of toxoplasmosis serodiagnosis in humans. 2020;10:204.
32. Ripoll Pastor G. Chimeric synthetic peptides as diagnostic tools: a novel IgM-specific immunoassay for the diagnosis of toxoplasmosis: Driving innovation towards next generation IgM immunoassays 2021.
33. Robert-Gangneux F, Dardé M-L. Epidemiology of and Diagnostic Strategies for Toxoplasmosis. 2012;25(2):264-96.
34. Khan AH, Noordin RJEJoCM, Diseases I. Serological and molecular rapid diagnostic tests for Toxoplasma infection in humans and animals. 2020;39(1):19-30.
35. Khames M, Sihem S, Hizia H, Nguewa PJAoP. High toxoplasmosis seroprevalence among young pregnant women in Medea, Algeria. 2020;66(4):509-15.
36. Devakumar D, Bamford A, Ferreira MU, Broad J, Rosch RE, Groce N, et al. Infectious causes of microcephaly: epidemiology, pathogenesis, diagnosis, and management. 2018;18(1):e1-e13.
37. Robert-Gangneux F, Guegan HJP. Anti-Toxoplasma IgG assays: What performances for what purpose? A systematic review. 2021;28.
38. Teimouri A, Mohtasebi S, Kazemirad E, Keshavarz HJJocm. Role of Toxoplasma gondii IgG avidity testing in discriminating between acute and chronic toxoplasmosis in pregnancy. 2020;58(9):e00505-20.
39. Oudah, Narjis Abdul Rahman, Kareem S. Chead Al-Teea, and Ahmed A. Mohammed. "Using the Level of Serum YKL-40 as an Indicator to the Pathogenesis of Allergic Asthma and Helminths Infection." Indian Journal of Public Health Research & Development 10.10 (2019).
40. Zhao, Ting, et al. "Chitinase-3 like-protein-1 function and its role in diseases." Signal Transduction and Targeted Therapy 5.1 (2020): 1-20.
41. Salomon, Joanna, et al. "Chitinase-3-like protein 1 (ykl-40) reflects the severity of symptoms in atopic dermatitis." Journal of immunology research 2017 (2017).
42. Gurung R, Choong AM, Woo CC, Foo R, Sorokin VJIjoms. Genetic and epigenetic mechanisms underlying vascular smooth muscle cell phenotypic modulation in abdominal aortic aneurysm. 2020;21(17):6334.
43. Majewski, Sebastian, et al. "Longitudinal and comparative measures of serum chitotriosidase and YKL-40 in patients with idiopathic pulmonary fibrosis." Frontiers in immunology (2022): 421.
44. Lee, Chun Geun, and Jack A. Elias. "Role of breast regression protein-39/YKL-40 in asthma and allergic responses." Allergy, asthma & immunology research 2.1 (2010): 20-27.
45. Giraldo, Mónica, et al. "Fractionation of membrane components from tachyzoite forms of Toxoplasma gondii: differential recognition by immunoglobulin M (IgM) and IgG present in sera from patients with acute or chronic toxoplasmosis." Journal of clinical microbiology 38.4 (2000): 1453-1460.
46. Villard, O., et al. "Serological diagnosis of Toxoplasma gondii infection: recommendations from the French National Reference Center for Toxoplasmosis." Diagnostic Microbiology and Infectious Disease 84.1 (2016): 22-33.
47. Giraldo, Mónica, et al. "Immunoglobulin M (IgM)-glycoinositolphospholipid enzyme-linked immunosorbent assay: an immunoenzymatic assay for discrimination between patients with acute toxoplasmosis and those with persistent parasite-specific IgM antibodies." Journal of Clinical Microbiology 40.4 (2002): 1400-1405.
48. Fricker-Hidalgo, Hélène, et al. "How to estimate time of infection with Toxoplasma gondii in pregnant women. Use of specific IgG and IgM kinetics by 7 techniques on 691 sera." Diagnostic microbiology and infectious disease 96.4 (2020): 114987.
49. Kamal, Amany M., et al. "Seropositivity of toxoplasmosis in pregnant women by ELISA at Minia University Hospital, Egypt." The Korean journal of parasitology 53.5 (2015): 605.
50. Al-Kuraishy, Hayder M., et al. "Toxoplasmosis and risk of endothelial dysfunction: Role of oxidative stress and pro-inflammatory mediators." Arch. Clin. Infect. Dis 14 (2019): e95563.
51. Gandhi, Puneet, et al. "Circulatory YKL-40 & NLR: underestimated prognostic indicators in diffuse glioma." International Journal of Molecular and Cellular Medicine 7.2 (2018): 111.
52. Coriati, Adèle, et al. "Ykl-40 as a clinical biomarker in adult patients with cf: Implications of a chi3l1 single nucleotide polymorphism in disease severity." Journal of Cystic Fibrosis 20.6 (2021): e93-e99.
53. Mazur, Marzena, et al. "Chitinases and Chitinase-Like Proteins as Therapeutic Targets in Inflammatory Diseases, with a Special Focus on Inflammatory Bowel Diseases." International Journal of Molecular Sciences 22.13 (2021): 6966.
54. Pinteac, Rucsanda, Xavier Montalban, and Manuel Comabella. "Chitinases and chitinase-like proteins as biomarkers in neurologic disorders." Neurology-Neuroimmunology Neuroinflammation 8.1 (2021).
55. Jankowska-Konsur, Alina, et al. "Chitinase-3-like Protein 1 (YKL-40): A New Biomarker of Inflammation in Pyoderma Gangrenosum." Acta Dermato-Venereologica (2021).
56. Kwon, Yoowon, et al. "Serum YKL-40 Levels Are Associated with the Atherogenic Index of Plasma in Children." Mediators of inflammation 2020 (2020).
57. Heukels, Peter, et al. "Inflammation and immunity in IPF pathogenesis and treatment." Respiratory Medicine 147 (2019): 79-91.
58. Chandan, Kumari, Meenakshi Gupta, and Maryam Sarwat. "Role of host and pathogen-derived microRNAs in immune regulation during infectious and inflammatory diseases." Frontiers in Immunology (2020): 3081.
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Jun 27, 2022
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Farah Abd AL-Zahra Shahad, Ahmed A. Mohammed, & Ghaith Ali Jasim. (2022). YKL-40 as a novel diagnostic biomarker in Toxoplasmosis. Journal of Population Therapeutics and Clinical Pharmacology, 29(02). https://doi.org/10.47750/jptcp.2022.932
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How to Cite
Farah Abd AL-Zahra Shahad, Ahmed A. Mohammed, & Ghaith Ali Jasim. (2022). YKL-40 as a novel diagnostic biomarker in Toxoplasmosis. Journal of Population Therapeutics and Clinical Pharmacology, 29(02). https://doi.org/10.47750/jptcp.2022.932