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Published in: BMC Infectious Diseases 1/2021

Open Access 01-12-2021 | Toxoplasmosis | Research article

Latent Toxoplasma gondii infections are associated with elevated biomarkers of inflammation and vascular injury

Authors: Andrey I. Egorov, Reagan R. Converse, Shannon M. Griffin, Jennifer N. Styles, Elizabeth Sams, Edward Hudgens, Timothy J. Wade

Published in: BMC Infectious Diseases | Issue 1/2021

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Abstract

Background

Toxoplasma gondii is a protozoan parasite that infects cats as definitive hosts and other warm-blooded animals including humans as intermediate hosts. It forms infectious cysts in the brain, muscle and other tissues establishing life-long latent infection. Approximately 10% of the US population is infected. While latent infections are largely asymptomatic, they are associated with neurological deficits and elevated risks of neuropsychiatric diseases.

Methods

This cross-sectional epidemiological study investigated associations of T. gondii infections with biomarkers of inflammation and vascular injury: soluble intercellular adhesion molecule 1 (ICAM-1), soluble vascular cell adhesion molecule 1 (VCAM-1), C-reactive protein (CRP), and serum amyloid A (SAA). Serum samples from 694 adults in the Raleigh-Durham-Chapel Hill, North Carolina metropolitan area were tested for IgG antibody response to T. gondii, and for the above biomarkers using commercially available assays.

Results

T. gondii seroprevalence rate in this sample was 9.7%. Seropositivity was significantly associated with 11% (95% confidence limits 4, 20%) greater median levels of VCAM-1 (p = 0.003), and marginally significantly with 9% (1, 17%), and 36% (1, 83%) greater median levels of ICAM-1, and CRP, respectively (p = 0.04 for each) after adjusting for sociodemographic and behavioral covariates, while the 23% (− 7, 64%) adjusted effect on SAA was not statistically significant (p = 0.15).

Conclusions

Latent infections with T. gondii are associated with elevated biomarkers of chronic inflammation and vascular injury that are also known to be affected by ambient air pollution.
Literature
1.
go back to reference An Z, Jin Y, Li J, Li W, Wu W. Impact of particulate air pollution on cardiovascular health. Curr Allergy Asthma Rep. 2018;18:15.PubMedCrossRef An Z, Jin Y, Li J, Li W, Wu W. Impact of particulate air pollution on cardiovascular health. Curr Allergy Asthma Rep. 2018;18:15.PubMedCrossRef
2.
go back to reference Attademo L, Bernardini F, Garinella R, Compton MT. Environmental pollution and risk of psychotic disorders: a review of the science to date. Schizophr Res. 2017;181:55–9.PubMedCrossRef Attademo L, Bernardini F, Garinella R, Compton MT. Environmental pollution and risk of psychotic disorders: a review of the science to date. Schizophr Res. 2017;181:55–9.PubMedCrossRef
3.
go back to reference Barragan A, Brossier F, Sibley LD. Transepithelial migration of toxoplasma gondii involves an interaction of intercellular adhesion molecule 1 (ICAM-1) with the parasite adhesin MIC2. Cell Microbiol. 2005;7:561–8.PubMedCrossRef Barragan A, Brossier F, Sibley LD. Transepithelial migration of toxoplasma gondii involves an interaction of intercellular adhesion molecule 1 (ICAM-1) with the parasite adhesin MIC2. Cell Microbiol. 2005;7:561–8.PubMedCrossRef
4.
go back to reference Baumann R, Gube M, Markert A, Davatgarbenam S, Kossack V, Gerhards B, Kraus T, Brand P. Systemic serum amyloid a as a biomarker for exposure to zinc and / or copper-containing metal fumes. J Expo Sci Environ Epidemiol. 2018;28:84–91. Baumann R, Gube M, Markert A, Davatgarbenam S, Kossack V, Gerhards B, Kraus T, Brand P. Systemic serum amyloid a as a biomarker for exposure to zinc and / or copper-containing metal fumes. J Expo Sci Environ Epidemiol. 2018;28:84–91.
5.
go back to reference Berrett AN, Gale SD, Erickson LD, Thacker EL, Brown BL, Hedges DW. Toxoplasma gondii seropositivity and substance use in US adults. Folia Parasitol. 2018;65:1–11. Berrett AN, Gale SD, Erickson LD, Thacker EL, Brown BL, Hedges DW. Toxoplasma gondii seropositivity and substance use in US adults. Folia Parasitol. 2018;65:1–11.
6.
go back to reference Bind M-A, Baccarelli A, Zanobetti A, Tarantini L, Suh H, Vokonas P, Schwartz J. Air pollution and markers of coagulation, inflammation, and endothelial function: associations and epigene-environment interactions in an elderly cohort. Epidemiology. 2013;23:332–40.CrossRef Bind M-A, Baccarelli A, Zanobetti A, Tarantini L, Suh H, Vokonas P, Schwartz J. Air pollution and markers of coagulation, inflammation, and endothelial function: associations and epigene-environment interactions in an elderly cohort. Epidemiology. 2013;23:332–40.CrossRef
7.
go back to reference Bind MA, Baccarelli A, Zanobetti A, Tarantini L, Suh H, Vokonas P, Schwartz J. Air pollution and markers of coagulation, inflammation, and endothelial function: associations and epigene-environment interactions in an elderly cohort. Epidemiology. 2012;23:332–40.PubMedPubMedCentralCrossRef Bind MA, Baccarelli A, Zanobetti A, Tarantini L, Suh H, Vokonas P, Schwartz J. Air pollution and markers of coagulation, inflammation, and endothelial function: associations and epigene-environment interactions in an elderly cohort. Epidemiology. 2012;23:332–40.PubMedPubMedCentralCrossRef
8.
go back to reference Birgisdottir A, Asbjornsdottir H, Cook E, Gislason D, Jansson C, Olafsson I, Gislason T, Jogi R, Thjodleifsson B. Seroprevalence of Toxoplasma gondii in Sweden, Estonia and Iceland. Scand J Infect Dis. 2006;38:625–31.PubMedCrossRef Birgisdottir A, Asbjornsdottir H, Cook E, Gislason D, Jansson C, Olafsson I, Gislason T, Jogi R, Thjodleifsson B. Seroprevalence of Toxoplasma gondii in Sweden, Estonia and Iceland. Scand J Infect Dis. 2006;38:625–31.PubMedCrossRef
9.
go back to reference Blankenberg S, Barbaux S, Tiret L. Adhesion molecules and atherosclerosis. Atherosclerosis. 2003;170:191–203.PubMedCrossRef Blankenberg S, Barbaux S, Tiret L. Adhesion molecules and atherosclerosis. Atherosclerosis. 2003;170:191–203.PubMedCrossRef
10.
go back to reference Boillat M, Hammoudi PM, Dogga SK, Pages S, Goubran M, Rodriguez I, Soldati-Favre D. Neuroinflammation-associated aspecific manipulation of mouse predator fear by Toxoplasma gondii. Cell Rep. 2020;30:320–334.e6.PubMedPubMedCentralCrossRef Boillat M, Hammoudi PM, Dogga SK, Pages S, Goubran M, Rodriguez I, Soldati-Favre D. Neuroinflammation-associated aspecific manipulation of mouse predator fear by Toxoplasma gondii. Cell Rep. 2020;30:320–334.e6.PubMedPubMedCentralCrossRef
11.
go back to reference Burgdorf KS, Trabjerg BB, Pedersen MG, Nissen J, Banasik K, Pedersen OB, Sorensen E, Nielsen KR, Larsen MH, Erikstrup C, Bruun-Rasmussen P, Westergaard D, Thorner LW, Hjalgrim H, Paarup HM, Brunak S, Pedersen CB, Torrey EF, Werge T, Mortensen PB, Yolken RH, Ullum H. Large-scale study of toxoplasma and Cytomegalovirus shows an association between infection and serious psychiatric disorders. Brain Behav Immun. 2019;79:152–8.PubMedCrossRef Burgdorf KS, Trabjerg BB, Pedersen MG, Nissen J, Banasik K, Pedersen OB, Sorensen E, Nielsen KR, Larsen MH, Erikstrup C, Bruun-Rasmussen P, Westergaard D, Thorner LW, Hjalgrim H, Paarup HM, Brunak S, Pedersen CB, Torrey EF, Werge T, Mortensen PB, Yolken RH, Ullum H. Large-scale study of toxoplasma and Cytomegalovirus shows an association between infection and serious psychiatric disorders. Brain Behav Immun. 2019;79:152–8.PubMedCrossRef
12.
go back to reference Chang CH, Lane HY, Liu CY, Cheng PC, Chen SJ, Lin CH. C-reactive protein is associated with severity of thought and language dysfunction in patients with schizophrenia. Neuropsychiatr Dis Treat. 2019;15:2621–7.PubMedPubMedCentralCrossRef Chang CH, Lane HY, Liu CY, Cheng PC, Chen SJ, Lin CH. C-reactive protein is associated with severity of thought and language dysfunction in patients with schizophrenia. Neuropsychiatr Dis Treat. 2019;15:2621–7.PubMedPubMedCentralCrossRef
14.
go back to reference Cook TB, Brenner LA, Cloninger CR, Langenberg P, Igbide A, Giegling I, Hartmann AM, Konte B, Friedl M, Brundin L, Groer MW, Can A, Rujescu D, Postolache TT. “Latent” infection with Toxoplasma gondii: association with trait aggression and impulsivity in healthy adults. J Psychiatr Res. 2015;60:87–94.PubMedCrossRef Cook TB, Brenner LA, Cloninger CR, Langenberg P, Igbide A, Giegling I, Hartmann AM, Konte B, Friedl M, Brundin L, Groer MW, Can A, Rujescu D, Postolache TT. “Latent” infection with Toxoplasma gondii: association with trait aggression and impulsivity in healthy adults. J Psychiatr Res. 2015;60:87–94.PubMedCrossRef
15.
go back to reference Costello H, Gould RL, Abrol E, Howard R. Systematic review and meta-analysis of the association between peripheral inflammatory cytokines and generalised anxiety disorder. BMJ Open. 2019;9:e027925.PubMedPubMedCentralCrossRef Costello H, Gould RL, Abrol E, Howard R. Systematic review and meta-analysis of the association between peripheral inflammatory cytokines and generalised anxiety disorder. BMJ Open. 2019;9:e027925.PubMedPubMedCentralCrossRef
16.
go back to reference Dabritz HA, Miller MA, Atwill ER, Gardner IA, Leutenegger CM, Melli AC, Conrad PA. Detection of Toxoplasma gondii-like oocysts in cat feces and estimates of the environmental oocyst burden. J Am Vet Med Assoc. 2007;231:1676–84.PubMedCrossRef Dabritz HA, Miller MA, Atwill ER, Gardner IA, Leutenegger CM, Melli AC, Conrad PA. Detection of Toxoplasma gondii-like oocysts in cat feces and estimates of the environmental oocyst burden. J Am Vet Med Assoc. 2007;231:1676–84.PubMedCrossRef
17.
go back to reference Deckert M, Lutjen S, Leuker CE, Kwok LY, Strack A, Muller W, Wagner N, Schluter D. Mice with neonatally induced inactivation of the vascular cell adhesion molecule-1 fail to control the parasite in toxoplasma encephalitis. Eur J Immunol. 2003;33:1418–28.PubMedCrossRef Deckert M, Lutjen S, Leuker CE, Kwok LY, Strack A, Muller W, Wagner N, Schluter D. Mice with neonatally induced inactivation of the vascular cell adhesion molecule-1 fail to control the parasite in toxoplasma encephalitis. Eur J Immunol. 2003;33:1418–28.PubMedCrossRef
19.
go back to reference Duan J, Cheng Q, Luo X, Bai L, Zhang H, Wang S, Xu Z, Gao J, Zhang Y, Su H. Is the serious ambient air pollution associated with increased admissions for schizophrenia? Sci Total Environ. 2018;644:14–9.PubMedCrossRef Duan J, Cheng Q, Luo X, Bai L, Zhang H, Wang S, Xu Z, Gao J, Zhang Y, Su H. Is the serious ambient air pollution associated with increased admissions for schizophrenia? Sci Total Environ. 2018;644:14–9.PubMedCrossRef
20.
go back to reference Dubey JP, Ferreira LR, Alsaad M, Verma SK, Alves DA, Holland GN, Mcconkey GA. 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. 2016;11:e0156255.PubMedPubMedCentralCrossRef Dubey JP, Ferreira LR, Alsaad M, Verma SK, Alves DA, Holland GN, Mcconkey GA. 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. 2016;11:e0156255.PubMedPubMedCentralCrossRef
21.
go back to reference Egorov AI, Converse R, Griffin SM, Styles J, Klein E, Sams E, Hudgens E, Wade TJ. Environmental risk factors for Toxoplasma gondii infections and the impact of latent infections on allostatic load in residents of Central North Carolina. BMC Infect Dis. 2018;18:421.PubMedPubMedCentralCrossRef Egorov AI, Converse R, Griffin SM, Styles J, Klein E, Sams E, Hudgens E, Wade TJ. Environmental risk factors for Toxoplasma gondii infections and the impact of latent infections on allostatic load in residents of Central North Carolina. BMC Infect Dis. 2018;18:421.PubMedPubMedCentralCrossRef
22.
go back to reference Egorov AI, Griffin SM, Converse RR, Styles JN, Sams EA, Wilson A, Jackson LE, Wade TJ. Vegetated land cover near residence is associated with reduced allostatic load and improved biomarkers of neuroendocrine, metabolic and immune functions. Environ Res. 2017;158:508–21.PubMedPubMedCentralCrossRef Egorov AI, Griffin SM, Converse RR, Styles JN, Sams EA, Wilson A, Jackson LE, Wade TJ. Vegetated land cover near residence is associated with reduced allostatic load and improved biomarkers of neuroendocrine, metabolic and immune functions. Environ Res. 2017;158:508–21.PubMedPubMedCentralCrossRef
23.
go back to reference El-Sayed NM, Ismail KA, Ahmed SA-E-G, Ezz-El-Din HM, Azzam HME-E-D. Possible association between Toxoplasma gondii infection and schizophrenia: Egyptian study. Infect Dis Clin Pract. 2012;20:394–9. El-Sayed NM, Ismail KA, Ahmed SA-E-G, Ezz-El-Din HM, Azzam HME-E-D. Possible association between Toxoplasma gondii infection and schizophrenia: Egyptian study. Infect Dis Clin Pract. 2012;20:394–9.
24.
go back to reference Fekadu A, Shibre T, Cleare AJ. Toxoplasmosis as a cause for behaviour disorders--overview of evidence and mechanisms. Folia Parasitol. 2010;57:105–13.CrossRef Fekadu A, Shibre T, Cleare AJ. Toxoplasmosis as a cause for behaviour disorders--overview of evidence and mechanisms. Folia Parasitol. 2010;57:105–13.CrossRef
25.
go back to reference Furtado JM, Bharadwaj AS, Ashander LM, Olivas A, Smith JR. Migration of toxoplasma gondii-infected dendritic cells across human retinal vascular endothelium. Invest Ophthalmol Vis Sci. 2012;53:6856–62.PubMedPubMedCentralCrossRef Furtado JM, Bharadwaj AS, Ashander LM, Olivas A, Smith JR. Migration of toxoplasma gondii-infected dendritic cells across human retinal vascular endothelium. Invest Ophthalmol Vis Sci. 2012;53:6856–62.PubMedPubMedCentralCrossRef
26.
go back to reference Haapakoski R, Mathieu J, Ebmeier KP, Alenius H, Kivimaki M. Cumulative meta-analysis of interleukins 6 and 1beta, tumour necrosis factor alpha and C-reactive protein in patients with major depressive disorder. Brain Behav Immun. 2015;49:206–15.PubMedPubMedCentralCrossRef Haapakoski R, Mathieu J, Ebmeier KP, Alenius H, Kivimaki M. Cumulative meta-analysis of interleukins 6 and 1beta, tumour necrosis factor alpha and C-reactive protein in patients with major depressive disorder. Brain Behav Immun. 2015;49:206–15.PubMedPubMedCentralCrossRef
27.
go back to reference Hermes G, Ajioka JW, Kelly KA, Mui E, Roberts F, Kasza K, Mayr T, Kirisits MJ, Wollmann R, Ferguson DJ, Roberts CW, Hwang JH, Trendler T, Kennan RP, Suzuki Y, Reardon C, Hickey WF, Chen L, Mcleod R. Neurological and behavioral abnormalities, ventricular dilatation, altered cellular functions, inflammation, and neuronal injury in brains of mice due to common, persistent, parasitic infection. J Neuroinflammation. 2008;5:48.PubMedPubMedCentralCrossRef Hermes G, Ajioka JW, Kelly KA, Mui E, Roberts F, Kasza K, Mayr T, Kirisits MJ, Wollmann R, Ferguson DJ, Roberts CW, Hwang JH, Trendler T, Kennan RP, Suzuki Y, Reardon C, Hickey WF, Chen L, Mcleod R. Neurological and behavioral abnormalities, ventricular dilatation, altered cellular functions, inflammation, and neuronal injury in brains of mice due to common, persistent, parasitic infection. J Neuroinflammation. 2008;5:48.PubMedPubMedCentralCrossRef
28.
go back to reference Hosseininejad Z, Sharif M, Sarvi S, Amouei A, Hosseini SA, Nayeri Chegeni T, Anvari D, Saberi R, Gohardehi S, Mizani A, Sadeghi M, Daryani A. Toxoplasmosis seroprevalence in rheumatoid arthritis patients: a systematic review and meta-analysis. PLoS Negl Trop Dis. 2018;12:e0006545.PubMedPubMedCentralCrossRef Hosseininejad Z, Sharif M, Sarvi S, Amouei A, Hosseini SA, Nayeri Chegeni T, Anvari D, Saberi R, Gohardehi S, Mizani A, Sadeghi M, Daryani A. Toxoplasmosis seroprevalence in rheumatoid arthritis patients: a systematic review and meta-analysis. PLoS Negl Trop Dis. 2018;12:e0006545.PubMedPubMedCentralCrossRef
29.
go back to reference House PK, Vyas A, Sapolsky R. Predator cat odors activate sexual arousal pathways in brains of Toxoplasma gondii infected rats. PLoS One. 2011;6:e23277.PubMedPubMedCentralCrossRef House PK, Vyas A, Sapolsky R. Predator cat odors activate sexual arousal pathways in brains of Toxoplasma gondii infected rats. PLoS One. 2011;6:e23277.PubMedPubMedCentralCrossRef
30.
go back to reference Jones J, Lopez A, Wilson M. Congenital toxoplasmosis. Am Fam Physician. 2003;67:2131–8.PubMed Jones J, Lopez A, Wilson M. Congenital toxoplasmosis. Am Fam Physician. 2003;67:2131–8.PubMed
31.
go back to reference Jones JL, Kruszon-Moran D, Rivera HN, Price C, Wilkins PP. Toxoplasma gondii seroprevalence in the United States 2009-2010 and comparison with the past two decades. Am J Trop Med Hyg. 2014;90:1135–9.PubMedPubMedCentralCrossRef Jones JL, Kruszon-Moran D, Rivera HN, Price C, Wilkins PP. Toxoplasma gondii seroprevalence in the United States 2009-2010 and comparison with the past two decades. Am J Trop Med Hyg. 2014;90:1135–9.PubMedPubMedCentralCrossRef
32.
go back to reference Jones JL, Kruszon-Moran D, Wilson M, Mcquillan G, Navin T, Mcauley JB. Toxoplasma gondii infection in the United States: seroprevalence and risk factors. Am J Epidemiol. 2001;154:357–65.PubMedCrossRef Jones JL, Kruszon-Moran D, Wilson M, Mcquillan G, Navin T, Mcauley JB. Toxoplasma gondii infection in the United States: seroprevalence and risk factors. Am J Epidemiol. 2001;154:357–65.PubMedCrossRef
33.
go back to reference Kaptoge S, Angelantonio ED, Pennells L. C-reactive protein, fibrinogen, and cardiovascular disease prediction. N Engl J Med. 2012;367:1310–20.PubMedCrossRef Kaptoge S, Angelantonio ED, Pennells L. C-reactive protein, fibrinogen, and cardiovascular disease prediction. N Engl J Med. 2012;367:1310–20.PubMedCrossRef
34.
go back to reference Lelu M, Villena I, Darde ML, Aubert D, Geers R, Dupuis E, Marnef F, Poulle ML, Gotteland C, Dumetre A, Gilot-Fromont E. Quantitative estimation of the viability of Toxoplasma gondii oocysts in soil. Appl Environ Microbiol. 2012;78:5127–32.PubMedPubMedCentralCrossRef Lelu M, Villena I, Darde ML, Aubert D, Geers R, Dupuis E, Marnef F, Poulle ML, Gotteland C, Dumetre A, Gilot-Fromont E. Quantitative estimation of the viability of Toxoplasma gondii oocysts in soil. Appl Environ Microbiol. 2012;78:5127–32.PubMedPubMedCentralCrossRef
35.
go back to reference Ley K. Adhesion molecules: function and inhibition, vol. 99; 2007. p. 141–2. Ley K. Adhesion molecules: function and inhibition, vol. 99; 2007. p. 141–2.
36.
go back to reference Majidiani H, Dalvand S, Daryani A, Galvan-Ramirez ML, Foroutan-Rad M. Is chronic toxoplasmosis a risk factor for diabetes mellitus? A systematic review and meta-analysis of case-control studies. Braz J Infect Dis. 2016;20:605–9.PubMedCrossRef Majidiani H, Dalvand S, Daryani A, Galvan-Ramirez ML, Foroutan-Rad M. Is chronic toxoplasmosis a risk factor for diabetes mellitus? A systematic review and meta-analysis of case-control studies. Braz J Infect Dis. 2016;20:605–9.PubMedCrossRef
37.
go back to reference Miller BJ, Culpepper N, Rapaport MH. C-reactive protein levels in schizophrenia: a review and meta-analysis. Clin Schizophr Relat Psychoses. 2014;7:223–30.PubMedCrossRef Miller BJ, Culpepper N, Rapaport MH. C-reactive protein levels in schizophrenia: a review and meta-analysis. Clin Schizophr Relat Psychoses. 2014;7:223–30.PubMedCrossRef
39.
go back to reference Nayeri Chegeni T, Sarvi S, Amouei A, Moosazadeh M, Hosseininejad Z, S AA, Daryani A. Relationship between toxoplasmosis and obsessive compulsive disorder: a systematic review and meta-analysis. PLoS Negl Trop Dis. 2019a;13:e0007306.PubMedPubMedCentralCrossRef Nayeri Chegeni T, Sarvi S, Amouei A, Moosazadeh M, Hosseininejad Z, S AA, Daryani A. Relationship between toxoplasmosis and obsessive compulsive disorder: a systematic review and meta-analysis. PLoS Negl Trop Dis. 2019a;13:e0007306.PubMedPubMedCentralCrossRef
40.
go back to reference Nayeri Chegeni T, Sarvi S, Moosazadeh M, Sharif M, Aghayan SA, Amouei A, Hosseininejad Z, Daryani A. Is Toxoplasma gondii a potential risk factor for Alzheimer's disease? A systematic review and meta-analysis. Microb Pathog. 2019b;137:103751.PubMedCrossRef Nayeri Chegeni T, Sarvi S, Moosazadeh M, Sharif M, Aghayan SA, Amouei A, Hosseininejad Z, Daryani A. Is Toxoplasma gondii a potential risk factor for Alzheimer's disease? A systematic review and meta-analysis. Microb Pathog. 2019b;137:103751.PubMedCrossRef
41.
go back to reference Nguyen TT, Dev SI, Chen G, Liou SC, Martin AS, Irwin MR, Carroll JE, Tu X, Jeste DV, Eyler LT. Abnormal levels of vascular endothelial biomarkers in schizophrenia. Eur Arch Psychiatry Clin Neurosci. 2018;268:849–60.PubMedCrossRef Nguyen TT, Dev SI, Chen G, Liou SC, Martin AS, Irwin MR, Carroll JE, Tu X, Jeste DV, Eyler LT. Abnormal levels of vascular endothelial biomarkers in schizophrenia. Eur Arch Psychiatry Clin Neurosci. 2018;268:849–60.PubMedCrossRef
42.
go back to reference Poirotte C, Kappeler PM, Ngoubangoye B, Bourgeois S, Moussodji M, Charpentier MJ. Morbid attraction to leopard urine in toxoplasma-infected chimpanzees. Curr Biol. 2016;26:R98–9.PubMedCrossRef Poirotte C, Kappeler PM, Ngoubangoye B, Bourgeois S, Moussodji M, Charpentier MJ. Morbid attraction to leopard urine in toxoplasma-infected chimpanzees. Curr Biol. 2016;26:R98–9.PubMedCrossRef
43.
go back to reference Qiu H, Zhu X, Wang L, Pan J, Pu X, Zeng X, Zhang L, PENG Z, ZHOU L. Attributable risk of hospital admissions for overall and specific mental disorders due to particulate matter pollution: a time-series study in Chengdu, China. Environ Res. 2019;170:230–7.PubMedCrossRef Qiu H, Zhu X, Wang L, Pan J, Pu X, Zeng X, Zhang L, PENG Z, ZHOU L. Attributable risk of hospital admissions for overall and specific mental disorders due to particulate matter pollution: a time-series study in Chengdu, China. Environ Res. 2019;170:230–7.PubMedCrossRef
44.
go back to reference Radon K, Windstetter D, Eckart J, Dressel H, Leitritz L, Reichert J, Schmid M, Praml G, Schosser M, Von Mutius E, Nowak D. Farming exposure in childhood, exposure to markers of infections and the development of atopy in rural subjects. Clin Exp Allergy. 2004;34:1178–83.PubMedCrossRef Radon K, Windstetter D, Eckart J, Dressel H, Leitritz L, Reichert J, Schmid M, Praml G, Schosser M, Von Mutius E, Nowak D. Farming exposure in childhood, exposure to markers of infections and the development of atopy in rural subjects. Clin Exp Allergy. 2004;34:1178–83.PubMedCrossRef
45.
go back to reference Reus GZ, Fries GR, Stertz L, Badawy M, Passos IC, Barichello T, Kapczinski F, Quevedo J. The role of inflammation and microglial activation in the pathophysiology of psychiatric disorders. Neuroscience. 2015;300:141–54.PubMedCrossRef Reus GZ, Fries GR, Stertz L, Badawy M, Passos IC, Barichello T, Kapczinski F, Quevedo J. The role of inflammation and microglial activation in the pathophysiology of psychiatric disorders. Neuroscience. 2015;300:141–54.PubMedCrossRef
47.
go back to reference Sa Q, Ochiai E, Sengoku T, Wilson ME, Brogli M, Crutcher S, Michie SA, Xu B, Payne L, Wang X, Suzuki Y. VCAM-1/alpha4beta1 integrin interaction is crucial for prompt recruitment of immune T cells into the brain during the early stage of reactivation of chronic infection with Toxoplasma gondii to prevent toxoplasmic encephalitis. Infect Immun. 2014;82:2826–39.PubMedPubMedCentralCrossRef Sa Q, Ochiai E, Sengoku T, Wilson ME, Brogli M, Crutcher S, Michie SA, Xu B, Payne L, Wang X, Suzuki Y. VCAM-1/alpha4beta1 integrin interaction is crucial for prompt recruitment of immune T cells into the brain during the early stage of reactivation of chronic infection with Toxoplasma gondii to prevent toxoplasmic encephalitis. Infect Immun. 2014;82:2826–39.PubMedPubMedCentralCrossRef
48.
go back to reference Shwab EK, Jiang T, Pena HF, Gennari SM, Dubey JP, Su C. The ROP18 and ROP5 gene allele types are highly predictive of virulence in mice across globally distributed strains of Toxoplasma gondii. Int J Parasitol. 2016;46:141–6.PubMedCrossRef Shwab EK, Jiang T, Pena HF, Gennari SM, Dubey JP, Su C. The ROP18 and ROP5 gene allele types are highly predictive of virulence in mice across globally distributed strains of Toxoplasma gondii. Int J Parasitol. 2016;46:141–6.PubMedCrossRef
49.
go back to reference Styles JN, Converse RR, Griffin SM, Wade TJ, Klein E, Nylander-French LA, Stewart JR, Sams E, Hudgens E, Egorov AI. Human cytomegalovirus infections are associated with elevated biomarkers of vascular injury. Front Cell Infect Microbiol. 2020;10:334.PubMedPubMedCentralCrossRef Styles JN, Converse RR, Griffin SM, Wade TJ, Klein E, Nylander-French LA, Stewart JR, Sams E, Hudgens E, Egorov AI. Human cytomegalovirus infections are associated with elevated biomarkers of vascular injury. Front Cell Infect Microbiol. 2020;10:334.PubMedPubMedCentralCrossRef
50.
go back to reference Sutterland AL, Kuin A, Kuiper B, Van Gool T, Leboyer M, Fond G, De Haan L. Driving us mad: the association of Toxoplasma gondii with suicide attempts and traffic accidents - a systematic review and meta-analysis. Psychol Med. 2019;49:1608–23.PubMedCrossRef Sutterland AL, Kuin A, Kuiper B, Van Gool T, Leboyer M, Fond G, De Haan L. Driving us mad: the association of Toxoplasma gondii with suicide attempts and traffic accidents - a systematic review and meta-analysis. Psychol Med. 2019;49:1608–23.PubMedCrossRef
51.
go back to reference Suvisaari J, Torniainen-Holm M, Lindgren M, Harkanen T, Yolken RH. Toxoplasma gondii infection and common mental disorders in the Finnish general population. J Affect Disord. 2017;223:20–5.PubMedPubMedCentralCrossRef Suvisaari J, Torniainen-Holm M, Lindgren M, Harkanen T, Yolken RH. Toxoplasma gondii infection and common mental disorders in the Finnish general population. J Affect Disord. 2017;223:20–5.PubMedPubMedCentralCrossRef
52.
go back to reference Taubert A, Krull M, Zahner H, Hermosilla C. Toxoplasma gondii and Neospora caninum infections of bovine endothelial cells induce endothelial adhesion molecule gene transcription and subsequent PMN adhesion. Vet Immunol Immunopathol. 2006;112:272–83.PubMedCrossRef Taubert A, Krull M, Zahner H, Hermosilla C. Toxoplasma gondii and Neospora caninum infections of bovine endothelial cells induce endothelial adhesion molecule gene transcription and subsequent PMN adhesion. Vet Immunol Immunopathol. 2006;112:272–83.PubMedCrossRef
53.
go back to reference Tedford E, Mcconkey G. Neurophysiological changes induced by chronic Toxoplasma gondii infection. Pathogens. 2017;6:19. Tedford E, Mcconkey G. Neurophysiological changes induced by chronic Toxoplasma gondii infection. Pathogens. 2017;6:19.
54.
go back to reference Tibuakuu M, Michos ED, Navas-Acien A, Jones MR. Air pollution and cardiovascular disease: a focus on vulnerable populations worldwide. Curr Epidemiol Rep. 2018;5:370–8.PubMedPubMedCentralCrossRef Tibuakuu M, Michos ED, Navas-Acien A, Jones MR. Air pollution and cardiovascular disease: a focus on vulnerable populations worldwide. Curr Epidemiol Rep. 2018;5:370–8.PubMedPubMedCentralCrossRef
55.
go back to reference Tomasik J, Schultz TL, Kluge W, Yolken RH, Bahn S, Carruthers VB. Shared immune and repair markers during experimental toxoplasma chronic brain infection and schizophrenia. Schizophr Bull. 2016;42:386–95.PubMedCrossRef Tomasik J, Schultz TL, Kluge W, Yolken RH, Bahn S, Carruthers VB. Shared immune and repair markers during experimental toxoplasma chronic brain infection and schizophrenia. Schizophr Bull. 2016;42:386–95.PubMedCrossRef
56.
go back to reference Tyebji S, Seizova S, Hannan AJ, Tonkin CJ. Toxoplasmosis: a pathway to neuropsychiatric disorders. Neurosci Biobehav Rev. 2019;96:72–92.PubMedCrossRef Tyebji S, Seizova S, Hannan AJ, Tonkin CJ. Toxoplasmosis: a pathway to neuropsychiatric disorders. Neurosci Biobehav Rev. 2019;96:72–92.PubMedCrossRef
57.
go back to reference Vyas A, Kim SK, Giacomini N, Boothroyd JC, Sapolsky RM. Behavioral changes induced by toxoplasma infection of rodents are highly specific to aversion of cat odors. Proc Natl Acad Sci U S A. 2007;104:6442–7.PubMedPubMedCentralCrossRef Vyas A, Kim SK, Giacomini N, Boothroyd JC, Sapolsky RM. Behavioral changes induced by toxoplasma infection of rodents are highly specific to aversion of cat odors. Proc Natl Acad Sci U S A. 2007;104:6442–7.PubMedPubMedCentralCrossRef
59.
go back to reference Yuan Y. Multiple imputation using SAS software. J Stat Softw. 2011;45:1–25.CrossRef Yuan Y. Multiple imputation using SAS software. J Stat Softw. 2011;45:1–25.CrossRef
60.
go back to reference Zakynthinos E, Pappa N. Inflammatory biomarkers in coronary artery disease. J Cardiol. 2009;53:317–33.PubMedCrossRef Zakynthinos E, Pappa N. Inflammatory biomarkers in coronary artery disease. J Cardiol. 2009;53:317–33.PubMedCrossRef
Metadata
Title
Latent Toxoplasma gondii infections are associated with elevated biomarkers of inflammation and vascular injury
Authors
Andrey I. Egorov
Reagan R. Converse
Shannon M. Griffin
Jennifer N. Styles
Elizabeth Sams
Edward Hudgens
Timothy J. Wade
Publication date
01-12-2021
Publisher
BioMed Central
Published in
BMC Infectious Diseases / Issue 1/2021
Electronic ISSN: 1471-2334
DOI
https://doi.org/10.1186/s12879-021-05882-6

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