Toxoplasma gondii is a globally distributed protozoan that mainly causes health issues in the fetuses of pregnant women who have never been exposed to this parasite and patients with deficient immune systems. Except in these vulnerable populations, the primary infection generally goes unnoticed in most healthy individuals. Apart from transplant/transfusion, congenital transmission, direct contact with infected cats or their feces, and environmental contamination (i.e., oocysts in food, water, and soil) pathways, humans can acquire the parasite through consumption of animal tissues infected by T. gondii. This meta-analysis estimated the risk of acquiring T. gondii by consuming raw or undercooked meat, regardless of which animal species are eaten. Using a random-effect model, crude and adjusted pooled measures of association (risk and odds ratio) were estimated according to study design (cohort, case–control, and cross-sectional studies). The meta-analysis included measures of heterogeneity as well as quality rating scales for each study design. Our results suggest that individuals who eat raw or undercooked meat have, respectively, 1.2–1.3 times the risk and 1.7–3.0 times the odds of T. gondii infection compared to those who thoroughly cook meat, regardless of the animal species they consume. These results align with the current understanding that adequately cooking meat inactivates the parasite and decreases the risk of transmission. Seroprevalence ranged from 1.3% to 88.6%, while the proportion of individuals eating raw or undercooked meat fluctuated from 0.7% to 98.3% across the studies in the meta-analysis. These numbers reflect various preferences with regard to eating meat (i.e., eating tartar, sausages, or salamis) as well as individual, cultural and religious food habits, and personal awareness.
Get full access to this article
View all access options for this article.
References
1.
AchasB, TesfaH, ZelekeAJ, WorkuL, et al.Sero-prevalence of Toxoplasma gondii and associated risk factors among psychiatric outpatients attending University of Gondar Hospital, Northwest Ethiopia. BMC Infect Dis, 2019; 19:581.
2.
AielloAE, LarsonEL. Causal inference: The case of hygiene and health. Am J Infect Control, 2002; 30:503–511.
3.
AkturkHK, SotelloD, AmeriA, AbuzaidAS, et al.Toxoplasma infection in an immunocompetent host: Possible risk of living with multiple cats. Cureus, 2017; 9:e1103.
4.
Al-MohammadHI, AminTT, BalahaMH, Al-MoghannumMS. Toxoplasmosis among the pregnant women attending a Saudi maternity hospital: Seroprevalence and possible risk factors. Ann Trop Med Parasitol, 2010; 104:493–504.
5.
Alvarado-EsquivelC, Estrada-MartinezS, LiesenfeldO. Toxoplasma gondii infection in workers occupationally exposed to unwashed raw fruits and vegetables: A case control seroprevalence study. Parasit Vectors, 2011; 4:1–7.
6.
Alvarado-EsquivelC, Estrada-MartinezS, Pizarro-VillalobosH, Arce-QuinonesM, et al.Seroepidemiology of Toxoplasma gondii infection in general population in a northern Mexican city. J Parasitol, 2010a; 97:40–43.
7.
Alvarado-EsquivelC, Cruz-Magallanes HM, Esquivel-CruzR, Estrada-MartínezS, et al.Infection in human adults from three rural communities in Durango state, Mexico. J Parasitol, 2008; 94:811–816.
8.
Alvarado-EsquivelC, Pacheco-VegaSJ, Hernandez-TinocoJ, Saldana-SimentalDE, et al.Lack of association between Toxoplasma gondii infection and occupational exposure to animals. Eur J Microbiol Immunol, 2014a; 4:184–192.
9.
Alvarado-EsquivelC, Pacheco-VegaSJ, Hernandez-TinocoJ, Sanchez-AnguianoLF, et al.Seroprevalence of Toxoplasma gondii infection and associated risk factors in Huicholes in Mexico. Parasites Vectors, 2014b; 7:301.
10.
Alvarado-EsquivelC, Rojas-RiveraA, Estrada-MartinezS, Sifuentes-AlvarezA, et al.Seroepidemiology of Toxoplasma gondii infection in a Mennonite community in Durango State, Mexico. J Parasitol, 2010b; 96:941.
11.
Alvarado-EsquivelC, Torres-CastorenaA, LiesenfeldO, Estrada-MartinezS, et al.High seroprevalence of Toxoplasma gondii infection in a subset of Mexican patients with work accidents and low socioeconomic status. Parasites Vectors, 2012b; 5:13.
12.
Alvarado-EsquivelCL, LiesenfeldO, Burciaga-LopezBD, Ramos-NevarezA, et al.Seroepidemiology of Toxoplasma gondii infection in elderly people in a northern Mexican city. Vector Borne Zoonotic Dis, 2012a; 12:568–574.
13.
AwokeKN, NibretE, MunsheaA. Sero-prevalence and associated risk factors of Toxoplasma gondii infection among pregnant women attending antenatal care at Felege Hiwot Referral Hospital, northwest Ethiopia. Asian Pac J Trop Med, 2015; 8:549–554.
14.
BarilL, AncelleT, GouletV, ThulliezP, et al.Risk factors for Toxoplasma infection in pregnancy: A case-control study in France. Scand J Infect Dis, 1999; 31:305–309.
15.
BellucoS, MancinM, ConficoniD, SimonatoG, et al.Investigating the determinants of Toxoplasma gondii prevalence in meat: A systematic review and meta-regression. PLoS One, 2016; 11:1–24.
16.
BiedermannK, FleppM, FierzW, Joller-JemelkaH, et al.Pregnancy, immunosuppression and reactivation of latent toxoplasmosis. J Perinat Med, 1995; 23:191–203.
17.
BlanchetC, RochetteL. Nutrition and food consumption among the Inuit ofNunavik. Nunavik Inuit HealthSurvey. 2004. Qanuippitaa? How are we? 2008. Available at https://www.inspq.qc.ca/sites/default/files/publications/762_esi_nutrition_report_ma.pdf
18.
BlandJM, AltmanDG. Multiple significance tests: The Bonferroni method. Br Med J, 1995; 310:170.
19.
BobicB, JevremovicI, MarinkovicJ, SibalicD, et al.Risk factors for Toxoplasma infection in a reproductive age female population in the area of Belgrade, Yugoslavia. Eur J Epidemiol, 1998; 14:605–610.
20.
BobicB, NikolicA, KlunI, VujanicM, et al.Undercooked meat consumption remains the major risk factor for Toxoplasma infection in Serbia. Parassitologia, 2007; 49:227–230.
21.
BorensteinM, HedgesLV, HigginsJP, RothstreinHR. Introduction to Meta-Analysis. United Kingdom: John Wiley and Sons, Ltd., 2009.
22.
BuffolanoW, GilbertRE, HollandFJ, FrattaD, et al.Risk factors for recent toxoplasma infection in pregnant women in Naples. Epidemiol Infect, 1996; 116:347–351.
23.
ChiangTY, KuoMC, ChenCH, YangJY, et al.Risk factors for acute Toxoplasma gondii diseases in Taiwan: A population-based case-control study. PLoS One, 2014; 9:e90880.
24.
CongW, DongW, BaiL, WangXY, et al.Seroprevalence and associated risk factors of Toxoplasma gondii infection in psychiatric patients: A case-control study in eastern China. Epidemiol Infect, 2015a; 143:3103–3109.
25.
CongW, LiuGH, MengQF, DongW, et al.Toxoplasma gondii infection in cancer patients: Prevalence, risk factors, genotypes and association with clinical diagnosis. Cancer Lett, 2015b; 359:307–313.
26.
CongWD, DongXY, MengQF, ZhouN, et al.Toxoplasma gondii infection in pregnant women: A seroprevalence and case-control study in Eastern China. Epidemiol Infect, 2015c; 143:3103–3109.
27.
CookAJG, GilbertRE, BuffolanoW, ZuffereyJ, et al.Sources of toxoplasma infection in pregnant women: European multicentre case-control study. European Research Network on congenital toxoplasmosis. Br Med J, 2000; 321:14–27.
28.
CutlerDM, Lleras-MuneyA. Understanding differences in health behaviors by education. J Health Econ, 2010; 29:1–28.
29.
DesmontsG, CouvreurJ, AlisonF, BaudelotJ, et al.Epidemiological study on toxoplasmosis: The influence of cooking slaughter-animal meat on the incidence of human infection. Rev Fr Etud Clin Biol, 1965; 10:952.
30.
DubeyJP. Toxoplasma gondii oocyst survival under defined temperatures. J Parasitol, 1998; 84:862–865.
31.
DubeyJP. The scientific basis for prevention of Toxoplasma gondii infection: Studies on tissue cyst survival, risk factors and hygiene measures. In: PetersenE, Ambroise-ThomasP, eds. Congenital Toxoplasmosis: Scientific Background, Clinical Management and Control. France: Springer-Velag, 2000:271–275.
32.
DubeyJP. Toxoplasma gondii of animals and humans. Boca Ratton, CRC Press, 2010.
33.
DubeyJP, KotulaA, ShararA, AndrewsCD, et al.Effect of high temperature on infectivity of Toxoplasma gondii tissue cysts in pork. J Parasitol, 1990; 76:201–204.
34.
EggerM, Davey SmithG, SchneiderM, MinderC. Bias in meta-analysis detected by a simple, graphical test. Br Med J, 1997; 315:629–634.
35.
EggerM, SchneiderM, SmithGD. Meta-analysis: Spurious precision? Meta-analysis of observational studies. Br Med J, 1998; 316:140–144.
36.
EgorovAI, ConverseR, GriffinSM, StylesJ, et al.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.
37.
ElmsthalS, GullbergB. Bias in diet assessment methods—Consequences of collinearity and measurement errors on power and observed relative risks. Int J Epidemiol, 1997; 26:1071–1079.
38.
FanCK, LiaoCW, KaoTC, LuJL, et al.Toxoplasma gondii infection: Relationship between seroprevalence and risk factors among inhabitants in two offshore islands from Taiwan. Acta Med Okayama, 2001; 55:301–308.
39.
FanCK, SuKE, WuGH, ChiouHY. Seroepidemiology of Toxoplasma gondii infection among two mountain aboriginal populations and Southeast Asian laborers in Taiwan. Journal of Parasitology, 2002; 88:411–414.
40.
FlattA, ShettyN. Seroprevalence and risk factors for toxoplasmosis among antenatal women in London: A re-examination of risk in an ethnically diverse population. Eur J Public Health, 2013; 23:648–652.
41.
FlegrJ, HrdaS, TachezyJ. The role of psychological factors in questionnaire-based studies on routes of human toxoplasmosis transmission. Central Eur J Public Health, 1998; 6:45–50.
42.
Fricker-HidalgoH, CimonB, ChemlaC, DardeML, et al.Toxoplasma seroconversion with negative or transient immunoglobulin M in pregnant women: Myth or reality? A French multicenter retrospective study. J Clin Microbiol, 2013; 51:2103–2111.
43.
FuCJ, ChuangTW, LinHS, WuCH, et al.Toxoplasma gondii infection: Seroprevalence and associated risk factors among primary school children in the capital area of the Republic of the Marshall Islands. Jpn J Infect Dis, 2014; 67:405–410.
44.
GebremedhinEZ, AgonafirA, TessemaTS, TilahunG, et al.Seroepidemiological study of ovine toxoplasmosis in East and West Shewa Zones of Oromia Regional State, Central Ethiopia. BMC Vet Res, 2013; 9:117.
45.
GelayeW, KebedeT, HailuA. High prevalence of anti-toxoplasma antibodies and absence of Toxoplasma gondii infection risk factors among pregnant women attending routine antenatal care in two Hospitals of Addis Ababa, Ethiopia. Int J Infect Dis, 2015; 34:41–45.
46.
GyangVPA, AkinwaleOP, LeeYL, ChuangTW, et al.Toxoplasma gondii infection: Seroprevalence and associated risk factors among primary schoolchildren in Lagos City, Southern Nigeria. Rev Soc Bras Med Trop, 2015; 48:56–63.
47.
HamzaH, El-TaweelH, Abou-HolwS, KhalilS, et al.Toxoplasma gondii seropositivity in renal patients: Rate, pattern, predictors and related morbidity. J Egypt Soc Parasitol, 2015; 45:7–15.
48.
HerreroL, GraciaMJ, Perez-ArquillueC, LazaroR, et al.Toxoplasma gondii in raw and dry-cured ham: The influence of the curing process. Food Microbiol, 2017; 65:213–220.
49.
HofhuisA, Van PeltW, Van DuynhovenYT, NijhuisCDM, et al.Decreased prevalence and age-specific risk factors for Toxoplasma gondii IgG antibodies in The Netherlands between 1995/1996 and 2006/2007. Epidemiol Infect, 2011; 139:530–538.
50.
JiangRL, ZhaoQ, JiangJ, ChenXL, et al.Toxoplasma gondii infection in dustmen in Northeastern China: A case-control seroprevalence study. BioMed Res Int, 2018; 2018:1–15.
51.
JonesJL, DargelasV, RobertsJ, PressC, et al.Risk factors for Toxoplasma gondii infection in the United States. Clin Infect Dis, 2009; 49:878–884.
KapperudG, JenumPA, Stray-PedersenB, MelbyKK, et al.Risk factors for Toxoplasma gondii infection in pregnancy: Results of a prospective case-control study in Norway. Am J Epidemiol, 1996; 144:405–412.
55.
KijlstraA, JongertE. Control of the risk of human toxoplasmosis transmitted by meat. Int J Parasitol, 2008; 38:1359–1370.
56.
KolbekovaP, KourbatovaE, NovotnaM, KodymP, et al.New and old risk-factors for Toxoplasma gondii infection: Prospective cross-sectional study among military personnel in the Czech Republic. Clin Microbiol Infect, 2007; 13:1012–1017.
57.
LiHL, DongL, LiQ, ZhangL, et al.Seroepidemiology of Toxoplasma gondii infection in Bai and Han ethnic groups in southwestern China. Epidemiol Infect, 2015; 143:881–886.
58.
LiuQ, WangZ-D, HuangS-Y, ZhuXQ. Diagnosis of toxoplasmosis and typing og Toxoplasma gondii. Parasit Vectors, 2015; 28:292.
59.
LiuQ, WeiF, GaoS, JiangL, et al.Toxoplasma gondii infection in pregnant women in China. Trans R Soc Trop Med Hyg, 2009; 103:162–166.
60.
LopesAP, DubeyJP, MoutinhoO, GargateMJ, et al.Seroepidemiology of Toxoplasma gondii infection in women from the North of Portugal in their childbearing years. Epidemiol Infect, 2012; 140:872–877.
61.
MahmoudvandH, Saedi DezakiE, SoleimaniS, BaneshiMR, et al.Seroprevalence and risk factors of Toxoplasma gondii infection among healthy blood donors in south-east of Iran. Parasite Immunol, 2015; 37:362–367.
MeirelesLR, EkmanCC, AndradeHF, LunaEJ. Human toxoplasmosis outbreaks and the agent infecting form: Findings from a systematic review. Rev Inst Med Trop Sao Paulo, 2015; 57:369–376.
64.
MessererL, BouzbidS, GourbdjiE, MansouriR, et al.[Seroprevalence of toxoplasmosis in pregnant women in Annaba, Algeria]. Rev Épidemiol Sante Publique, 2014; 62:160–165.
65.
MickeyRM, GreenlandS. The impact of confounder selection criteria on effect estimation. Am J Epidemiol, 1989; 129:125–137.
66.
MoherD, ShamseerL, ClarkeM, GhersiD, et al.Preferred reporting items for systematic review and meta-analysis protocols (PRISMA-P) 2015 statement. Syst Rev, 2015; 4:1–9.
MurebwayireE, NjanaakeK, NgabonzizaJC, NjunwaKJ, et al.Seroprevalence and risk factors of Toxoplasma gondii infection among pregnant women attending antenatal care in Kigali, Rwanda. Tanzania J Health Res, 2017; 19(1). https://doi.org/10.4314/thrb.v19i1.2
69.
MurrayR, Glass-KaastraS, GardhouseC, MarshallB, et al.Canadian consumer food safety practices and knowledge: Foodbook Study. J Food Protect, 2017; 80:1711–1718.
70.
NegeroJ, YohannesM, WoldemichaelK, TegegneD. Seroprevalence and potential risk factors of T. gondii infection in pregnant women attending antenatal care at Bonga Hospital, Southwestern Ethiopia. Int J Infect Dis, 2017; 57:44–49.
71.
NissapatornV, LeeCK, ChoSM, RohelaM, et al.Toxoplasmosis in HIV/AIDS patients in Malaysia. Southeast Asian J Trop Med Public Health, 2003; 34Suppl 2:80–85.
72.
PappasG, RoussosN, FalagasME. Toxoplasmosis snapshots: Global status of Toxoplasma gondii seroprevalence and implications for pregnancy and congenital toxoplasmosis. Int J Parasitol, 2009; 39:1385–1394.
73.
RoghmannMC, FaulknerCT, LefkowitzA, PattonS, et al.Decreased seroprevalence for Toxoplasma gondii in Seventh Day Adventists in Maryland. Am J Trop Med Hygiene, 1999; 60:790–792.
74.
RostamiA, SeyyedtabaeiSJ, AghamolaieS, BehniafarH, et al.Seroprevalence and risk factors associated with Toxoplasma gondii infection among rural commuities in Northern Iran Rev Inst Med Trop São Paulo. 2016; 58:70.
75.
SaidB, HalsbyKD, O'ConnorCM, FrancisJ, et al.Risk factors for acute toxoplasmosis in England and Wales. Epidemiol Infect, 2017; 145:23–29.
76.
Sang-EunL, HongSH, JeongYI, LeeJH, et al.Cross-sectional analysis of the seropositivity and risk factors of Toxoplasma gondii infection among veterinarians, in relation to their public professional activities. Vet Parasitol, 2014; 203:29–34.
77.
SharbatkhoriM, Dadi MoghaddamY, PaghehAS, MohammadiR, et al.Seroprevalence of Toxoplasma gondii infections in pregnant women in Gorgan City, Golestan Province, northern Iran-2012. Iran J Parasitol, 2014; 9:181–187.
78.
SharifM, DaryaniA, BarzegarG, NasrolaheiM. A seroepidemiological survey for toxoplasmosis among schoolchildren of Sari, Northern Iran. Trop Biomed, 2010; 27:220–225.
79.
SilvaMG, CamaraJT, VinaudMC, CastroAM. Epidemiological factors associated with seropositivity for toxoplasmosis in pregnant women from Gurupi, State of Tocantins, Brazil. Rev Soc Bras Med Trop, 2014; 47:469–475.
80.
TegeneD, AbdurahamanM, MosissaT, YohannesM. Anti-Toxoplasma antibodies prevalence and associated risk factors among HIV patients. Asian Pac J Trop Med, 2016; 9:460–464.
81.
TeweldemedhinM, GebremichaelA, GeberkirstosG, HadushH, et al.Seroprevalence and risk factors of Toxoplasma gondii among pregnant women in Adwa district, northern Ethiopia [Article]. BMC Infect Dis, 2019; 19:327.
82.
TianAL, GuYL, ZhouN, CongW, et al.Seroprevalence of Toxoplasma gondii infection in arthritis patients in eastern China. Infect Dis Poverty, 2017a; 6:153.
83.
TianAL, LiGX, ElsheikhaHM, GardnerDS, et al.Seroepidemiology of Toxoplasma gondii infection in patients with liver disease in eastern China. Epidemiol Infect, 2017b; 145:2296–2302.
84.
VergnesJ-N, Marchal-SixouC, NabetC, MaretD. Ethics in systematic reviews. BMC Med Ethics, 2010; 36:771–774.
85.
VittinghoffE, GliddenDV, ShiboskiSC, McCullochCE. Regression Methods in Biostatistics Linear, Logistic, Survival, and Repeated Measures Models. New York: Springer, 2005.
86.
WalleF, KebedeN, TsegayeA, KassaT. Seroprevalence and risk factors for toxoplasmosis in HIV infected and non-infected individuals in Bahir Dar, Northwest Ethiopia. Parasit Vectors, 2013; 6:15.
87.
WamEC, SamaLF, AliIM, EbileWA, et al.Seroprevalence of Toxoplasma gondii IgG and IgM antibodies and associated risk factors in women of child-bearing age in Njinikom, NW Cameroon. BMC Res Notes, 2016; 9:406.
88.
WangZ-D, LiuH-H, MaZ-X, MaH-Y, et al.Toxoplasma gondii infection in immunocompromised patients: A systematic review and meta-analysis. Front Microbiol, 2017; 8:389.
89.
WellsGA, SheaB, O'ConnellD, PetersonJ, et al.(2019). The Newcastle-Ottawa Scale ( NOS) for assessing the quality of nonrandomised studies in meta-analyses. Available at http://www.ohri.ca/programs/clinical_epidemiology/oxford.asp (accessed March17, 2020).
90.
YangN, WangD, XingM, LiC, et al.Seroepidemiology and risk factors of Toxoplasma gondii infection among the newly enrolled undergraduates and postgraduate students in China. Front Microbiol, 2017; 8:2092.
91.
YohanesT, DebalkeS, ZemeneE. Latent Toxoplasma gondii infection and associated risk factors among HIV-infected individuals at Arba Minch Hospital, South Ethiopia. AIDS Res ment, 2014; 2014:652941.
92.
ZelekeAJ, MelsewYA. Seroprevalence of Toxoplasma gondii and associated risk factors among HIV-infected women within reproductive age group at Mizan Aman General Hospital, Southwest Ethiopia: A cross sectional study. BMC Res Notes, 2017; 10:70.
93.
ZemeneE, YewhalawD, AberaS, BelayT, et al.Seroprevalence of Toxoplasma gondii and associated risk factors among pregnant women in Jimma town, Southwestern Ethiopia. BMC Infect Dis, 2012; 12:337.
94.
ZhangXX, ZhaoQ, ShiCW, YangWT, et al.Seroprevalence and associated risk factors of Toxoplasma gondii infection in the Korean, Manchu, Mongol and Han ethnic groups in eastern and northeastern China. Epidemiol Infect, 2016; 144:2018–2024.
95.
ZhaoYJ, ZhaoYH, ZhangXY, SunXJ, et al.First report of Toxoplasma gondii infection in tuberculosis patients in China. Vector Borne Zoonotic Dis, 2017; 17:799–803.
Supplementary Material
Please find the following supplemental material available below.
For Open Access articles published under a Creative Commons License, all supplemental material carries the same license as the article it is associated with.
For non-Open Access articles published, all supplemental material carries a non-exclusive license, and permission requests for re-use of supplemental material or any part of supplemental material shall be sent directly to the copyright owner as specified in the copyright notice associated with the article.
