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. 2019 Sep 30;147(1):12–28. doi: 10.1017/S0031182019001318

A review of toxoplasmosis in humans and animals in Turkey

Z Kolören 1,2, J P Dubey 2,✉
PMCID: PMC10317629  PMID: 31554526

Abstract

Infections by the protozoan parasite Toxoplasma gondii are widely prevalent in humans and animals in Turkey but little is known of the burden of their clinical toxoplasmosis. Many early papers on toxoplasmosis in Turkey were published in Turkish and often not available widely. Here, we review prevalence, clinical spectrum, epidemiology and diagnosis of T. gondii in humans and animals in Turkey. This knowledge should be useful to biologists, public health workers, veterinarians and physicians. Although one-third of the human population in Turkey is seropositive, the rate of congenital toxoplasmosis is unknown and no information is available in children 12 years old or younger. One large outbreak of acute toxoplasmosis has been reported in 14–18-year old school children in Turkey. An alarming rate (36%) of T. gondii tissue cysts were reported in tissues of sheep and water buffalo meats destined for human consumption; these reports require verification. Genetically, T. gondii strains from domestic cats and wild birds in Turkey were generally classical type II and III, like those prevalent in Europe. A separate genotype, Type 1 Africa, was isolated from two congenitally infected children and a domestic cat in Turkey.

Key words: Animals, clinical, Toxoplasma gondii, toxoplasmosis, Turkey, zoonosis

Introductıon

Turkey is a geographically important link between Asia, Europe and Africa and is surrounded by seas (Fig. 1). It has a population of nearly 83 million. Much of the literature on toxoplasmosis in Turkey is in Turkish. Here, we review the available literature on Toxoplasma gondii infection in humans and animals in Turkey.

Fig. 1.

Fig. 1.

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Map of Turkey with seven regions and human population. Marmara region (M), Central Anatolia (CA), Aegean region (A), Mediterranean region (ME), Black Sea region (B), Eastern Anatolia (EA) and Southern anatolia (SA).

Methods for review

We consulted original manuscripts to minimize mistakes in translation. Detailed historical, serological, parasitological, clinical and genetic information on T. gondii infections in humans and other animals are summarized in tables throughout the review.

Most of the reports on toxoplasmosis relate to serological surveys with no uniformity with respect to tests used and cut-off values. In Table 1, information on serological assays used in Turkey is summarized and noted throughout the paper where applicable.

Table 1.

Details of serological tests used for the seropositivity of T. gondii in humans and animals in Turkey

Abbreviation of test Antigen Cut-off titer Manufacturer Tables referred
Sabin-–Feldman dye test (SFDT)
1. SFDT Live tachyzoites ⩾1: 16 In-house 2, 5, 6, 10
2. SFDT ⩾1: 4 In-house 5, 7, 10
Immunofluorescence assay (IFA)
1. IFA Inactivated IgM ⩾ 1:16 Euroimmun GmbH 2
IgG ⩾ 1:64
2. IFA Inactivated IgG ⩾ 1:16 In-house 3, 4, 5
Indirect fluorescent antibody test (IFAT)
1. IFAT Inactivated IgM ⩾ 1:16 Euroimmun GmbH 2
2. IFAT IgG ⩾ 1:64 In-house 6
IgM ⩾ 1:16
3. IFAT IgG ⩾ 1:16 In-house 4, 5
Indirect haemagglutination assay (IHA) Soluble IgG ⩾ 1:80 Toxo-HAI Fumouze kit 2
IgM: NS
Latex agglutination test (LAT) Soluble NS Toxolatex Fumouze Diagnostics 6, 10
Chemiluminescence microparticle immunoassay (CMIA) p30 antigen IgG ⩾ 3 IU mL−1 ARCHITECT i1000 System, Abbott 3
IgM ⩾ 0.6 IU mL−1
Chemiluminescence immunoassay (CLIA)
1. CLIA Solid >1 IU mL−1 UniCel DxI 800, Beckman Coulter 3
>6 IU mL−1
2. CLIA Solid IgG ⩾ 8.8 IU mL−1 Cobas 6000, Roche Diagnostics 3
IgM ⩾ 1.0 IU mL−1
3. CLIA Solid IgG ⩾ 8.8 IU mL−1 LIAISON, DiaSorin S.p.A 3
IgM ⩾ 1.0 IU mL−1
4. CLIA Solid IgG ⩾ 3 IU mL−1 Cobas 6000, Roche Diagnostics 3
IgM ⩾ 0.49 IU mL−1
5. CLIA Solid NS Vitros Eciq ABD 3
Electrochemiluminescence method (ECLIA)
1. ECLIA Soluble IgG ⩾ 3.0 IU ml−1 Cobas e-170 analyser, Roche Diagnostics 2
IgM ⩾ 1.0 IU mL−1
2. ECLIA Soluble IgG ⩾ 3.0 IU ml−1 ECLIA-Roche, Elecsys 3
IgM ⩾ 1.0 IU mL−1
3. ECLIA Soluble IgG ⩾ 3.0 IU mL−1 Cobas e-601 analyser, Roche Diagnostics 3
IgM ⩾ 1.0 IU mL−1
Enzyme linked immunosorbent assay (ELISA)
1. ELISA Kit NS ⩾1,1 IU mL−1 Atlas Link Microwell 2
2. ELISA Kit Soluble IgG and IgM > 1 IU mL−1 IgG (Equipar) 2
VIDAS IgM indices >0.65 IU mL−1 IgM (Equipar) and (VIDAS TOXO IgM; Biomerieux)
3. ELISA Soluble whole tachyzoites NS In-house 2
4. IgG ELISA Whole tachyzoites NS Abbott Axsym System 2
5. ELISA Whole tachyzoites IgG ⩾ 10 IU mL−1 Meddens Diagnostica BV 2, 3
6. ELISA Soluble IgG > 8 IU mL−1 VIDAS, Biomerieux 2
IgM > 0.65 IU mL−1
7. Macro ELISA Inactivated IgG = 3 IU mL−1 Cobas E411, Roche Diagnostics 2
IgM = 1 IU mL−1 Abbott Architect system, Wiesbaden
8. Macro ELISA Inactivated IgG ⩾ 8 IU mL−1 Immulite® 2, 3
IgM ⩾ 1.1 IU mL−1 2000 XPi™ İmmunoassay System (Siemens)
9. ELISA NS IgG 3 IU mL−1 (Axsym, Abbott) 3
IgM 0.490 IU mL−1
10. MEIA Soluble ⩾3 IU mL−1 (Axsym Plus immünoanalizör) 3
11. Micro ELISA Soluble IgG > 20 IU mL−1 DYNEX technologies, inc. 3
12. ELISA NS IgG 3 IU mL−1 Cobas 4000 e411 (Roche) 3
IgM 0.6 IU mL−1
13. ELISA Inactivated IgG ⩾ 8 IU mL−1 Immulite® 3
IgM ⩾ 1.1 IU mL−1 2000 XPi™ İmmunoassay System Siemens Healthcare Diagnostics Inc.
14. Micro ELISA Soluble IgG > 3.0 IU mL−1 Cobas e-601 analyser, Roche Diagnostics 3
IgM < 1.0 IU mL−1
15. ELISA Soluble NS In house 3
16. ELISA Soluble whole tachyzoites NS Institut Pourquier 5
17. ELISA Sonicated tachyzoite NS In-house 9
Enzyme-Linked fluorescence assay (ELFA) Membrane and cytoplasmic Toxoplasma RH strain IgG ⩾ 8 IU mL−1 VIDAS TOXO IgG II (BioMerieux) 2, 3
IgM 0.65 IU mL−1
Enzyme immunoassay (EIA)
1. EIA NS >1.1 IU mL−1 Euroimmun Labordiagnostica 2
2. EIA Soluble IgG ⩾ 3 IU mL−1 Axsym, Abbott 3
IgM ⩾ 0.600 IU mL−1
3. EIA Soluble IgA = 10–40 AU mL−1 Differenta 3
Microimmunoflorescence (MIF) IgG kit Tachyzoites in the solid phase NS Euroimmun Labordiagnostica 2
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IgG ve IgM antibodies (Cobas Core, Roche), IgA antibodies (ETI-TOXOK-A reverse); IgG Avidity EIA Well-RADIM.

History

Although T. gondii was discovered in 1908, there was no information from Turkey until 1950 (Dubey, 2008). Professor Hayati Ekmen poineered research on toxoplasmosis in Turkey in 1970's. He first isolated viable T. gondii from a dog (Ekmen and Altıntaş, 1970) and from a child (Ekmen et al., 1974). The report on the baby was unfortunately published only as an abstract (Döşkaya et al., 2013). Toxoplasmosis was suspected in a child born to a mother from Ankara in 1972. The mother had been treated with anti-T. gondii therapy (sulfadiazine and pyrimethamine) during the last 2 months of pregnancy. Nothing was reported concerning the symptoms of toxoplasmosis in the newborn but the child must have had neurological signs because child's cerebrospinal fluid (CSF) was bioassayed in mice for the isolation of viable T. gondii. A virulent strain of T. gondii was recovered from the mice and designated the Ankara strain. This strain has been maintained since 1972 and used for molecular studies (Döşkaya et al., 2013).

Another noteworthy publication is an outbreak of acute toxoplasmosis in school children in Turkey (Doganci et al., 2006). In 2002, a boarding school in Izmir, Turkey, saw 171 (9.5%) of 1797 students, aged 14–18-year, develop mild flu-like illness. All students were examined physically, including ophthalmic testing. The symptoms were typical of acquired toxoplasmosis (cervical lymph adenopathy, fever, myalgia, headache and dizziness). Antibodies to T. gondii were found in all 171 students by means of several serological techniques; all were positive for IgM antibodies and 40 of 43 randomly selected students had low-avidity T. gondii antibodies. The IgM and low-avidity antibodies are indicative of recent infection. None of the students had ocular lesions. Epidemiological investigation revealed no common source. Near the dining hall, there was a sheltering place for large numbers of stray cats. However, the school authorities removed the cats before they could be tested for T. gondii. This outbreak provided reference sera for acute toxoplasmosis for other investigations (Liang et al., 2011).

Toxoplasmosis in humans

Toxoplasma gondii infections are prevalent worldwide but are mostly asymptomatic. However, T. gondii can cause severe illness in humans, particularly in congenitally infected children, and those with suppressed immunity, and even immunocompetent persons have died of toxoplasmosis (Robert-Gangneux and Dardè, 2012; Torgerson and Mastroiacovo, 2013; Peyron et al., 2016).

Serological prevalence in the general population

The seropositivity of T. gondii antibodies in the general population, including 15–40 years old women and those pregnant is summarized in Tables 2 and 3, respectively; seroprevalence varied between 18–100%.

Table 2.

Serological prevalence of T. gondii in the general human population of different regions in Turkey

Group/age Region/province No. tested Positive % Test Important findings/coinfections with other pathogens References
Hospital patients Aegean 50 26 (52) IHA IgG Ertuğ et al. (2000)
Izmir 28 (56) ELISA-IgG
28 (56) IFA-IgG
People in car accident Aegean 185 45 (24.32) ELISA1 IgG Yereli et al. (2006)
Izmir 6 (3.24) ELISA1 IgM
Manisa
Hospital patients Aegean 72 36 (50) IFA IgG Delibas et al. (2006)
Aydin ELISA2 IgG
Dustmen worker Eastern Anatolia 150 37 (24.6) SFDT1 Sweepers had higher prevalence, coinfection with listeriosis Çelik et al. (2008)
Malatya
Drivers Marmara 243 130 (53.5) EIA1 IgG, MIF IgG Kocazeybek et al. (2009)
Istanbul and its suburbs 2 (0.82) EIA1 IgM
130 (53.5) SFDT
Prisoners Central Anatolia 628 236 (37.58) IFA1-IgG Yaman et al. (2009)
Kayseri 11 (1.75) IFA1- IgG /IgM
Hospital patients Eastern Anatolia 4908 1522 (31.01) ELISA5 IgG IgG was found in 171 (31.09%) newborn whereas no positives for IgM Kuk and Ozden (2007)
Elazig 38 (0.77) ELISA5 IgM
Hospital patients Marmara 10295 2761 (26.8) ELFA IgG Alver et al. (2014)
Bursa 202 (1.9) ELFA IgM
Hospital patients Aegean 1887 452 (24) ECLIA1 IgG IgG was positive in 40 (18%) pregnant women whereas no positives for IgM Aşcı and Akgün (2015)
Afyonkarahisar 446 27 (1.4) ECLIA IgM
Hospital patients Aegean 2942 954 (32.4) Macro ELISA8-IgG Pektaş et al. (2015)
Izmır 3899 106 (2.7) Macro ELISA8-IgM
Hospital patients Black Sea 4048 863 (21.3) Macro ELISA7-IgG IgG was found in 18 (24.3%) of 74 newborn whereas no positives in 93 newborn for IgM Aydın Türkoğlu et al. (2018)
Bolu 13 605 162 (1.2) Macro ELISA7-IgM
Hospital patients Central Anatolia 7051 576 (29.53) ELISA6-IgG Maçin et al. (2018)
Konya 120 (2.44) ELISA6-IgM
Women from urban area Central 321 (44.9) ELISA IgG Risk assessment Nas et al. (2007)
Ankara 1732 (40.7)
Womena Marmara 96 33 (34.4) ELISA4-IgG Risk assessment Tansel et al. (2009)
Edirne
Womena Marmara 17 751 (24.61) EIA IgG TORCH pathogens Akyar (2011)
Istanbul, Bursa, Kocaeli (1.34) IgM
Mediterranean
Adana
Central
Kayseri
Womena Central Anatolia 1314 376 (28.6) ELISA-IgG Risk assessment Aral Akarsu et al. (2011)
Ankara 1 (0.07) ELISA-IgM
Womena Mediterranean 2986 (32.64) Macro ELISA7 Pekintürk et al. (2012)
Antalya 5013 (1.8) IgG
IgM
Womena Marmara 5073 1559 (30.7) ELFA IgG Alver et al. (2014)
Bursa
Womena Marmara 1101 (31) ELISA TORCH pathogens Numan et al. (2015)
İstanbul IgG
IgM
Students Aegean 171 171 (100) ELISA3 IgG/IgM Risk assessment Doganci et al. (2006)
Izmir
School students Marmara 388 61 (18) ELISA-IgG Risk assessment/cystic echinococcosis Tamer (2009)
Kocaeli ELISA-IgM
Students Central Anatolia 347 81(23.3) IFAT1 IgG Foreign student Çetinkaya et al. (2011)
Kayseri 6 (1.72) IFAT1 IgG /IgM
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15–50 year old.

Table 3.

Seroprevalence of T. gondii in pregnant women tested in hospital from different regions in Turkey

Region/province No. tested Test IgG (%) IgM (%) References
Central Anatolia/Ankara 37 ELISA5 35 (94.6) 2 (5.4) Tanyuksel et al. (2004)
Agean/Aydin 389 ELISA15 IFA2 (30.1) None Ertug et al. (2005)
Aegan/Izmir 52 EIA5 14 (26.9) 14 (26.9) Bahar et al. (2005)
Southeastern Anatolia/Şanliurfa 2586 CLIA1 1798 (69.5 ) 78 (3) Tekay and Özbek (2007)
Mediterranean/Hatay 1652 ELISA9 860 (52.1) 9 (0.54) Ocak et al. (2007)
Marmara/Kocaeli 1972 ELISA9 952 (48.3) 8 (0.4) Tamer et al. (2009)
Eastern Anatolia/Van 625 EIA4 225 (36) 2 (0.3) Efe et al. (2009)
Central Anatolia/Kayseri 2235 MEIA10 (33.42) (2.95) Inci et al. (2009)
Central Anatolia/Kayseri 1676 EIA4 IgG 568 (33.9) 46 (2.5) Kayman and Kayman (2010)
1813 EIA4 IgM
Marmara/Edirne 1646 ELISA9 426 (31.95) 13 (0.97) Varol et al. (2011)
Mediterranean/Antalya 7520 CLIA2 1262 (31) 22 (0.5) Çekin et al. (2011)
Aegean/Denizli 1102 Automated Vitros ECiQ system 408 (37) 15 (1.4) Karabulut et al. (2011)
Eastern/Malatya 312 ELISA 117 (37.5) 104 (33.3) Doğan et al. (2012)
Mediterranean/Hatay 3340 ELISA 1910 (57) 120 (3.6) Okyay et al. (2013)
Central/Ankara 30 863 CLIA3 ELISA 7869 (25.5) 83 (0.3) Şevki et al. (2013)
Aegean/Uşak 1465 Micro ELISA11 268 (18.3) 44 (3.0) Doğan Toklu (2013)
Marmara/Istanbul 1258 ELFA 291 (23.1) 5 (0.4) Karacan et al. (2014)
Marmara/Canakkale 196 ELISA (28.8) (2.7) Gencer et al. (2014)
Black Sea/Artvin 1133 CMIA 343 (30.3) 15 (1.3) İnci et al. (2014)
Central/Ankara 4758 ELFA 1278 (26.9) 8 (0.2) Mumcuoglu et al. (2014)
Black Sea/Tokat 3162 ELISA 1011 (32) 36 (1.1) Çeltek et al. (2014)
Mediterranean/Kahraman Maraş 4113 Micro ELISA IgG 84 (64.6) 12 (4.8) Bakacak et al. (2015)
7201 Micro ELISA IgM
Easten Anatolia/Van 457 ELISA12 IgG 172 (37.6) 99 (1.1) Parlak et al. (2015)
9156 ELISA12 IgM
Black Sea/Zonguldak 910 CLIA4 (43.9) (2.5) Aynioglu et al. (2015)
Black Sea/Amasya 1838 CLIA5 IgG 430 (23.39) 19 (1.02) Kılınç et al. (2015)
1852 CLIA5 IgM
Aegean/Afyonkarahisar 1091 EIA5 IgG 256 (23.4) 16 (1.5) Şimşek et al. (2016)
1020 EIA5 IgM
Black Sea/Ordu 1394 ECLIA2 IgG 385 (27.6) 22 (1.6) Çalgın et al. (2017)
1397 CMIA IgM
Aegean/Mugla 191 Automated analyser 36 (18.8) 7 (3.7) Kasap et al. (2017)
Aegean/Izmir 7513 CLIA3 IgG, IgM 2427 (32.3) 138 (1.9) Sirin et al. (2017)
Mediterranean/Hatay 11.564 ECLIA3 IgG, IgM (48.70) (3.9 ) Çetin and Çetin (2017)
CMIA IgG
Mediterranean/Isparta 1937 Macro8 ELISAIgG 344 (28.4) 34 (1.8) Akpınar et al. (2017)
1203 Macro8 ELISAIgM
Eastern Anatolia/Bingöl 10 178 ECLIA3 6155 (63) 196 (2) Nazik et al. (2017)
Mediterranean/Adana 11.313 ELISA13 5233 (46.3) 200 (1.8) Bozok (2017)
Marmara/Bursa 412a Micro ELISA14 125 (30.6) 27 (6.6) Dinçgez Çakmak et al. (2018)a
828a 157 (19.2) 35 (4.2)
Marmara/Adapazarı 1007 CMIA IgG 261 (25.9) No positivity Aydemir et al. (2018)
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Pregnancies with abortion (412), normal pregnancies (828).

Most of these serological studies were retrospective and based on convenience samples. There were no data on children less than 14 years of age. Notable among these surveys are reports that assayed more than 7,000 sera from different regions of Turkey. A study found T. gondii IgG antibodies in 28.8% and IgM antibodies in 1.9% of 10 295 patients from the Marmara region (Alver et al., 2014). Another study reported T. gondii IgG antibodies in 21.3% of 4,048 and IgM antibodies in 1.2% of 13 605 patients from Bolu province in the Black Sea region (Aydın Türkoğlu et al., 2018). From the Central region of Turkey, IgG antibodies were found in 29.5% and IgM antibodies in 2.4% of the 7051 hospital patients (Maçin et al., 2018). The prevalence of T. gondii antibodies in pregnant women varied a great deal (Table 3). In the largest sample of 30 863 women tested, IgG antibodies were detected in 25.5% and IgM antibodies were present in 0.3% (Çelen et al., 2013). Several authors emphasized the need to use multiple serological tests for diagnosis of acute infection and serological conversion during pregnancy (Tanyuksel et al., 2004; Bahar et al., 2005; Ertug et al., 2005; Doğan et al., 2012; Uysal et al., 2013; Karacan et al., 2014; Dinçgez et al., 2018).

Limited risk factor analysis data indicated that eating raw meat (Tekay and Özbek, 2007; Doğan Toklu, 2013; Gencer et al., 2014), contact with soil (Doğan Toklu, 2013; Gencer et al., 2014), and consumption of raw eggs (Gencer et al., 2014) were the main factors associated with seroprevalence. One study found seroprevalence of T. gondii IgG in 64.6% of 84 Syrian refugees (Bakacak et al., 2015).

Mother to foetus transmission of T. gondii and congenital toxoplasmosis

There are no firm data with respect to transmission of T. gondii during pregnancy. Toxoplasma gondii DNA was detected in amniotic fluid in one of 300 foetuses tested between 15th and 18th week of gestation (Gunel et al., 2012). Evidence of recently acquired infection (based on low-avidity antibodies) in one of 4651 women tested during the first trimester (Uysal et al., 2013). The intrauterine growth of the foetus was retarded with deficient amniotic fluid; there was no follow up. Chorioretinitis was diagnosed in one of the seven babies born to mothers that had IgM antibodies.

One study followed the outcomes of pregnancy in 13 women who had seroconverted to T. gondii infection during pregnancy; all were given anti-T. gondii therapy (Samanci et al.,1995). One of the childrens had classical symptoms of congenital toxoplasmosis: chorioretinitis, intracerebral calcification and hydrocephalus at birth. Thus, the authors estimated the risk of foetal infection at 7.1% (1 of 13), based only on symptoms; there was no confirmation of congenital toxoplasmosis.

Evidence was presented that spiramycin therapy during pregnancy can reduce congenital transmission of T. gondii (Avci et al., 2016). Of the 61 women who acquired T. gondii infection during pregnancy, 55 (90.2%) received spiramycin prophylaxis while six (6.6%) refused it. Obvious lesions of congenital toxoplasmosis were evident by ultrasonographic examination of foetuses of two mothers who refused spiramycin therapy. Both foetuses had intracranial calcification, enlarged ventricles and hepatomegaly. Pregnancy was terminated in foetuses from four of the six mothers who refused treatment; autopsy was not permitted. In summary, there are no estimates of the rate of congenital toxoplasmosis in Turkey.

There are only two proven cases of congenital toxoplasmosis, as documented by the isolation of viable T. gondii. The first report by Ekmen et al. (1974) was discussed earlier in the history section. The second case of congenital toxoplasmosis was a child who had bilateral chorioretinitis, hepato-splenomegaly and jaundice at birth and died 2 weeks later (Döşkaya et al., 2013). The CSF collected from the baby at postmortem was inoculated intraperitoneally into mice and viable tachyzoites were found in the peritoneal fluid. This highly mouse-virulent strain was designated Ege-1 strain. Retrospectively, T. gondii IgG and IgM antibodies were found in serum samples of the child and mother; low-IgG avidity in mother serum indicating recent infection. Additionally, T. gondii DNA was detected by the polymerase chain reaction (PCR) in CSF. There was no screening for T. gondii antibodies in mother before or during pregnancy.

Clinical toxoplasmosis in adults

Ocular disease is a common sequelae of toxoplasmosis but definitive diagnosis is difficult. There are several reports of ocular toxoplasmosis in Turkey (Ozcan, 1975; Küçükerdönmez et al., 2002; Atmaca et al., 2004; Tanyuksel et al., 2004; Tugal-Tutkun et al., 2005; Avkan Oguz et al., 2012; Celebi et al., 2015; Oray et al., 2015; Türkcü et al., 2017). However, most of these reports were based on lesions and the presence of T. gondii antibodies in the serum. One of the shortcomings of serological diagnosis is that chronically infected patients have low-antibody titers, not different than in the general population; a negative serological test, however, rules out ocular toxoplasmosis. Among the reports of ocular toxoplasmosis, two studies are discussed here. Atmaca et al. (2004) reported 189 cases of ocular toxoplasmosis from 1972 to 1999; 140 (74%) were considered congenital toxoplasmosis and 49 (26%) acquired toxoplasmosis. At the first examination, 65 active lesions were detected in 65 eyes. Lesions were seen in macula of 59%. Manifestations of congenital toxoplasmosis included were: strabismus in 15%, nystagmus in 9.2%, microphthalmia in 2.6%, optic nerve atrophy in 3.1% and lens opacities in 1%. The second study (Tugal-Tutkun et al., 2005) reported on 109 consecutive patients with active ocular disease in the Department of Ophthalmology, Istambul Faculty of Medicine in the last decade. The patients had IgG but no IgM antibodies to T. gondii. Retino-choroidal scars were present in 90 (83%) of 189 patients. Bilateral lesions, suggestive of congenital toxoplasmosis, were seen in 21 patients and active lesions were detected in 55 patients. All patients were treated with anti-T. gondii drugs with favourable prognosis.

Confirmatory tests, such as the detection of T. gondii antibodies in aqueous humour or T. gondii DNA, were not used in any reports on ocular toxoplasmosis.

Lymphadenitis, dermal rash, fever, headaches, myalgia, hepatitis and chorioretinitis are some of the common symptoms of acquired toxoplasmosis. A 46-year old woman who had a history of eating undercooked meat developed maculopapular rashes, hepatomegaly and elevated liver enzymes (Atilla et al., 2015). She had both IgG and IgM T. gondii antibodies, and T. gondii-like bodies were seen in histological sections of liver biopsy.

Reactivation of chronic T. gondii infection in patients with human immunodeficiency virus (HIV) has been reported worldwide, but rarely from Turkey. We are aware of only two reports of toxoplasmosis in HIV-infected patients in Turkey. Cerebral toxoplasmosis was diagnosed in a 29-year-old woman with HIV infection who had fever, vomiting, headache, weakness of the right side and seizure (Yapar et al., 2005). Cranial MRI revealed four mass lesions in the cerebellar cortex. The patient had T. gondii IgG antibodies but no IgM antibodies. She was treated with clindamycin and antiviral therapy. After 2 months, the neural lesions were resolved.

The second patient, a 37-year-old male, who had neurological signs, cranial MRI revealed multiple cerebral lesions and the diagnosis of toxoplasmosis was confirmed by brain biopsy (Midi et al., 2008). Despite antitoxoplasmosis, antiretroviral and antidopaminergic treatments, the patient died because of bacterial septicemia.

There is only limited information concerning toxoplasmosis in patients with other immunosuppressive disorders or transplant recipients. Possible toxoplasmosis was reported in five of 170 allogenic haematopoietic stem cell transplant patients, based on MRI, response to treatment with anti-T. gondii therapy and the PCR on CSF (Hakko et al., 2013). Two of these patients died of toxoplasmosis; postmortem was not performed.

Toxoplasmosis was detected in four of 40 liver transplants in a transplant service in Turkey (Caner et al., 2008). Both the donors and the recipients were seropositive to T. gondii. Toxoplasmosis was suspected when symptoms of fever, headaches and nausea were noted. Diagnosis was supported by positive DNA detection in blood of patients using PCR and anti-T. gondii therapy; all four patients recovered.

A rare case of spinal cord arachnoiditis was reported by Cosan et al. (2011). Toxoplasma gondii-like tachyzoites and bradyzoites were said to be detected but images are too low power to be convincing.

There are several reports of higher T. gondii serological prevalence in patients with schizophrenia (Cetinkaya et al., 2007; Tamer et al., 2008; Dogruman et al., 2009; Tanyüksel et al., 2010; Çelik et al., 2015; Cevizci et al., 2015; Karabulut et al., 2015; Yuksel et al. 2010) and patients with chronic renal failure (Yazar et al., 2003; Ocak et al., 2005), neoplastic disorders (Yazar et al., 2004), cirrhosis (Ustun et al., 2004; Atilla et al., 2015), chronic heart failure (Yazar et al., 2006), reactive arthritis (Sert et al., 2007), idiopathic Parkinson's disease (Celik et al., 2010), Alzheimer's disease (Kusbeci et al., 2011) and Multiple Sclerosis (Koskderelioglu et al., 2017); however, the sample size and appropriate controls were lacking for cause effect relationship.

Toxoplasmosis ın anımals

Companion animals

Cats

Cats are key in the epidemiology of T. gondii because they are the only hosts that can excrete environmentally resistant oocysts. Seroprevalence varied with age and life style of the cat (Table 4). Viable T. gondii was isolated from homogenates of hearts and brains in 20 of 100 cats by bioassay in mice (Can et al., 2014). Additionally, T. gondii DNA was detected in tissues of 12 additional cats. These 32 T. gondii strains were used for genotyping – (see molecular epidemiology and genotyping analysis section).

Table 4.

Serological prevalence of T. gondii at cats in different regions of Turkey

Category Region (place) No. tested Test Positive % Cut-off titer References
Stray Central 77 SFDT 16 (21) ⩾1:16 Ekmen (1970)
Ankara
Pets Central 65 SFDT 28 (43) ⩾1:16 Inci et al. (1996)
Ankara
Petsa Central 99 SFDT 40 (40.3) ⩾1:16 Taylan Özkan et al. (2008)
Ankara IFAT3 IgG 34 (34.3)
Strayb Central 72 SFDT 55 (76.4) ⩾1:16 Karatepe et al. (2008)
Nigde
Stray and petsc Izmir 1121 ELISA27 IgG 33.4–34.4 – Can et al. (2014)
IFA2 IgG 42–48 ⩾1:16
Indoord Eastern Anatolia 102 SFDT1 45 (44.1) ⩾1:16 Erkılıç et al. (2016)
Kars
Indoore Central Anatolia 102 SFDT1e 49 (48.03) ⩾1:16 Yasa Duru et al. (2017)
Kırıkkale
Ankara
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a

The seropositivity of T. gondii in cats older than 1 year (47.8%) was more about three times than cats less than a year old (13.6%). The seropositivity in indoor cats was 23.1% by IFAT and 30.8% by SFDT. The seropositivity in stray cats was 41.7% by IFAT and 52.8% by the SFDT. The presence of antibodies was significantly related to outdoor access.

b

Seropositivity in male cats (48.6%) was lower than in female cats (51.4%).

c

Tissues of 100 cats were used to isolate viable T. gondii (shown in the text).

d

No significant differences for the seropositivity between 20 (44.4%) of 45 males and 25 (43.9%) of 57 females.

e

Nested PCR was positive for four cats (8.2%). Foetal toxoplasmosis was diagnosed in one cat.

To our knowledge, there is only one report dealing with prevalence of T. gondii-like oocysts in cats from Turkey. Toxoplasma gondii-like oocysts measuring 9–14 µm in size were found in faeces of three of 36 (8.3%) cats from farms, however, results were not confirmed by bioassay or by PCR (Muz et al., 2013).

There are three reports of clinical toxoplasmosis in cats from Turkey. The first report concerns three cats (one, 8-month old male necropsied in 1988, one 3-month old female and one 6 month old female, both necropsied in 1984) (Haziroglu et al., 1988; Haziroglu, 1993). All three cats had disseminated toxoplasmosis and T. gondii was detected in multiple tissues of these cats histologically and by transmission electron microscopy.

Histologically confirmed disseminated toxoplasmosis was detected in a 2.5 year-old queen and her two kittens (Atmaca et al., 2013). The queen was hospitalized because of dystocia. Ultrasound examination revealed that three of five kittens had died in utero. After cesarean section, the queen and the two live kittens died. The queen had pneumonia and hepatitis. The presence of T. gondii was confirmed by both immunohistochemical examination and PCR testing in the kittens and the queen, thus, confirming transplacental toxoplasmosis.

Dermal toxoplasmosis was diagnosed in 2-year old female immunocompetent Angora cat (Kul et al., 2011). The cat had an antibody titer of 1:256 using the dye test and diagnosis was confirmed immunohistochemically and by PCR testing. The dermal lesions resolved after treatment with azithromycin.

Dogs

Serologic reports are summarized in Table 5. Viable T. gondii was isolated from lungs of a dog (Ekmen and Altıntaş, 1970) but details of the dog's condition are missing. Clinical toxoplasmosis was diagnosed postmortem in a dog owned by an American visitor to Turkey (Akcay et al., 1950); in retrospect it is not clear if the dog had toxoplasmosis or neosporosis (Dubey et al., 2017).

Table 5.

Serological prevalence of T. gondii in dogs from different regions of Turkey

Type of dog Region (place) No. tested Test Positive % Cut-off titer References
Healthy stray Central Anatolia 116 SFDT1 72 (62.0) 1:16 Aslantaş et al. (2005)
Ankara IFAT3
Stray and pets Marmara 116 SFDT1 81 (69.8%) ⩾1:16 Simşek et al. (2006)
Izmit (Kocaeli)
Stray Marmara 150 IFAT3 77 (51.3) 1:64 Öncel et al. (2007)
Istanbul
Stray Southern Anatolia 80 SFDT1 78 (97.5) ⩾1:16 Babür et al. (2007a)
Şanlıurfa
Stray Eastern Anatolia 69 SFDT2 40 (57.9) ⩾1:4 Babür et al. (2007b)
Van
Stray Central Anatolia 35 SFDT1 19 (54.3) ⩾1:16 Yıldız et al. (2009b)
Kırıkkale
Stray Central Anatolia 107 SFDT1 58 (54) ⩾1:16 Şahal et al. (2009)
Ankara
Stray Southeastern Anatolia 100 SFDT2 94 (94) ⩾1:4 Içen et al. (2010)
Diyarbakir
Stray Eastern Anatolia 72 SFDT1 70 (97%) ⩾1:16 Balkaya et al. (2010)
Erzurum
Pets and sheep dog Eastern Anatolia 179 SFDT1 172 (96.1) No data Gicik et al. (2010)
Kars
Military dogs Central Anatolia 140 SFDT1 81 (57.86) ⩾1:16 Kırbaş et al. (2011)
Nevsehir
Pets and stray Central Anatolia 120 SFDT1 115 (95.8) ⩾1:16 Altay et al. (2013)
Sivas
Shepherd dogs Mediterranean 46 ELISA16 IgG 27 (58.7) No data Muz et al. (2013)
Hatay
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Toxoplasmosis in livestock

Sheep and goats

Serological surveys indicate widespread exposure to T. gondii in sheep and goats in Turkey (Tables 6 and 7). Although toxoplasmosis is a major cause of abortion in sheep and goats worldwide (Dubey, 2010), there is little information from Turkey. Toxoplasma gondii-associated abortion cannot be diagnosed alone by serological testing of ewes; a negative serology rules out toxoplasmosis but positive result does not establish aetiology because seroprevalence is high in general population and antibodies can remain elevated in the next pregnancy (Dubey, 2010). To our knowledge, there is no confirmed report of T. gondii-associated abortion in sheep or goats from Turkey. Although T. gondii DNA was found in five of 20 sheep tissues (Ergin et al., 2009), there is no report of isolation of viable T. gondii from sheep and goats in Turkey.

Table 6.

Serological prevalence of T. gondii in sheep in different regions of Turkey

Region/province No. tested Test Positive % Antibody titer range References
Central Ankara 123 SFDT1 48 (29.1) 1:16 Ekmen (1967)
– 250 SFDT1 (38) 1:16–1:256 Weilland and Dalchow (1970)
Eastern Anatolia 295 IHA (27.7) 1:32–1:256 Dumanli et al. (1991)
Elaziğ
Central Ankara 1050 LAT (14.6) 1:64–1:154 Zeybek et al. (1995)
Mediterranean Adana 42a IHA (9.5) 1:64–1:154 Oz et al. (1995)
– 603 SFDT (31.1) 1:16–1:256 Altıntaş (1996)
Black Sea 62 SFDT (88.7) 1:16–1:256 Babür et al. (1997)
Samsun
Central Kayseri 154 SFDT (33.8) 1:16–1:256 Inci et al. (1999)
Eastern Anatolia 154b SFDT1b 72 (46.8) 1:16–1:1024 Aktas et al. (2000)
Elaziğ
Central Konya 1110c IFA2 (13.78) 1:64–1:2048 Sevinç et al. (2000)
Eastern Anatolia 103d SFDT1 53 (51.45) No data Aslantaș and Babür (2000)
Kars
Central Yozgat 152 SFDT1 (45.4) 1:16 Babür et al. (2001)
Aegean Afyon 172 SFDT (54.6) 1:16–1:256 Çicek et al. (2004)
Central Niğde 110 SFDT (50.9) 1:16–1:256 Karatepe et al. (2004)
Marmara 63 SFDT1 42 (66.66) 1:16–1:256 Oncel et al. (2005)
Yalova LATe 41 (65.08)
South-eastern Şanlıurfa 300f SFDT1 167 (55.66)f 1:16–1:1024 Sevgili et al. (2005)
Marmara 182g ELISA19 IgG 56 (31) – Oncel and Vural (2006)
Istanbul
Eastern Anatolia 460 ELISA (95.7) – Mor and Arslan (2007)
Kars
Aegean Afyonkarahisar 186 SFDT1 184 (98.92) 1:16–1:256 Çiçek et al. (2011)
Mediterranean Hatay 184 ELISA10 IgG 99 (53.8) – Muz et al. (2013)
South-eastern Anatolia 100h IFAT2 97 (97) 1:16–1:256 Leblebicier and Yıldız (2014)
Silopi
Differenti 610 Indirect ELISA21 IgG 122 (20.0) – Zhou et al. (2017)
Central Nevşehir 180j ELISA22 IgG 18 (10) – Özmutlu Çakmak and Karatepe (2017)
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a

25.5% seropositivity of 259 aborted sheep with titers of 1:64–1:256.

b

Pregnant 56, aborted 57 in the previous year, aborted 41 within the period of the study. Inactivating temperature for the ovine complement was 56 °C. Ovine sera should be heated to 60°C to inactivate complement (Dubey, 2010).

c

Healthy ewes 827, ewes aborted 283 (10.16%). No significant difference between the two groups for the presence of antibody titers.

d

5 of 10 aborted sheep were seropositive for T. gondii.

e

63 sheep older than one year of age were tested. SFDT was accepted as a reference test. The specificity and sensitivity of LAT were 61.90 and 78.57%, respectively. The correlation between two tests was 73.01%.

f

The seropositivity of 0–1 year old was 58.34% and >1 year age was 47.23%, respectively. The seropositivity of male (47.45%) and female (57.67%) and the seropositivity of Akkaraman breed (54.8%), Ivesi (55.71%) and Morkaraman (63.63%). No significant correlation between serum titers of age, sex and breed.

g

No dissimilarity between female (31.4%) and male ewes (30). The significant difference between 0.6–1 year age (12.5%) and >1 year age (41%),

h

Seropositivity of aborted 25 sheep was 96%. No significant difference between 2–4 year (96%) and 5–10 year (100%) sheep.

i

Karaman, Konya provinces from Central region and Zonguldak province from Black Sea. Identify specific antibodies to T. gondii (rTgSAG2-ELISA).

j

The seropositivity 1 to 2 years sheep (11.53%) and 5 to 7 years (8.51%). No statistically significant differences between the two age groups. Toxoplasma gondii antibodies were detected in 18 (11.1%) out of 162 ewes, while there was no seropositivity in the 18 rams tested.

Table 7.

Serological prevalence of T. gondii in goats from different regions of Turkey

Goat type Region/province No test Test Positive % Cut-off titer References
Mohair of Siirta South-eastern Anatolia (Siirt) 181 SFDT2 137 (75.7) ⩾1:4 Ataseven et al. (2006)
Norduz of Vana Eastern Anatolia (Van) 94 63 (67)b
Unspecified Eastern Anatolia Van 98 SFDT1 79 (80.61) 1:16 Karaca et al. (2007)
Saanen × Kilis Central Anatolia 74 SFDT1 60 (81. 1)c ⩾1:16 Ural et al. (2009)
Angora goats Ankara 63 52 (82. 53)c
Unspecified Mediterranean Hatay 184 ELISA20 IgG 66 (35.9) – Muz et al. (2013)
Unspecifiedd South-eastern Anatolia 105 SFDT1 100 (95.24) ⩾1:16 Beyhan et al. (2013)
Kilis
Unspecified Central Anatolia 249 Indirect ELISA21 IgG 32 (12.9) – Zhou et al. (2017)
Karaman and Konya provinces
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a

Mohair goats used for the production of mohair and blankets and Norduz are dairy breed.

b

42.85% seropositive at 1:16, 27.55% at 1:64, 7.17% at 1:256 and 3.06% at 1:1024.

c

38.33% seropositivity of 60 Saanen × Kilis goats at 1:16, 50% at 1:64, 6.67% at 1:256 and 5% at 1:1024. 36.5% seropositivity of 52 Angora goats at 1:16, 44.2% at 1:64, 11.53% at 1:256 and 7.7% at 1:1024.

d

100% of the Shami goats were seropositive with titers of 1:16 in 40 of 53, 12 at 1:64 and 1 at 1:256. 90.38% of Kilis goats were seropositive with titers of 1:16 in 36 of 52, 10 at 1:64 and 1 at 1:256.

Horses

Serologic data are summarized in Table 8. There is no report of clinical toxoplasmosis in horses.

Table 8.

Serological prevalence of T. gondii in horses in different regions of Turkey

Region/place No. tested Test Positive % Cut-off titer References
Central Anatolia 125 SFDT1 9 (7.2) ⩾1:16 Karatepe et al. (2010)
Niğde
East Anatolia 74 IHA 13.5 1:160 Göz et al. (2007)
Hakkari SFDT1 28.3 1:16
Central Ankara 100 SFDT1 28 ⩾1:16 Güçlü et al. (2007)
Central Ankara 168 SFDT1 62 (36.9) ⩾1:16 Gazyağci et al. (2011)
Mediterranean 616 Indirect ELISA21 IgG 285 (46.3) – Zhou et al. (2017)
Adana
Central Anatolia
Konya
Aegaen
Izmir
Marmara
Bursa and Istanbul
South-eastern Anatolia
Gaziantep
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Cattle

There is limited information concerning toxoplasmosis in cattle in Turkey (Table 9). Additionally, the dye test used in several surveys is nonspecific and gives erratic results with cattle sera (Dubey and Beattie, 1988). Finding of T. gondii DNA in five of 10 beef samples (Ergin et al., 2009) needs confirmation.

Table 9.

Serological prevalence of T. gondii in cattle in different regions of Turkey

Region (place) No. tested Test Positive % Cut-off titer References
East Anatolia 112 SFDT1 32 (22.3) ⩾1:16 Ekmen (1967)
Kars
Central Anatolia
Ankara
East Anatolia 115a SFDT1 57 (49.56) No data Aslantaș and Babür (2000)
Kars
Central Kirikkale 100 SFDT1 53 (53) ⩾1:16 Öcal et al. (2008)
East Anatolia 216 ELISA17 202 (93.5) – Akca and Mor (2010)
Kars
Kirikkale, Tokat, Izmir 557b SFDT1 138 (24.77) ⩾1:16 Yıldız et al. (2009a)
Adana 132 SFDT1 (56.06) ⩾1:16 Yağci et al. (2014)
Mediterranean Hatay 184 ELISA16 IgG 112 (60.9) – Muz et al. (2013)
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a

13 of 30 aborted cattle were seropositive for T. gondii.

b

Aborted 234, pregnant cows 323.

Pigs

Toxoplasma gondii infection is not a significant direct risk for human in Turkey because pork is not eaten in Turkey due to religious restrictions, 99.8% of population is muslim ((Library of Congress. Federal Research Division website: https://en.wikipedia.org/wiki/Islam_in_Turkey#cite_note-11 (accessed 29 August 2018)).

Various other animals

Serologic prevalence of T. gondii in miscellaneous animals is shown in Table 10. There is no confirmed report of clinical toxoplasmosis in animals, except in a zoo animal. Fatal toxoplasmosis was diagnosed in a captive kangaroo (Macropus sp.) from a zoo in Ankara (Kabak et al., 2011). Toxoplasma gondii DNA was demonstrated in the brain of a badger (Meles meles); indicating contamination of local waters by T. gondii (Karakavuk et al., 2018a).

Table 10.

Serological prevalence of T. gondii in miscellaneous animals in different regions of Turkey

Animal Region (place) No. tested Test Positive % Cut-off titer References
Goitered gazelles (Gazella subgutturosa) Southern Anatolia 82 SFDT1 23 (28.04) ⩾1:16 Gokcen et al. (2007)
Şanliurfa
Camels Central Anatolia 11 SFDT1 10 (90.9) ⩾1:16 Utuk et al. (2012)
Nevşehir
Layer hensa Central Anatolia 287 SFDT2 1(0.34) 1:16 Altinöz et al. (2007)
Konya
Domestic pigeon (105) Central Anatolia 105 SFDT1 1 (0.95) 1:16 Karatepe et al. (2011)
Wild pigeons (111) Niğde 111 1 (0.90)
Water buffaloes (Bubalus bubalis) Black Sea 131 SFDT1 115 (87.79) ⩾1:16 Beyhan et al. (2014)
Samsun
Central Anatolia
Afyon
Wild boars (Sus scrofa) Eastern Anatolia (Erzurum) 12 SFDT1 4 (33.3) 1:16 Balkaya et al. (2015)
Quails (Coturnix coturnix japonica) Central Anatolia 144 SFDT 0 No data Kılıç et al. (2017)
Niğde
Geese Eastern Anatolia 400 LAT 1 ( 0.25) No data Tasçi et al. (2018)
Kars
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a

The SFDT does not work with chicken sera (Dubey, 2010).

Meat as source of T. gondii infectıon

Humans acquire T. gondii infection postnatally by eating undercooked meat containing tissue cysts or ingesting food and water contaminated with oocysts (Dubey, 2010). There are reports of very high prevalence of T. gondii tissue cysts in sheep in Turkey destined for human consumption (Yildiz et al., 2014, 2015). In the first of these two reports, antibodies to T. gondii were found in 88 of 100 sheep; tissue cysts were detected in 46, in 36 by using the Percoll concentration technique in 5 g of ovine brain. Additionally, by using immunohistochemical staining with T. gondii antibodies, tissue cysts were found in 17% of tissue sections. However, the parasites assumed to be Toxoplasma depicted in Fig. 2 of their paper are not T. gondii and are most likely Sarcocystis spp. (J. P. Dubey, own opinion). Polyclonal T. gondii antibodies can cross react with Sarcocystis (Dubey, 2010). In the second report by these authors, tissue cysts were detected in 21.2% of 250 sheep meat samples by the Percoll method (Yildiz et al., 2015).

There is a similar report of high prevalence of T. gondii tissue cysts in buffalo meat imported from India into Turkey (Gencay et al., 2013). Tissue cysts were found in meat in three of 20 (15%) buffaloes tested by the Percoll method. The diagnosis was reported to be confirmed by PCR in both the buffalo and sheep-derived tissue cysts. However, the parasites assumed to be T. gondii depicted in Fig. 1 of their paper (Gencay et al., 2013) are most likely pollen grains and not T. gondii tissue cysts (J. P. Dubey, own opinion). Additionally, water buffaloes are considered resistant hosts of T. gondii, and T. gondii has not been isolated from buffalo meat in any country (Dubey, 2010).

These studies need confirmation because the density of T. gondii cysts in adult sheep is one tissue cyst in more than 100 g sheep tissue (Dubey, 2010). Reports of the presence of DNA in tissues of food animals are summarized in Table 11. However, detection of DNA does not relate to the presence of live organisms.

Table 11.

Detection of T. gondii from tissues of food animals in different regions of Turkey

Samples Regions (place) No. tested Test Positive % References
Slaughterhouse cattle Marmara 50a Nested PCR targeting B1 gene 5 (10) Ergin et al. (2009)
Slaughterhouse sheep İstanbul 20a 5 (25)
Imported meat samples Marmara 20 Nested PCR targeting B1 gene 3 (15) Gencay et al. (2013)
Istanbul
Shellfish mussels (M. galloprovincialis) Agean Izmir 53 EvaGreen® real time PCR and high resolution melting (HRM) 21 (39.6) Aksoy et al. (2014)
Brain and skeletal muscles from sheep Central Anatolia 100 Nested PCR targeting B1 gene 46 (46)b Yildiz et al. (2014)
Kirikkale
Boneless sheep meat Central Anatolia 250 Nested PCR for B1 gene 102 (40.8) Yildiz et al. (2015)
Kirikkale Ankara
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a

Toxoplasma gondii was found in 2% of 50 bovine brains, 6% of 50 bovine muscles, 4.17% of 120 ovine brains, 20% of 20 ovine muscles and 19% of 100 fermented sausage samples.

b

Tissue cysts were at 78.2% of 36 brain and at 69.5% of 32 of skeletal muscles (masseter, tongue, diaphragm, intercostal and leg).

Environmental contamination by T. gondii oocysts

Cats can excrete millions of T. gondii oocysts and oocysts that can survive harsh conditions in the environment (Dubey, 2010). Toxoplasma oocyst DNA has been detected in water samples from different regions in Turkey but not in drinking water (Table 12). Overall, sedimentation and filtration procedures are efficient in trapping T. gondii oocysts, water used for irrigation and farm animals may not be filtered.

Table 12.

Detection of Toxoplasma gondii from water samples in different region of Turkey

Samples Regions (place) No. tested Test Positive
%		 References
Water samples Sinop, 30 LAMP 30 (100) Koloren, 2013
Ordu n-PCR 13 (43.33)
Rize, Amasya,
Water samples Ordu 56 LAMP 20 (35.7) Koloren and Demirel 2013a
Conventional PCR 12 (21.42)
n-PCR 16 (28.57)
Water samples Amasya 120 n-PCR 48 (40) Koloren and Demirel 2013b
Water samples Giresun 76 LAMP 10 (13.2) Demirel et al., 2014
Conventional PCR
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Additionally, T. gondii oocysts can be concentrated by molluscs and fish. Toxoplasma gondii DNA was detected in 39.6% of edible shellfish (Mytilus galloprovincialis) in Izmir (Aksoy et al., 2014).

Molecular characterization

Although T. gondii infections are prevalent worldwide, there is a geographic distribution of T. gondii genetic types (Shwab et al., 2014). Except for minor variations, T. gondii strains are broadly divided into four types: I, II, III and atypical. In general, Type I stains are rare worldwide (Dubey, 2010). Type II and Type III strains are prevalent worldwide, except Brazil where they are rare. The T. gondii strains in Europe are similar to those in North America. An unusual strain, designated Africa 1 genotype, has been identified in humans from sub-Saharan Africa (Döşkaya et al., 2013), and more recently in Denmark (Jokelainen et al., 2018).

As stated in the Introduction section, Turkey is geographically unique, a bridge between Asia, Africa and Europe therefore, providing an avenue for cross mixing of T. gondii strains.

For genotyping of T. gondii, it is important to have good quality T. gondii DNA with minimal contamination of host tissue. For this, it is often necessary to extract DNA from viable strains. This has been achieved in three studies from Turkey. Döşkaya et al. (2013) found that both the T. gondii isolates obtained from CSF of diseased children were Africa 1 genotype. This Africa 1 genotype has been found in a cat but not yet identified in other hosts in Turkey. Of the 22 isolates of T. gondii genotyped from domestic cats in Turkey, 19 were classical Type II, two were Type III, and one was Africa 1 genotype (Can et al., 2014). Of the five viable isolates of T. gondii genotyped from wild birds in Turkey, four were Type II and one was Type III (Karakavuk et al., 2018b). Thus, the predominant distribution of genetic types of T. gondii in Turkey was like Europe.

Conclusıon

It is evident from this review that there are many gaps in our knowledge of toxoplasmosis in humans and animals, particular data on clinical infections are lacking. There is no centralized facility for advice and confirmation of diagnosis. Little is known about the rate of congenital toxoplasmosis, and follow up of subclinically infected children for clinical toxoplasmosis. No information is available concerning modes of transmission. Little information is available concerning the presence of viable T. gondii in edible meats, and T. gondii oocysts in the environment. Educational programs are needed to prevent T. gondii infection in humans and animals.

Acknowledgements

We thank Oliver Kwok, Meghan Sadler, Camila Cezar and Fernando Murata for their help with the paper.

Fınancıal support

We would like to thank The Scientific and Technological Research Council of Turkey (1059B191800417) for fellowship to Zeynep Kolören.

Conflıcts of ınterest

None.

Ethıcal standards

Not applicable.

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