Molecular prevalence of Toxoplasma gondii in sheep from Isfahan, Iran as detected in heart samples by loop-mediated isothermal amplification (LAMP)


Keywords:
Toxoplasma gondii sheep Loop-mediated isothermal amplification (LAMP) Iran
H. RAIESZADEH
V. NOAMAN
G. RAZMI
A. JAMSHIDI
Abstract
Toxoplasmosis is considered an important zoonosis that affects not only humans but also livestock worldwide. Small ruminants are important intermediate hosts of T. gondii. This study aimed to determine the molecular prevalence of T. gondii in the slaughtered sheep by loop-mediated isothermal amplification (LAMP) assay in Isfahan, Iran. A total of 250 sheep heart samples were collected from five different slaughterhouses in Isfahan, Iran, from October 2017 to May 2018. The LAMP assay was optimized targeting the sequence of 529 bp DNA fragments of T. gondii and detected T. gondii DNA in 96.4% (241/250) of samples. A significantly higher prevalence of T. gondii was recorded among female animals as compared to male animals (p ≤ 0.05). No statistically significant difference in T. gondii prevalence was noted between the seasons, type of animals, and age groups (p >0.05). To the best of our knowledge, the current study is the first to use the LAMP assay to determine the prevalence of T. gondii in sheep in Iran. The prevalence obtained in this study by the LAMP assay was higher than the prevalence reported by previous studies that used other methods. This study suggests that sheep meat may play a more prominent role as a source of infection of humans and the LAMP technique can be a recommended tool for accurate diagnosis of toxoplasmosis.
Article Details
  • Section
  • Research Articles
Downloads
Download data is not yet available.
References
Abdallah M-C, Kamel M, Karima B, Samir A, Djamel K, Rachid K, Khatima A-O (2019) Cross-Sectional Survey on Toxoplasma gondii Infection in Cattle, Sheep, and Goats in Algeria: Seroprevalence and Risk Factors. Vet Sci 6:63.
Abdoli A, Dalimi A, Soltanghoraee H, Ghaffarifar F (2016) Molecular detection of Toxoplasma gondii in house sparrow (Passer domesticus) by LAMP and PCR methods in Tehran, Iran. J Parasit Dis 40:1317-1321.
Alvarado-Esquivel C, Silva-Aguilar D, Villena I, Dubey JP (2013) Seroprevalence and correlates of Toxoplasma gondii infection in domestic sheep in Michoacán State, Mexico. Prev Vet Med 112:433-437.
Armand B, Solhjoo K, Shabani-Kordshooli M, Davami MH, Sadeghi M (2016) Toxoplasma infection in sheep from south of Iran monitored by serological and molecular methods; risk assessment to meat consumers. Veterinary world 9:850.
Asgari Q, Sarnevesht J, Kalantari M, Sadat SJA, Motazedian MH, Sarkari B (2011) Molecular survey of Toxoplasma infection in sheep and goat from Fars province, Southern Iran. Trop Anim Health Prod 43:389-392.
Burg JL, Grover CM, Pouletty P, Boothroyd J (1989) Direct and sensitive detection of a pathogenic protozoan, Toxoplasma gondii, by polymerase chain reaction. J Clin Microbiol 27:1787-1792.
Dard C, Fricker-Hidalgo H, Brenier-Pinchart M-P, Pelloux H (2016) Relevance of and new developments in serology for toxoplasmosis. Trends Parasitol 32:492-506.
Dubey J, Sundar N, Hill D, Velmurugan G, Bandini L, Kwok O, Majumdar D, Su C (2008) High prevalence and abundant atypical genotypes of Toxoplasma gondii isolated from lambs destined for human consumption in the USA. Int J Parasitol 38:999-1006.
Dubey J (2009) Toxoplasmosis in sheep—the last 20 years. Vet Parasitol 163:1-14.
Esteban-Redondo I, Maley S, Thomson K, Nicoll S, Wright S, Buxton D, Innes E (1999) Detection of T. gondii in tissues of sheep and cattle following oral infection. Vet Parasitol 86:155-171.
Fallahi S, Tabaei SJS, Pournia Y, Zebardast N, Kazemi B (2014) Comparison of loop-mediated isothermal amplification (LAMP) and nested-PCR assay targeting the RE and B1 gene for detection of Toxoplasma gondii in blood samples of children with leukaemia. Diagn Microbiol Infect Dis 79:347-354.
Foroutan M, Dalvand S, Daryani A, Ahmadpour E, Majidiani H, Khademvatan S, Abbasi E (2018) Rolling up the pieces of a puzzle: a systematic review and meta-analysis of the prevalence of toxoplasmosis in Iran. Alexandria J Med 54:189-196.
Gebremedhin EZ, Abdurahaman M, Hadush T, Tessema TS (2014) Seroprevalence and risk factors of Toxoplasma gondii infection in sheep and goats slaughtered for human consumption in Central Ethiopia. BMC Res Notes 7:696.
Guo M, Dubey JP, Hill D, Buchanan RL, Gamble HR, Jones JL, Pradhan AK (2015) Prevalence and risk factors for Toxoplasma gondii infection in meat animals and meat products destined for human consumption. J Food Prot 78:457-476.
Habibi G, Imani A, Gholami M, Hablolvarid M, Behroozikhah A, Lotfi M, Kamalzade M, Najjar E, Esmaeil-Nia K, Bozorgi S (2012) Detection and identification of Toxoplasma gondii type one infection in sheep aborted fetuses in Qazvin Province of Iran. Iran J Parasitol 7:64-72.
Hassanain MA, El-Fadaly HA, Hassanain NA, Shaapan RM, Barakat AM, Abd El-Razik K (2013) Serological and molecular diagnosis of toxoplasmosis in human and animals. World J Med Sci 9:243-247.
Homan W, Vercammen M, De Braekeleer J, Verschueren H (2000) Identification of a 200-to 300-fold repetitive 529 bp DNA fragment in Toxoplasma gondii, and its use for diagnostic and quantitative PCR. Int J Parasitol 30:69-75.
Kamani J, Mani AU, Egwu GO (2010) Seroprevalence of Toxoplasma gondii infection in domestic sheep and goats in Borno state, Nigeria. Trop Anim Health Prod 42:793-797.
Khan AH, Noordin R (2019) Serological and molecular rapid diagnostic tests for Toxoplasma infection in humans and animals. Eur J Clin Microbiol Infect Dis:1-12.
Khezri M, Mohammadian B, Esmailnia K, Khezri O (2012) Toxoplasmosis in sheep from Kurdistan province, Iran. Afr J Microbiol Res 6:3989-3992.
Kong Q-M, Lu S-H, Tong Q-B, Lou D, Chen R, Zheng B, Kumagai T, Wen L-Y, Ohta N, Zhou X-N (2012) Loop-mediated isothermal amplification (LAMP): early detection of Toxoplasma gondii infection in mice. Parasit Vectors 5:2.
Lin Z, Zhang Y, Zhang H, Zhou Y, Cao J, Zhou J (2012) Comparison of loop-mediated isothermal amplification (LAMP) and real-time PCR method targeting a 529-bp repeat element for diagnosis of toxoplasmosis. Parasitol 185:296-300.
Lopes WDZ, dos Santos TR, da Silva RdS, Rossanese WM, de Souza FA, de Faria Rodrigues JDA, de Mendonça RP, Soares VE, da Costa AJ (2010) Seroprevalence of and risk factors for Toxoplasma gondii in sheep raised in the Jaboticabal microregion, São Paulo State, Brazil. Res Vet Sci 88:104-106.
Nematollahi A, allah Jafari R, Shahbazi P, Khoshkerdar M, Zaboli N, Nouruzi M (2014) Survey on ovine toxoplasmosis by IFAT and double-tube nested-PCR in Tabriz, Iran. Comparative Clinical Pathology 23:1583-1586.
Olsen A, Berg R, Tagel M, Must K, Deksne G, Enemark HL, Alban L, Johansen MV, Nielsen HV, Sandberg M, Lundén A, Stensvold CR, Pires
SM, Jokelainen P (2019) Seroprevalence of Toxoplasma gondii in domestic pigs, sheep, cattle, wild boars, and moose in the Nordic-Baltic region: A systematic review and meta-analysis. Parasite Epidemiol Control 5:e00100.
Pan M, Lyu C, Zhao J, Shen B (2017) Sixty years (1957–2017) of research on toxoplasmosis in China—An overview. Front Microbiol 8:1825.
Razmi GR, Ghezi K, Mahooti A, Naseri Z (2010) A serological study and subsequent isolation of Toxoplasma gondii from aborted ovine fetuses in Mashhad area, Iran. J Parasitol 96:812-815.
Rostami A, Karanis P, Fallahi S (2018) Advances in serological, imaging techniques and molecular diagnosis of Toxoplasma gondii infection. Infect 46:303-315.
Sharif M, Sarvi S, Shokri A, Teshnizi SH, Rahimi M, Mizani A, Ahmadpour E, Daryani A (2015) Toxoplasma gondii infection among sheep and goats in Iran: a systematic review and meta-analysis. Parasitol Res 114:1-16.
Stelzer S, Basso W, Silván JB, Ortega-Mora L, Maksimov P, Gethmann J, Conraths F, Schares G (2019) Toxoplasma gondii infection and toxoplasmosis in farm animals: risk factors and economic impact. Food and Waterborne Parasitol 15:e00037.
Sun X-m, Ji Y-s, Liu X-y, Xiang M, He G, Xie L, Suo J-x, Suo X (2017) Improvement and evaluation of loop-mediated isothermal amplification for rapid detection of Toxoplasma gondii infection in human blood samples. PLoS One 12:1-11.
Tavakoli-Kareshk A, Mahmoudvand H, Keyhani A, Oliaee TR, Mohammadi M, Babaei Z, Hajhosseini M, Zia-Ali N (2017) Molecular detection and genetic diversity of Toxoplasma gondii in different tissues of sheep and goat in Eastern Iran. Trop Biomed 34:681-690.
Tavassoli M, Esmaeilnejad B, Malekifard F, Soleimanzadeh A, Dilmaghani M (2013) Detection of Toxoplasma gondii DNA in Sheep and Goat Milk in Northwest of Iran by PCR-RFLP. Jundishapur J Microbiol 6:8201.
Tavassoli M, Ghorbanzadehghan M, Esmaeilnejad B (2013) Detection of Toxoplasma gondii in sheep and goats blood samples by PCR-RFLP in Urmia. Vet Res Forum 4:43-47.
Yin M-Y, Wang J-L, Huang S-Y, Qin S-Y, Zhou D-H, Liu G-X, Tan Q-D, Zhu X-Q (2015) Seroprevalence and risk factors of Toxoplasma gondii in Tibetan Sheep in Gansu province, Northwestern China. BMC Vet Res 11:41.
Zhang H, Thekisoe OM, Aboge GO, Kyan H, Yamagishi J, Inoue N, Nishikawa Y, Zakimi S, Xuan X (2009) Toxoplasma gondii: sensitive and rapid detection of infection by loop-mediated isothermal amplification (LAMP) method. Exp Parasitol 122:47-50.