Analyze Diet
Frontiers in veterinary science2023; 9; 1080139; doi: 10.3389/fvets.2022.1080139

A review of foodborne Toxoplasma gondii with a special focus on its prevalence in Pakistan from 2000 to 2022.

Abstract: Third-world countries have a higher prevalence of food-related disorders than developed nations. Millions of people in underdeveloped countries are seriously at risk from the potential water supply contamination with protozoan diseases. is one of the important protozoans causing diseases in livestock and humans. Despite the standard tests for diagnosing this parasite and different treatment methods, the spread of these parasites is uncontrollable and rising every year due to other management disorders. In this review, we summarize etiopathogenesis and prevalence in Pakistan. We looked for papers reporting the seroprevalence of in people and animals between 2000 and 2022 in different databases: PubMed, Google Scholar, ScienceDirect, Scopus, and Web of Science. Data on the seroprevalence of i in Pakistan's domestic animals (sheep and goats, horses, donkeys, mules, cattle, and buffaloes), domestic pets (cats and dogs), poultry and rodents, and humans were gathered. According to the findings, sheep had an estimated pooled seroprevalence of that varied from 11.20 to 26.50 %, and goats from 24.50 to 38.40%. Whereas in buffalo the opposite trend was followed, and the prevalence was observed is 0% in 2022, in horses, donkeys, and mules, only one study was reported according to which a high prevalence was observed in mules (28.60%) followed by donkeys (23.50%) and horses (23.50%), in cats 38.5% prevalence was observed in a recent study and in dogs 28.43% observed, and in humans from 22 to 60%. Human beings are found to be the most affected species showing high prevalence among all. According to our findings, animals and pets not only serve as a reservoir for the parasite but also serve as a direct route for human infection with . The diagnostic techniques used in the observed studies were mostly serological testing whereas only a few studies have only been observed with molecular testing. To know the exact pattern of the disease for its control, the trend of molecular and advanced testing should be adopted as it is more reliable. Moreover, to decrease the transmission chances of to humans, it is crucial to manage infections in non-human species.
Publication Date: 2023-01-18 PubMed ID: 36744224PubMed Central: PMC9890071DOI: 10.3389/fvets.2022.1080139Google Scholar: Lookup
The Equine Research Bank provides access to a large database of publicly available scientific literature. Inclusion in the Research Bank does not imply endorsement of study methods or findings by Mad Barn.
  • Systematic Review

Summary

This research summary has been generated with artificial intelligence and may contain errors and omissions. Refer to the original study to confirm details provided. Submit correction.

This research examines the prevalence of the parasitic disease Toxoplasma gondii in various animals and humans in Pakistan from 2000 to 2022, finding high rates of infection and emphasizing the need for better testing and management to prevent transmission.

Objective and Methodology

  • The study’s primary goal was to investigate the seroprevalence of the parasite Toxoplasma gondii, which causes diseases in both livestock and humans, in Pakistan over a 22-year period.
  • To achieve this, the researchers collated data from several databases, including PubMed, Google Scholar, ScienceDirect, Scopus, and Web of Science, focusing mainly on papers that reported the seroprevalence of the parasite in people and animals from 2000 to 2022.

Findings and Analysis

  • In their findings, the researchers found that the prevalence of toxoplasmosis varied significantly among different species. For instance, sheep and goats showed seroprevalence rates of 11.20 to 26.50% and 24.50 to 38.40%, respectively.
  • On the other hand, buffalo showed a decreasing trend, with no incidence reported in 2022. In horses, donkeys, and mules, one study indicated a high prevalence, especially in mules (28.60%), followed by donkeys (23.50%) and horses (23.50%).
  • Domestic pets like cats and dogs also showed significant infection rates, with recent studies reporting 38.5% prevalence in cats and 28.43% in dogs respectively.
  • The most affected species were found to be humans, with prevalence ranging from 22 to 60%.

Implications and Recommendations

  • The results of the study demonstrate that animals and pets not only act as a reservoir for the parasite but can also directly transmit the infection to humans, thereby increasing the danger of the disease.
  • To provide more accurate information on the spread of the disease and enable better control, the study suggests the adoption of molecular and advanced testing, which is more dependable than the predominantly used serological testing.
  • Additionally, to reduce the chances of Toxoplasma gondii being transmitted to humans, the study deems it crucial to manage the infections in non-human species better. This can significantly mitigate the risk of the disease and ensure the health and safety of both humans and animals.

Cite This Article

APA
Qamar W, Alsayeqh AF. (2023). A review of foodborne Toxoplasma gondii with a special focus on its prevalence in Pakistan from 2000 to 2022. Front Vet Sci, 9, 1080139. https://doi.org/10.3389/fvets.2022.1080139

Publication

ISSN: 2297-1769
NlmUniqueID: 101666658
Country: Switzerland
Language: English
Volume: 9
Pages: 1080139
PII: 1080139

Researcher Affiliations

Qamar, Warda
  • Department of Parasitology, University of Agriculture, Faisalabad, Pakistan.
Alsayeqh, Abdullah F
  • Department of Veterinary Medicine, College of Agriculture and Veterinary Medicine, Qassim University, Buraidah, Saudi Arabia.

Conflict of Interest Statement

The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.

References

This article includes 126 references
  1. Javed A. Foodborne health issues and their relevance to Pakistani Society.. Am Acad Sci Res J Eng Technol Sci (2016) 26:235–51.
  2. World Health Organization. Multicriteria-based ranking for risk management of food-born parasites.. Microbiological Risk Assessment Series 23. Rome, Italy: FAO, World Health Organization; (2014).
  3. Strbac F, Bosco A, Amadesi A, Rinaldi L, Stojanović D, Simin N. Ovicidal potential of five different essential oils to control gastrointestinal nematodes of sheep.. Pak Vet J (2020) 41:353–8.
    doi: 10.29261/pakvetj/2021.026google scholar: lookup
  4. Alvi MA, Ohiolei JA, Saqib M, Li L, Tayyab MH, Alvi AA, Wu YT, Fu BQ, Yan HB, Jia WZ. Echinococcus granulosus (sensu stricto) (G1, G3) and E. ortleppi (G5) in Pakistan: phylogeny, genetic diversity and population structural analysis based on mitochondrial DNA.. Parasit Vectors 2020 Jul 13;13(1):347.
    doi: 10.1186/s13071-020-04199-8pmc: PMC7359271pubmed: 32660553google scholar: lookup
  5. Kandeel M, Akhtar T, Zaheer T, Ahmad S, Ashraf U, Omar M. Anti-parasitic applications of nanoparticles: a review.. Pak Vet J (2022) 42:2074–7764.
    doi: 10.29261/pakvetj/2022.040google scholar: lookup
  6. Mahmood Q, Younus M, Sadiq S, Iqbal S, Idrees A, Khan S. Prevalence and associated risk factors of cystic echinococcosis in food animals–a neglected and prevailing zoonosis.. Pak Vet J (2022) 42:59–64.
    doi: 10.29261/pakvetj/2022.008google scholar: lookup
  7. S Al-Malki E. Toxoplasmosis: stages of the protozoan life cycle and risk assessment in humans and animals for an enhanced awareness and an improved socio-economic status.. Saudi J Biol Sci 2021 Jan;28(1):962-969.
    doi: 10.1016/j.sjbs.2020.11.007pmc: PMC7783816pubmed: 33424388google scholar: lookup
  8. Thompson RC. Parasite zoonoses and wildlife: One Health, spillover and human activity.. Int J Parasitol 2013 Nov;43(12-13):1079-88.
  9. Torgerson PR, Devleesschauwer B, Praet N, Speybroeck N, Willingham AL, Kasuga F, Rokni MB, Zhou XN, Fèvre EM, Sripa B, Gargouri N, Fürst T, Budke CM, Carabin H, Kirk MD, Angulo FJ, Havelaar A, de Silva N. World Health Organization Estimates of the Global and Regional Disease Burden of 11 Foodborne Parasitic Diseases, 2010: A Data Synthesis.. PLoS Med 2015 Dec;12(12):e1001920.
  10. Trevisan C, Torgerson PR, Robertson LJ. Foodborne Parasites in Europe: Present Status and Future Trends.. Trends Parasitol 2019 Sep;35(9):695-703.
    doi: 10.1016/j.pt.2019.07.002pubmed: 31358427google scholar: lookup
  11. Leung AKC, Leung AAM, Wong AHC, Sergi CM, Kam JKM. Giardiasis: An Overview.. Recent Pat Inflamm Allergy Drug Discov 2019;13(2):134-143.
  12. Almeria S, Dubey JP. Foodborne transmission of Toxoplasma gondii infection in the last decade. An overview.. Res Vet Sci 2021 Mar;135:371-385.
    doi: 10.1016/j.rvsc.2020.10.019pubmed: 33148402google scholar: lookup
  13. Gorcea M, Neculicioiu V, Junie L. Cryptosporidium and Giardia–an overview.. Sci Parasitol (2020) 21:18–24.
  14. Siwila J, Mwaba F, Chidumayo N, Mubanga C. Food and waterborne protozoan parasites: The African perspective.. Food Waterborne Parasitol 2020 Sep;20:e00088.
  15. Robert-Gangneux F, Dardé ML. Epidemiology of and diagnostic strategies for toxoplasmosis.. Clin Microbiol Rev 2012 Apr;25(2):264-96.
    doi: 10.1128/CMR.05013-11pmc: PMC3346298pubmed: 22491772google scholar: lookup
  16. Pappas G, Roussos N, Falagas ME. Toxoplasmosis snapshots: global status of Toxoplasma gondii seroprevalence and implications for pregnancy and congenital toxoplasmosis.. Int J Parasitol 2009 Oct;39(12):1385-94.
    doi: 10.1016/j.ijpara.2009.04.003pubmed: 19433092google scholar: lookup
  17. Schlüter D, Däubener W, Schares G, Groß U, Pleyer U, Lüder C. Animals are key to human toxoplasmosis.. Int J Med Microbiol 2014 Oct;304(7):917-29.
    doi: 10.1016/j.ijmm.2014.09.002pubmed: 25240467google scholar: lookup
  18. Dubey JP, Murata FHA, Cerqueira-Cézar CK, Kwok OCH, Su C. Economic and public health importance of Toxoplasma gondii infections in sheep: 2009-2020.. Vet Parasitol 2020 Oct;286:109195.
    doi: 10.1016/j.vetpar.2020.109195pubmed: 32979682google scholar: lookup
  19. Howe DK, Sibley LD. Toxoplasma gondii comprises three clonal lineages: correlation of parasite genotype with human disease.. J Infect Dis 1995 Dec;172(6):1561-6.
    doi: 10.1093/infdis/172.6.1561pubmed: 7594717google scholar: lookup
  20. Lorenzi H, Khan A, Behnke MS, Namasivayam S, Swapna LS, Hadjithomas M, Karamycheva S, Pinney D, Brunk BP, Ajioka JW, Ajzenberg D, Boothroyd JC, Boyle JP, Dardé ML, Diaz-Miranda MA, Dubey JP, Fritz HM, Gennari SM, Gregory BD, Kim K, Saeij JP, Su C, White MW, Zhu XQ, Howe DK, Rosenthal BM, Grigg ME, Parkinson J, Liu L, Kissinger JC, Roos DS, Sibley LD. Local admixture of amplified and diversified secreted pathogenesis determinants shapes mosaic Toxoplasma gondii genomes.. Nat Commun 2016 Jan 7;7:10147.
    doi: 10.1038/ncomms10147pmc: PMC4729833pubmed: 26738725google scholar: lookup
  21. Khan A, Dubey JP, Su C, Ajioka JW, Rosenthal BM, Sibley LD. Genetic analyses of atypical Toxoplasma gondii strains reveal a fourth clonal lineage in North America.. Int J Parasitol 2011 May;41(6):645-55.
  22. Ajzenberg D, Yera H, Marty P, Paris L, Dalle F, Menotti J, Aubert D, Franck J, Bessières MH, Quinio D, Pelloux H, Delhaes L, Desbois N, Thulliez P, Robert-Gangneux F, Kauffmann-Lacroix C, Pujol S, Rabodonirina M, Bougnoux ME, Cuisenier B, Duhamel C, Duong TH, Filisetti D, Flori P, Gay-Andrieu F, Pratlong F, Nevez G, Totet A, Carme B, Bonnabau H, Dardé ML, Villena I. Genotype of 88 Toxoplasma gondii isolates associated with toxoplasmosis in immunocompromised patients and correlation with clinical findings.. J Infect Dis 2009 Apr 15;199(8):1155-67.
    doi: 10.1086/597477pubmed: 19265484google scholar: lookup
  23. Verma SK, Ajzenberg D, Rivera-Sanchez A, Su C, Dubey JP. Genetic characterization of Toxoplasma gondii isolates from Portugal, Austria and Israel reveals higher genetic variability within the type II lineage.. Parasitology 2015 Jun;142(7):948-57.
    doi: 10.1017/S0031182015000050pubmed: 25677825google scholar: lookup
  24. Jiang T, Shwab EK, Martin RM, Gerhold RW, Rosenthal BM, Dubey JP, Su C. A partition of Toxoplasma gondii genotypes across spatial gradients and among host species, and decreased parasite diversity towards areas of human settlement in North America.. Int J Parasitol 2018 Jul;48(8):611-619.
    doi: 10.1016/j.ijpara.2018.01.008pubmed: 29577892google scholar: lookup
  25. Khan A, Fux B, Su C, Dubey JP, Darde ML, Ajioka JW, Rosenthal BM, Sibley LD. Recent transcontinental sweep of Toxoplasma gondii driven by a single monomorphic chromosome.. Proc Natl Acad Sci U S A 2007 Sep 11;104(37):14872-7.
    doi: 10.1073/pnas.0702356104pmc: PMC1965483pubmed: 17804804google scholar: lookup
  26. Lehmann T, Marcet PL, Graham DH, Dahl ER, Dubey JP. Globalization and the population structure of Toxoplasma gondii.. Proc Natl Acad Sci U S A 2006 Jul 25;103(30):11423-8.
    doi: 10.1073/pnas.0601438103pmc: PMC1544101pubmed: 16849431google scholar: lookup
  27. Su C, Khan A, Zhou P, Majumdar D, Ajzenberg D, Dardé ML, Zhu XQ, Ajioka JW, Rosenthal BM, Dubey JP, Sibley LD. Globally diverse Toxoplasma gondii isolates comprise six major clades originating from a small number of distinct ancestral lineages.. Proc Natl Acad Sci U S A 2012 Apr 10;109(15):5844-9.
    doi: 10.1073/pnas.1203190109pmc: PMC3326454pubmed: 22431627google scholar: lookup
  28. Innes EA. Toxoplasmosis: comparative species susceptibility and host immune response.. Comp Immunol Microbiol Infect Dis 1997 Feb;20(2):131-8.
    doi: 10.1016/S0147-9571(96)00038-0pubmed: 9208198google scholar: lookup
  29. Mukhopadhyay D, Arranz-Solís D, Saeij JPJ. Influence of the Host and Parasite Strain on the Immune Response During Toxoplasma Infection.. Front Cell Infect Microbiol 2020;10:580425.
    doi: 10.3389/fcimb.2020.580425pmc: PMC7593385pubmed: 33178630google scholar: lookup
  30. Ihara F, Nishikawa Y. Toxoplasma gondii manipulates host cell signaling pathways via its secreted effector molecules.. Parasitol Int 2021 Aug;83:102368.
    doi: 10.1016/j.parint.2021.102368pubmed: 33905814google scholar: lookup
  31. Tomita T, Guevara RB, Shah LM, Afrifa AY, Weiss LM. Secreted Effectors Modulating Immune Responses to Toxoplasma gondii.. Life (Basel) 2021 Sep 20;11(9).
    doi: 10.3390/life11090988pmc: PMC8467511pubmed: 34575137google scholar: lookup
  32. Hakimi MA, Olias P, Sibley LD. Toxoplasma Effectors Targeting Host Signaling and Transcription.. Clin Microbiol Rev 2017 Jul;30(3):615-645.
    doi: 10.1128/CMR.00005-17pmc: PMC5475222pubmed: 28404792google scholar: lookup
  33. Calero-Bernal R, Gennari SM. Clinical Toxoplasmosis in Dogs and Cats: An Update.. Front Vet Sci 2019;6:54.
    doi: 10.3389/fvets.2019.00054pmc: PMC6399377pubmed: 30863754google scholar: lookup
  34. Speer CA, Dubey JP. Ultrastructural differentiation of Toxoplasma gondii schizonts (types B to E) and gamonts in the intestines of cats fed bradyzoites.. Int J Parasitol 2005 Feb;35(2):193-206.
    doi: 10.1016/j.ijpara.2004.11.005pubmed: 15710440google scholar: lookup
  35. Shapiro K, Bahia-Oliveira L, Dixon B, Dumètre A, de Wit LA, VanWormer E, Villena I. Environmental transmission of Toxoplasma gondii: Oocysts in water, soil and food.. Food Waterborne Parasitol 2019 Jun;15:e00049.
  36. Torrey EF, Yolken RH. Toxoplasma oocysts as a public health problem.. Trends Parasitol 2013 Aug;29(8):380-4.
    doi: 10.1016/j.pt.2013.06.001pubmed: 23849140google scholar: lookup
  37. Tilley M, Fichera ME, Jerome ME, Roos DS, White MW. Toxoplasma gondii sporozoites form a transient parasitophorous vacuole that is impermeable and contains only a subset of dense-granule proteins.. Infect Immun 1997 Nov;65(11):4598-605.
  38. Belluco S, Simonato G, Mancin M, Pietrobelli M, Ricci A. Toxoplasma gondii infection and food consumption: A systematic review and meta-analysis of case-controlled studies.. Crit Rev Food Sci Nutr 2018;58(18):3085-3096.
    doi: 10.1080/10408398.2017.1352563pubmed: 29020460google scholar: lookup
  39. Thebault A, Kooh P, Cadavez V, Gonzales-Barron U, Villena I. Risk factors for sporadic toxoplasmosis: a systematic review and meta-analysis.. Microb Risk Anal (2021) 17:100133.
  40. Borges M, Magalhães Silva T, Brito C, Teixeira N, Roberts CW. How does toxoplasmosis affect the maternal-foetal immune interface and pregnancy?. Parasite Immunol 2019 Mar;41(3):e12606.
    doi: 10.1111/pim.12606pubmed: 30471137google scholar: lookup
  41. Foroutan-Rad M, Majidiani H, Dalvand S, Daryani A, Kooti W, Saki J, Hedayati-Rad F, Ahmadpour E. Toxoplasmosis in Blood Donors: A Systematic Review and Meta-Analysis.. Transfus Med Rev 2016 Jul;30(3):116-22.
    doi: 10.1016/j.tmrv.2016.03.002pubmed: 27145927google scholar: lookup
  42. Dard C, Marty P, Brenier-Pinchart MP, Garnaud C, Fricker-Hidalgo H, Pelloux H, Pomares C. Management of toxoplasmosis in transplant recipients: an update.. Expert Rev Anti Infect Ther 2018 Jun;16(6):447-460.
    doi: 10.1080/14787210.2018.1483721pubmed: 29855213google scholar: lookup
  43. Montoya JG, Liesenfeld O. Toxoplasmosis.. Lancet 2004 Jun 12;363(9425):1965-76.
    doi: 10.1016/S0140-6736(04)16412-Xpubmed: 15194258google scholar: lookup
  44. Dunn D, Wallon M, Peyron F, Petersen E, Peckham C, Gilbert R. Mother-to-child transmission of toxoplasmosis: risk estimates for clinical counselling.. Lancet 1999 May 29;353(9167):1829-33.
    doi: 10.1016/S0140-6736(98)08220-8pubmed: 10359407google scholar: lookup
  45. McAuley JB. Congenital Toxoplasmosis.. J Pediatric Infect Dis Soc 2014 Sep;3 Suppl 1(Suppl 1):S30-5.
    doi: 10.1093/jpids/piu077pmc: PMC4164182pubmed: 25232475google scholar: lookup
  46. Wang ZD, Wang SC, Liu HH, Ma HY, Li ZY, Wei F, Zhu XQ, Liu Q. Prevalence and burden of Toxoplasma gondii infection in HIV-infected people: a systematic review and meta-analysis.. Lancet HIV 2017 Apr;4(4):e177-e188.
    doi: 10.1016/S2352-3018(17)30005-Xpubmed: 28159548google scholar: lookup
  47. Ali MI, Abd El Wahab WM, Hamdy DA, Hassan A. Toxoplasma gondii in cancer patients receiving chemotherapy: seroprevalence and interferon gamma level.. J Parasit Dis 2019 Sep;43(3):464-471.
    doi: 10.1007/s12639-019-01111-9pmc: PMC6667530pubmed: 31406412google scholar: lookup
  48. Blanchard N, Dunay IR, Schlüter D. Persistence of Toxoplasma gondii in the central nervous system: a fine-tuned balance between the parasite, the brain and the immune system.. Parasite Immunol 2015 Mar;37(3):150-8.
    doi: 10.1111/pim.12173pubmed: 25573476google scholar: lookup
  49. Tyebji S, Seizova S, Hannan AJ, Tonkin CJ. Toxoplasmosis: A pathway to neuropsychiatric disorders.. Neurosci Biobehav Rev 2019 Jan;96:72-92.
  50. Nogareda F, Le Strat Y, Villena I, De Valk H, Goulet V. Incidence and prevalence of Toxoplasma gondii infection in women in France, 1980-2020: model-based estimation.. Epidemiol Infect 2014 Aug;142(8):1661-70.
    doi: 10.1017/S0950268813002756pmc: PMC9151203pubmed: 24229712google scholar: lookup
  51. Khan F, Rooman M, Rehman H, Rab A, Khan A, Rehman A. Prevalence of Toxoplasma gondii antibodies among pregnant women in District Bannu, Khyber Pakhtunkhwa, Pakistan.. Int J Biosci (2018) 12:235−9.
    doi: 10.12692/ijb/12.5.233-237google scholar: lookup
  52. Ullah A, Bibi Y, Mohammad S, Ullah F, Fatima N, Shuaib SL. Prevalence of toxoplasmosis in pregnant women.. Pak J Med Health Sci (2022) 16:857–857.
    doi: 10.53350/pjmhs22166857google scholar: lookup
  53. Rehman F, Shah M, Ali A, Rapisarda AMC, Cianci A. Seroprevalence and risk factors of Toxoplasma gondii infection in women with recurrent fetal loss from the province of Khyber Pakhtunkhwa, Pakistan.. J Neonatal Perinatal Med 2021;14(1):115-121.
    doi: 10.3233/NPM-190323pubmed: 32925112google scholar: lookup
  54. Ali A, Omer T, Ullah A, Haleem A, Naseem M, Ullah M. Epidemiological survey of Toxoplasma gondii and associated risk factors in ruminant species of the Khyber Pakhtunkhwa Province of Pakistan.. J Parasitol Res (2021) 2021:1–8.
    doi: 10.1155/2021/6653239google scholar: lookup
  55. Kamal A, Din JU, Kamil A, Khan MT, Bibi H, Hussain A. Seroprevalence of Toxoplasma gondii in sheep and buffalo of District Charsadda, Khyber Pakhtunkhwa, Pakistan.. Int J Biosci (2019) 14:497–502.
    doi: 10.12692/ijb/14.3.482-487google scholar: lookup
  56. Zolfaghari Emameh R, Purmonen S, Sukura A, Parkkila S. Surveillance and diagnosis of zoonotic foodborne parasites.. Food Sci Nutr 2018 Jan;6(1):3-17.
    doi: 10.1002/fsn3.530pmc: PMC5778216pubmed: 29387356google scholar: lookup
  57. Todd ECD. Foodborne diseases: overview of biological hazards and foodborne diseases.. Encycl Food Saf (2014) 221:221–42.
  58. Dubey JP. Outbreaks of clinical toxoplasmosis in humans: five decades of personal experience, perspectives and lessons learned.. Parasit Vectors 2021 May 19;14(1):263.
    pmc: PMC8136135pubmed: 34011387doi: 10.1186/s13071-021-04769-4google scholar: lookup
  59. Shahzad A, Khan MS, Ashraf K, Avais M, Pervez K, Khan JA. Sero-epidemiological and haematological studies on toxoplasmosis in cats, dogs and their owners in Lahore, Pakistan.. J Protozool Res (2006) 16:60–73.
  60. Khan SN, Khan S, Ayaz S, Jan AH, Jehangir S, Attaullah S. Seroprevalance and risk factors of toxoplasmosis among pregnant women in District Kohat, Khyber Pakhtunkhwa, Pakistan.. World Appl Sci J (2011) 14:1032–6.
  61. Ahmad MS, Maqbool A, Mahmood-ul-Hassan M, Mushtaq-ul-Hassan M, Anjum AA. Prevalence of Toxoplasma gondii antibodies in human beings and commensal rodents trapped from Lahore, Pakistan.. J Anim Plant Sci (2012) 22:51–3.
  62. Tasawar Z, Aziz F, Lashari MH, Shafi S, Ahmad M, Lal V. Seroprevalence of Human toxoplasmosis in southern Punjab, Pakistan.. Pak J Life Soc Sci (2012) 10:48–52.
  63. Khan MZ, Rahman SU, Gul N, Khan AA. Toxoplasmosis; seroprevalence, comparative analysis of diagnostic techniques and identification of risk factors in humans in Malakand Agency, Khyber Pakhtunkhwa, Pakistan.. Int J Biosci (2014) 5:1–6.
    doi: 10.12692/ijb/5.4.1-6google scholar: lookup
  64. Nazir MM, Akhtar M, Maqbool A, Waheed A, Sajid MA, Ali MA, Oneeb M, Alam MA, Ahmad AN, Nazir N, Fatima S, Lindsay DS. Antibody Prevalence and Risk Factors for Toxoplasma gondii Infection in Women from Multan, Pakistan.. Zoonoses Public Health 2017 Nov;64(7):537-542.
    doi: 10.1111/zph.12336pubmed: 28067995google scholar: lookup
  65. Khan MT, Din JU, Ali S, Kamal A, Hussain A, Yar A. Seroprevalence of toxoplasma gondii infection in cows and goats of district Charsadda, Khyber Pakhtunkhwa, Pakistan.. Int J Fauna Biol Stud (2018) 5:18–22.
  66. HasnainJan MH, Faisal S, Abid Kamal MT, Khan KA, Muhammad W. Sero-epidemiology of human Toxoplasma gondii infection among male population in Charsadda, KPK, Pakistan (2018).. .
  67. Ahmad N, Khan IA, Iqbal Z, Naseem AA, Kayani AR, Afshan K. Seroepidemiology of toxoplasmosis in human population with reference to its zoonotic potential in sub-tropical areas of Pakistan.. Pak Vet J (2019) 39:2074–7764.
    doi: 10.29261/pakvetj/2019.017google scholar: lookup
  68. Ali S, Amjad Z, Khan TM, Maalik A, Iftikhar A, Khan I, Ahmed H. Occurrence of Toxoplasma gondii antibodies and associated risk factors in women in selected districts of Punjab province, Pakistan.. Parasitology 2020 Sep;147(10):1133-1139.
    doi: 10.1017/S0031182020000967pubmed: 32517832google scholar: lookup
  69. Ahmad S, Hanif W, Younas S. Toxoplasma gondii infection in sheep, goats and farmers from Bahawalpur (Pakistan).. Biologia (2020) 66:125–31.
  70. Ullah N, Nawaz D, Shah M, Rasool A, Akbar F, Israr M. Prevalence of Toxoplasma Gondii in Women Population in Swat, Pakistan.. Biomed J Sci Tech Res (2020) 30:23247–51.
  71. Abdul Hafeez M, Mehdi M, Aslam F, Ashraf K, Aleem MT, Khalid AR, Sattar A, Waheed SF, Alouffi A, Alharbi OO, Shabbir MAB, Chaudhry U, Almutairi MM. Molecular Characterization of Toxoplasma gondii in Cats and Its Zoonotic Potential for Public Health Significance.. Pathogens 2022 Apr 4;11(4).
    doi: 10.3390/pathogens11040437pmc: PMC9026455pubmed: 35456112google scholar: lookup
  72. Afshan K, Baseer S, Kiran S, Narjis G, Firasat S. Seroprevalence of Toxoplasma gondii in pregnant and non-pregnant women of Khyber Pakhtunkhwa, Pakistan.. (2022).
  73. Ahmad F, Maqbool A, Mahfooz A, Hayat S. Serological survey of Toxoplasma gondii in dogs and cats.. Pak Vet J (2001) 21:31–5.
    pubmed: 0
  74. Ahmad S, Tasawar Z. Seroprevalence of Toxoplasmosis in small ruminants from Cholistan desert and agricultural areas of Rahim Yar Khan and Rajan Pur (Punjab) Pakistan.. Pak J Zool (2016) 48.
  75. Nabi H, Rashid MI, Islam S, Bajwa AA, Gul R, Shehzad W, Akbar H, Ahmad N, Durrani AZ, Waqas M, Ashraf K. Prevalence of Toxoplasma gondii oocysts through Copro-PCR in cats at Pet Center (UVAS), Lahore, Pakistan.. J Pak Med Assoc 2018 Jan;68(1):115-118.
    pubmed: 29371731
  76. Majid A, Ahmad N, Haleem S, Akbar NU, Zareen S, Taib M, Khan S, Hussain R, Sohail. Detection of toxoplasmosis in pets and stray cats through molecular and serological techniques in Khyber Pakhtunkhwa, Pakistan.. BMC Vet Res 2021 Nov 19;17(1):357.
    doi: 10.1186/s12917-021-03064-9pmc: PMC8603471pubmed: 34798893google scholar: lookup
  77. Raza H, Tipu MY, Ahmad A, Umar T, Suleman M, Asfa sakhawat, Sara Attique, Ziaur Rehman. Screening of toxoplasmosis in cats through serology and PCR from selected districts of Khyber Pakhtunkhwa Pakistan.. Pure Appl Biol (2022) 12: 78–86.
  78. Jadoon A, Akhtar T, Maqbool A, Anjum AA, Ajmal A. Seroprevalence of Toxoplasma gondii in Canines.. J Anim Plant Sci (2009) 19:179–81.
  79. Ramzan M, Akhtar M, Muhammad F, Hussain I, Hiszczyńska-Sawicka E, Haq AU, Mahmood MS, Hafeez MA. Seroprevalence of Toxoplasma gondii in sheep and goats in Rahim Yar Khan (Punjab), Pakistan.. Trop Anim Health Prod 2009 Oct;41(7):1225-9.
    doi: 10.1007/s11250-009-9304-0pubmed: 19225903google scholar: lookup
  80. Shah M, Zahid M, Asmat P, Alam A, Sthanadar A. Seroprevalence of Toxoplasma gondii in goats and sheep of district Mardan, Pakistan.. Int J Biosci (2013) 7:90–7.
  81. Ahmad N, Iqbal Z, Mukhtar M, Mushtaq M, Khan KM, Qayyum M. Seroprevalence and associated risk factors of toxoplasmosis in sheep and goats in Pothwar region, Northern Punjab, Pakistan.. Pak J Zool (2015) 1:161–7.
  82. Ahmad S, Tasawar Z. Seroprevalence of Toxoplasma gondii in four ovine breeds of Cholistan desert of Pakistan.. Pak J Life Soc Sci (2015) 2:91–6.
  83. Ahmed H, Malik A, Arshad M, Mustafa I, Khan MR, Afzal MS, Ali S, Mobeen M, Simsek S. Seroprevalence and Spatial Distribution of Toxoplasmosis in Sheep and Goats in North-Eastern Region of Pakistan.. Korean J Parasitol 2016 Aug;54(4):439-46.
    doi: 10.3347/kjp.2016.54.4.439pmc: PMC5040087pubmed: 27658595google scholar: lookup
  84. Hanif M, Tasawar Z. Seroprevalence and risk factors associated with toxoplasmosis in sheep in Multan and Khanewal districts of Punjab (Pakistan).. J Anim Plant Sci (2016) 26:1620–7.
  85. Ullah MZ, Awais MM, Akhtar M, Anwar MI, Navid MT, Khan I, Razzaq A. Seroprevalence, associated risk factors and hematological impacts of toxoplasmosis in small ruminants of Multan, Punjab-Pakistan.. Trop Biomed 2018 Dec 1;35(4):1028-1040.
    pubmed: 33601850
  86. Khan FU, Hussain N. NH serological and molecular based diagnosis of toxoplasma gondii in galliformes by using ToxPK1 gene.. J Scient Res Med Biol Sci (2020) 1:116–22.
  87. Lashari MH, Farooq U, Mubeen S, Hassan W, Azhar MF, Shahida S. Seroprevalence of Toxoplasma gondii and associated hematological alterations in small ruminants of DG Khan district of Southern Punjab, Pakistan.. Arq Med Vet Zootec (2020) 72:1698–704.
    doi: 10.1590/1678-4162-11723google scholar: lookup
  88. Yousaf A, Soomro AG, Subhani A, Fazilani SA, Jan MN, Babar A. Detection of Toxoplasma Gondii Infection in Goats and Sheep using the Indirect Haemagglutination Test in Peshawar, Kyber Pakhtunkhwa-Pakistan.. J Vet Med Anim Sci (2021) 4:1087.
  89. Yousaf A, Tabbasum R, Awais T, Sakhawat A, Khan S, Bhutto AL. Prevalence of Toxoplasma Gondii in domestic breeds of goats in Faisalabad, Punjab.. Anim Vet Sci (2021) 9:145–8.
  90. Zafar MA, Shafique M, Zahoor MA, Saqalein M, Aslam B, Arshad MI. Evaluation of seroprevalence and associated risk factors of Toxoplasmosis in sheep and goats in District Jhang-Pakistan.. J Hell Vet Med Soc (2022) 73:3881–8.
    doi: 10.12681/jhvms.26205google scholar: lookup
  91. Saeed MS, Randhawa UA, Ahmad I, Ullah MI, Gul ST, Hassan MM. Seroprevalence and risk factors of toxoplasmosis in beetal goats in district Faisalabad and its association with reproductive problems.. Pak J Agric Sci (2021) 58:2067–80.
    doi: 10.21162/PAKJAS/21.1555google scholar: lookup
  92. Aziz MN, Iqbal RK, Irfan M, Parveen A, Asif M, Ozubek S, Aktas M, Said MB, Iqbal F. First report on molecular epidemiology, seasonality and phylogeny of Toxoplasma gondii infecting goats from Khanewal district in Punjab, Pakistan.. Acta Trop 2022 Apr;228:106304.
  93. Rafique A, Nasir S, Ashraf A, Nawaz Z, Zahid FM, Abbas A. Sero-surveillance and risk factors analysis of caprine toxoplasmosis in Faisalabad Punjab, Pakistan.. Pak Vet J (2022) 42:129–35.
  94. Ahmad N, Qayyum M. Seroprevalence and risk factors for toxoplasmosis in large ruminants in northern Punjab, Pakistan.. J Infect Dev Ctries 2014 Aug 13;8(8):1022-8.
    doi: 10.3855/jidc.4405pubmed: 25116669google scholar: lookup
  95. Taalay I, Iqbal RK, Asif M, Ahmad A, Amjad M, Anwar FN, Aktas M, Ben Said M, Iqbal F. Molecular survey of Toxoplasma gondii in cattle and buffaloes and phylogenetic position of Pakistani isolates based on ITS-1 gene.. Comp Immunol Microbiol Infect Dis 2022 May;84:101782.
    doi: 10.1016/j.cimid.2022.101782pubmed: 35259631google scholar: lookup
  96. Sarfraz-Ur-Rahman, Akbar H, Shabbir MZ, Ullah U, Rashid MI. Serological Investigation of Bovine Toxoplasmosis Using Commercial and Indigenous ELISA Kits While Validating Cattle Toxo IgG ELISA Kit.. Animals (Basel) 2022 Aug 14;12(16).
    doi: 10.3390/ani12162067pmc: PMC9405383pubmed: 36009657google scholar: lookup
  97. Awais MA, Ahmed A, Muhammad M, Muhammad A, Saleemi K, Ashraf K. Seroprevalence of Toxoplasma gondii in the Backyard chickens of the rural areas of Faisalabad Punjab Pakistan.. Int J Agric Biol (2014) 16.
  98. Naveed A, Ali S, Ahmed H, Simsek S, Rizwan M, Kaleem I, Gondal MA, Shabbir A, Pervaiz F, Khan MA, Nadeem MS, Afzaal MS, Umar S. Seroprevalence and Risk Factors of Toxoplasma gondii in Wild Birds of Punjab Province, Pakistan.. J Wildl Dis 2019 Jan;55(1):129-135.
    doi: 10.7589/2017-09-228pubmed: 29953314google scholar: lookup
  99. Khan MB, Khan S, Rafiq K, Khan SN, Attaullah S, Ali I. Molecular identification of Toxoplasma gondii in domesticated and broiler chickens (Gallus domesticus) that possibly augment the pool of human toxoplasmosis.. PLoS One 2020;15(4):e0232026.
  100. Tayyub M, Ali S, Javid A, Imran M. Molecular detection of Toxoplasma gondii and Neospora caninum in rock pigeons (Columba livia) in Punjab, Pakistan.. Parasitol Res 2022 May;121(5):1499-1505.
    doi: 10.1007/s00436-022-07494-8pubmed: 35320837google scholar: lookup
  101. Saqib M, Hussain MH, Sajid MS, Mansoor MK, Asi MN, Fadya AA, Zohaib A, Sial AU, Muhammad G, Ullah I. Sero-epidemiology of equine toxoplasmosis using a latex agglutination test in the three metropolises of Punjab, Pakistan.. Trop Biomed 2015 Jun;32(2):276-85.
    pubmed: 26691256
  102. Chaudhry UN, Ali AA, Ashraf S, Khan MT, Nadeem SM, Ashraf K. Seroprevalence of Toxoplasma gondii infection in camels (Camelus dromedarius) in and around Bahawalpur region of Pakistan.. J Inf Mol Biol (2014) 2:16–8.
  103. Lashari MH, Ghouri MT, Akhtar MS, Kamran Z, Chaudhari MS, Ayaz M. Hematological and biochemical alterations associated with toxoplasmosis in dromedaries (Camelus dromedarius) habitating in Cholistan desert of Bahawalpur, Punjab, Pakistan.. J Anim Plant Sci (2018) 28.
  104. Fatima T, Mehnaz S, Wang M, Yang J, Sajid MS, Shen B, Zhao J. Seroprevalence of Toxoplasma gondii in one-humped camels (Camelus dromedarius) of Thal and Cholistan deserts, Punjab, Pakistan.. Parasitol Res 2019 Jan;118(1):307-316.
    doi: 10.1007/s00436-018-6124-zpubmed: 30413878google scholar: lookup
  105. Shehzad A, Masud A, Fatima T, Khan FM, Rehman S, Effendi MH, Suwanti LT, Khan I, Tyasningsih W, Faisal S, Abadeen ZU, Bibi S. Seroprevalence of Toxoplasma gondii and associated alterations in hematology and serum biochemistry of one-humped camels (Camelus dromedarius) in Pakistan.. Vet World 2022 Jan;15(1):110-118.
  106. Jones JL, Dargelas V, Roberts J, Press C, Remington JS, Montoya JG. Risk factors for Toxoplasma gondii infection in the United States.. Clin Infect Dis 2009 Sep 15;49(6):878-84.
    doi: 10.1086/605433pubmed: 19663709google scholar: lookup
  107. Kaplan JE, Benson C, Holmes KK, Brooks JT, Pau A, Masur H. Guidelines for prevention and treatment of opportunistic infections in HIV-infected adults and adolescents: recommendations from CDC, the National Institutes of Health, and the HIV Medicine Association of the Infectious Diseases Society of America.. MMWR Recomm Rep 2009 Apr 10;58(RR-4):1-207; quiz CE1-4.
    doi: 10.1037/e537722009-001pubmed: 19357635google scholar: lookup
  108. Velusamy V, Arshak K, Korostynska O, Oliwa K, Adley C. An overview of foodborne pathogen detection: in the perspective of biosensors.. Biotechnol Adv 2010 Mar-Apr;28(2):232-54.
  109. Cerutti A, Blanchard N, Besteiro S. The Bradyzoite: A Key Developmental Stage for the Persistence and Pathogenesis of Toxoplasmosis.. Pathogens 2020 Mar 21;9(3).
    doi: 10.3390/pathogens9030234pmc: PMC7157559pubmed: 32245165google scholar: lookup
  110. Schares G, Koethe M, Bangoura B, Geuthner AC, Randau F, Ludewig M, Maksimov P, Sens M, Bärwald A, Conraths FJ, Villena I, Aubert D, Opsteegh M, Van der Giessen J. Toxoplasma gondii infections in chickens - performance of various antibody detection techniques in serum and meat juice relative to bioassay and DNA detection methods.. Int J Parasitol 2018 Aug;48(9-10):751-762.
    doi: 10.1016/j.ijpara.2018.03.007pubmed: 29782830google scholar: lookup
  111. Nyholt D. Novel insights into host-parasite interactions informed by the ≪in vitro≫ study of serum biomarkers: case of Chagas' disease and apolipoprotein AI.. (2008).
    pubmed: 0
  112. Aldebert D, Hypolite M, Cavailles P, Touquet B, Flori P, Loeuillet C, Cesbron-Delauw MF. Development of high-throughput methods to quantify cysts of Toxoplasma gondii.. Cytometry A 2011 Nov;79(11):952-8.
    doi: 10.1002/cyto.a.21138pubmed: 21905211google scholar: lookup
  113. Ismael SMM, Salem SA, Elshahidy MS. Isolation and molecular characterization of circulating foot and mouth disease virus in Egypt during 2018-2020.. Int J Vet Sci (2021) 10:162–71.
  114. Nasr EA, Fawzy RE, Marian GS, Abbas AM, Khalifa E. Using of gamma interferon γIFN and multiplex PCR (m-PCR) for detection of bovine tuberculosis in dairy herds in Egypt.. Int J Vet Sci (2021) 10:229–33.
  115. Osman SA, Tharwat M, Saeed EMA. An outbreak of epidemiological, clinical and treatment outcomes of ovine listeriosis in Qassim region, Saudi Arabia.. Int J Vet Sci (2021) 10:312–6.
  116. Ali S, Ijaz M, Ahmed A, Aziz MU, Naveed M, Javed MU. Prevalence and associated risk factors of bovine babesiosis in Lahore, Pakistan.. Agrobiol Records (2020) 2:17–23.
  117. Zaman MA, Mehreen U, Qamar W, Qamar MF, Kashif M, Shahid Z. Brief account of bovine theileriosis prevalence in some South Asian countries.. Agrobiol Records (2020) 2:38–48.
  118. Sharif M, Tunio SA, Bano S. Synergistic effects of Zinc oxide nanoparticles and conventional antibiotics against methicillin resistant Staphylococcus aureus.. Adv Life Sci (2021) 8:167–71.
  119. Reshetnikova TI, Zenkin AS, Krylova TG. Experimental use of the Triazavirin antiviral medication in conditions of group administration at the pig-breeding unit.. Adv Life Sci (2021) 8:381–6.
  120. Özcan U, Sezener MG, Sayilkan BU, Ergüden VE, Küllük E, Yaman SA. New aspect in neonatal calf diarrhea: presence of Escherichia coli CS31A at unexpected ratio.. Kafkas Univ Vet Fak Derg (2021) 27:133–4.
  121. Özdemir O, Ortatatli M, Terzi F, Hatipoglu FH, Çiftçi MK, Ateş MB. The usability of cytological and immunocytological methods for rapid diagnosis of encephalitic listeriosis in ruminants.. Kafkas Univ Vet Fak Derg (2021) 27:225–33.
  122. Aksel EG, Akçay A, Arslan K, Sohel MH, Güngör G, Akyüz B. The effects of MBL1 gene polymorphism on subclinical mastitis in Holstein cows.. Kafkas Univ Vet Fak Derg (2021) 27:389–95.
  123. Selim A, Abdelhady A, Alahadeb. Prevalence and molecular characterization of Ehrlichia canis in Egyptian DOGS.. Pak Vet J (2021) 41:117–21.
    doi: 10.29261/pakvetj/2020.061google scholar: lookup
  124. Jalil PJ, Shnawa BH, Hammad SM. Silver nanoparticles: green synthesis, characterization, blood compatibility and protoscolicidal efficacy against Echinococcus granulosus.. Pak Vet J (2021) 41:393–9.
    doi: 10.29261/pakvetj/2021.039google scholar: lookup
  125. Wajiha, Qureshi NA. In vitro anticoccidial, antioxidant activities and biochemical screening of methanolic and aqueous leaves extracts of selected plants.. Pak Vet J (2021) 41:57–63.
    doi: 10.29261/pakvetj/2020.071google scholar: lookup
  126. Ali KM, Hassan EA, Abuowarda MM, Mahmoud MA, Torad FA. Bilateral panophthalmia as a late sequel of leishmaniasis in dogs.. Pak Vet J (2021) 41:13–8.
    doi: 10.29261/pakvetj/2021.006google scholar: lookup

Citations

This article has been cited 1 times.
  1. Sousa DER, Wilson TM, Macêdo IL, Romano APM, Ramos DG, Passos PHO, Costa GRT, Fonseca VS, Mares-Guia MAMM, Giovanetti M, Alcantara LCJ, de Filippis AMB, Paludo GR, Melo CB, Castro MB. Case report: Urbanized non-human primates as sentinels for human zoonotic diseases: a case of acute fatal toxoplasmosis in a free-ranging marmoset in coinfection with yellow fever virus.. Front Public Health 2023;11:1236384.
    doi: 10.3389/fpubh.2023.1236384pubmed: 37670831google scholar: lookup