Risk of infection with arboviruses in a healthy population in Pakistan based on seroprevalence

Shengyao Chen; Muhammad Saqib; Hafiz Sajid Khan; Yuan Bai; Usman Ali Ashfaq; Muhammad Khalid Mansoor; Abulimti Moming; Jing Liu; Min Zhou; Saifullah Khan Niazi; Qiaoli Wu; Awais-Ur-Rahman Sial; Shuang Tang; Muhammad Hassan Sarfraz; Aneela Javed; Sumreen Hayat; Mohsin Khurshid; Iahtasham Khan; Muhammad Ammar Athar; Zeeshan Taj; Bo Zhang; Fei Deng; Ali Zohaib; Shu Shen

doi:10.1016/j.virs.2024.04.001

June 2024

Citation: Shengyao Chen, Muhammad Saqib, Hafiz Sajid Khan, Yuan Bai, Usman Ali Ashfaq, Muhammad Khalid Mansoor, Abulimti Moming, Jing Liu, Min Zhou, Saifullah Khan Niazi, Qiaoli Wu, Awais-Ur-Rahman Sial, Shuang Tang, Muhammad Hassan Sarfraz, Aneela Javed, Sumreen Hayat, Mohsin Khurshid, Iahtasham Khan, Muhammad Ammar Athar, Zeeshan Taj, Bo Zhang, Fei Deng, Ali Zohaib, Shu Shen. Risk of infection with arboviruses in a healthy population in Pakistan based on seroprevalence .VIROLOGICA SINICA, 2024, 39(3) : 369-377. http://dx.doi.org/10.1016/j.virs.2024.04.001

Risk of infection with arboviruses in a healthy population in Pakistan based on seroprevalence

a. Key Laboratory of Virology and National Virus Resource Center, Wuhan Institute of Virology, Chinese Academy of Sciences, Wuhan 430071, China;
b. University of Chinese Academy of Sciences, Beijing 100049, China;
c. Faculty of Veterinary Science, University of Agriculture Faisalabad, Faisalabad 38040, Pakistan;
d. The Children's Hospital Faisalabad, 38000, Pakistan;
e. Department of Bioinformatics and Biotechnology, Government College University Faisalabad, Faisalabad 38000, Pakistan;
f. Department of Microbiology, Faculty of Veterinary and Animal Sciences, The Islamia University of Bahawalpur, Bahawalpur 63100, Pakistan;
g. Hubei Jiangxia Laboratory, Wuhan 430200, China;
h. Key Laboratory of Special Pathogens and Biosafety, Wuhan Institute of Virology, Center for Biosafety Mega-Science, Chinese Academy of Sciences, Wuhan 430071, China;
i. Armed Forces Institute of Pathology (AFIP), Rawalpindi 46000, Pakistan;
j. Department of Clinical Studies, Faculty of Veterinary & Animal Sciences, Pir Mehr Ali Shah Arid Agriculture University, Rawalpindi 46300, Pakistan;
k. Institute of Microbiology, Government College University Faisalabad, Faisalabad 38000, Pakistan;
l. Atta-ur-Rahman School of Applied Biosciences, National University of Science and Technology, Islamabad 44000, Pakistan;
m. Department of Clinical Sciences, University of Veterinary and Animal Sciences, Lahore Sub-campus, Jhang 35200, Pakistan;
n. Department of Molecular Pathology, National Medical Center DHA Phase 1, Karachi 75500, Pakistan

Corresponding author: Fei Deng, df@wh.iov.cn
Ali Zohaib, ali.zohaib@iub.edu.pk
Shu Shen, shenshu@wh.iov.cn
Received Date: 19 November 2023
Accepted Date: 01 April 2024
Available online: 08 April 2024

Abstract

Infectious diseases caused by arboviruses are a public health concern in Pakistan. However, studies on data prevalence and threats posed by arboviruses are limited. This study investigated the seroprevalence of arboviruses in a healthy population in Pakistan, including severe fever with thrombocytopenia syndrome virus (SFTSV), Crimean-Congo hemorrhagic fever virus (CCHFV), Tamdy virus (TAMV), and Karshi virus (KSIV) based on a newly established luciferase immunoprecipitation system (LIPS) assays, and Zika virus (ZIKV) by enzyme-linked immunosorbent assays (ELISA). Neutralizing activities against these arboviruses were further examined from the antibody positive samples. The results showed that the seroprevalence of SFTSV, CCHFV, TAMV, KSIV, and ZIKV was 17.37%, 7.58%, 4.41%, 1.10%, and 6.48%, respectively, and neutralizing to SFTSV (1.79%), CCHFV (2.62%), and ZIKV (0.69%) were identified, as well as to the SFTSV-related Guertu virus (GTV, 0.83%). Risk factors associated with the incidence of exposure and levels of antibody response were analyzed. Moreover, co-exposure to different arboviruses was demonstrated, as thirty-seven individuals were having antibodies against multiple viruses and thirteen showed neutralizing activity. Males, individuals aged ≤40 years, and outdoor workers had a high risk of exposure to arboviruses. All these results reveal the substantial risks of infection with arboviruses in Pakistan, and indicate the threat from co-exposure to multiple arboviruses. The findings raise the need for further epidemiologic investigation in expanded regions and populations and the necessity to improve health surveillance in Pakistan.
- Arbovirus
- , Pakistan
- , Seroprevalence
- , Tick-borne virus
- , Mosquito-borne virus

Electronic Supplementary Material

10.1016j.virs.2024.04.001-ESM.docx
References
1. Atif, M., Saqib, A., Ikram, R., Sarwar, M.R.,Scahill, S., 2017. The reasons why Pakistan might be at high risk of Crimean Congo haemorrhagic fever epidemic; a scoping review of the literature. Virol J, 14, 63.
2. Awan, U.A., Zahoor, S., Ayub, A., Ahmed, H., Aftab, N.,Afzal, M.S., 2021. COVID-19 and arboviral diseases: Another challenge for Pakistan's dilapidated healthcare system. J Med Virol, 93, 4065-4067.
3. Badar, N., Salman, M., Ansari, J., Aamir, U., Alam, M.M., Arshad, Y., Mushtaq, N., Ikram, A.,Qazi, J., 2020. Emergence of Chikungunya Virus, Pakistan, 2016-2017. Emerg Infect Dis, 26, 307-310.
4. Bai, Y., Zhang, Y., Su, Z., Tang, S., Wang, J., Wu, Q., Yang, J., Moming, A., Zhang, Y., Bell-Sakyi, L., Sun, S., Shen, S.,Deng, F., 2022. Discovery of Tick-Borne Karshi Virus Implies Misinterpretation of the Tick-Borne Encephalitis Virus Seroprevalence in Northwest China. Frontiers in Microbiology, 13.
5. Begum, F., Wisseman Cl, J.,Casals, J., 1970a. Tick-borne viruses of West Pakistan. 3. Dera Ghazi Khan virus, a new agent isolated from Hyalomma dromedarii ticks in the D. G. Khan District of West Pakistan. Am J Epidemiol., 92(3), 195-196.
6. Begum, F., Wisseman Cl, J.,Traub, R., 1970b. Tick-borne viruses of West Pakistan. I. Isolation and general characteristics. Am J Epidemiol., 92(3), 180-191.
7. Burbelo, P.D., Chaturvedi, A., Notkins, A.L.,Gunti, S., 2019. Luciferase-Based Detection of Antibodies for the Diagnosis of HPV-Associated Head and Neck Squamous Cell Carcinoma. Diagnostics (Basel), 9.
8. Butt, A.M., Siddique, S., Gardner, L.M., Sarkar, S., Lancelot, R.,Qamar, R., 2016. Zika virus in Pakistan: the tip of the iceberg? The Lancet Global Health, 4, e913-e914.
9. Butt, M.H., Safdar, A., Amir, A., Zaman, M., Ahmad, A., Saleem, R.T., Misbah, S., Khan, Y.H.,Mallhi, T.H., 2021. Arboviral diseases and COVID-19 coincidence: Challenges for Pakistan's derelict healthcare system. J Med Virol, 93, 6465-6467.
10. Chen, S., Xu, M., Wu, X., Bai, Y., Shi, J., Zhou, M., Wu, Q., Tang, S., Deng, F., Qin, B.,Shen, S., 2022. A new luciferase immunoprecipitation system assay provided serological evidence for missed diagnosis of severe fever with thrombocytopenia syndrome. Virol Sin, 37, 107-114.
11. Dai, S., Zhang, T., Zhang, Y., Wang, H.,Deng, F., 2018a. Zika Virus Baculovirus-Expressed Virus-Like Particles Induce Neutralizing Antibodies in Mice. Virol Sin, 33, 213-226.
12. Dai, S., Zhang, Y., Zhang, T., Zhang, B., Wang, H.,Deng, F., 2018b. Establishment of Baculovirus-Expressed VLPs Induced Syncytial Formation Assay for Flavivirus Antiviral Screening. Viruses, 10.
13. Darwish, M., Hoogstraal, H., Roberts, T., Ahmed, I.,Omar, F., 1983. A sero-epidemiological survey for certain arboviruses (Togaviridae) in Pakistan. Trans R Soc Trop Med Hyg, 77, 442-445.
14. Darwish. Ma, Hoogstraal. H, Roberts. Tj, Ghazi. R,Amer. T, 1983. A sero-epidemiological survey for Bunyaviridae and certain other arboviruses in Pakistan. Trans R Soc Trop Med Hyg, 77(4), 446-450.
15. Fazal, O.,Hotez, P.J., 2020. NTDs in the age of urbanization, climate change, and conflict: Karachi, Pakistan as a case study. PLoS Negl Trop Dis, 14, e0008791.
16. Guo, R., Shen, S., Zhang, Y., Shi, J., Su, Z., Liu, D., Liu, J., Yang, J., Wang, Q., Hu, Z., Zhang, Y.,Deng, F., 2017. A new strain of Crimean-Congo hemorrhagic fever virus isolated from Xinjiang, China. Virol Sin, 32, 80-88.
17. Heymann, D.L., Hodgson, A., Sall, A.A., Freedman, D.O., Staples, J.E., Althabe, F., Baruah, K., Mahmud, G., Kandun, N., Vasconcelos, P.F.C., Bino, S.,Menon, K.U., 2016. Zika virus and microcephaly: why is this situation a PHEIC? The Lancet, 387, 719-721.
18. Huang, D., Jiang, Y., Liu, X., Wang, B., Shi, J., Su, Z., Wang, H., Wang, T., Tang, S., Liu, H., Hu, Z., Deng, F.,Shen, S., 2017. A Cluster of Symptomatic and Asymptomatic Infections of Severe Fever with Thrombocytopenia Syndrome Caused by Person-to-Person Transmission. Am J Trop Med Hyg, 97, 396-402.
19. Khan, M.A., Imtiaz, K., Shafaq, H., Farooqi, J., Hassan, M., Zafar, A., Long, M.T., Barr, K.L.,Khan, E., 2022. Screening for arboviruses in healthy blood donors: Experience from Karachi, Pakistan. Virol Sin, 37, 774-777.
20. Lvov, D., Sidorova, G., Gromashevsky, V., Kurbanov, M., Skvoztsova, L., Gofman, Y., Berezina, L., Klimenko, S., Zakharyan, V., Aristova, V.,Vm., N., 1976a. Virus "Tamdy"-a new arbovirus, isolated in the Uzbee S.S.R. and Turkmen S.S.R. from ticks Hyalomma asiaticum asiaticum Schulee et Schlottke, 1929, and Hyalomma plumbeum plumbeum Panzer, 1796. . Arch Virol., 51(1-2), 15-21.
21. Lvov, D., Vm., N., Gromashevsky, V., Skvortsova, T., Berezina, L., Sidorova, G., Zhmaeva, Z., Gofman, Y., Klimenko, S.,Fomina, K., 1976b. "Karshi" virus, a new flavivirus (Togaviridae) isolated from Ornithodoros papillipes (Birula, 1895) ticks in Uzbek S.S.R. Arch Virol., 50(1-2), 29-36.
22. Mlakar, J., Korva, M., Tul, N., Popovic, M., Poljsak-Prijatelj, M., Mraz, J., Kolenc, M., Resman Rus, K., Vesnaver Vipotnik, T., Fabjan Vodusek, V., Vizjak, A., Pizem, J., Petrovec, M.,Avsic Zupanc, T., 2016. Zika Virus Associated with Microcephaly. N Engl J Med, 374, 951-958.
23. Moming, A., Shen, S., Fang, Y., Zhang, J., Zhang, Y., Tang, S., Li, T., Hu, Z., Wang, H., Zhang, Y., Sun, S., Wang, L.F.,Deng, F., 2021. Evidence of Human Exposure to Tamdy Virus, Northwest China. Emerg Infect Dis, 27, 3166-3170.
24. Moming, A., Bai, Y., Chen, S., Wu, Q., Wang, J., Jin, J., Tang, S., Sun, S., Zhang, Y., Shen, S.,Deng, F., 2023. Epidemiological surveys revealed the risk of tick-borne Tamdy virus spillover to hosts. Infect Dis (Lond), 18:1-7.
25. Mostafavi, E., Ghasemian, A., Abdinasir, A., Nematollahi Mahani, S.A., Rawaf, S., Salehi Vaziri, M., Gouya, M.M., Minh Nhu Nguyen, T., Al Awaidy, S., Al Ariqi, L., Islam, M.M., Abu Baker Abd Farag, E., Obtel, M., Omondi Mala, P., Matar, G.M., Asghar, R.J., Barakat, A., Sahak, M.N., Abdulmonem Mansouri, M.,Swaka, A., 2021. Emerging and Re-emerging Infectious Diseases in the WHO Eastern Mediterranean Region, 2001-2018. Int J Health Policy Manag, 10.34172/ijhpm.2021.13.
26. Raza, F.A., Javed, H., Khan, M.M., Ullah, O., Fatima, A., Zaheer, M., Mohsin, S., Hasnain, S., Khalid, R.,Salam, A.A., 2021. Dengue and Chikungunya virus co-infection in major metropolitan cities of provinces of Punjab and Khyber Pakhtunkhwa: A multi-center study. PLoS Negl Trop Dis, 15, e0009802.
27. Shen, S., Duan, X., Wang, B., Zhu, L., Zhang, Y., Zhang, J., Wang, J., Luo, T., Kou, C., Liu, D., Lv, C., Zhang, L., Chang, C., Su, Z., Tang, S., Qiao, J., Moming, A., Wang, C., Abudurexiti, A., Wang, H., Hu, Z., Zhang, Y., Sun, S.,Deng, F., 2018. A novel tick-borne phlebovirus, closely related to severe fever with thrombocytopenia syndrome virus and Heartland virus, is a potential pathogen. Emerg Microbes Infect, 7, 95.
28. Waris, A., Anwar, F., Asim, M.,Bibi, F., 2022. Is the bell ringing for another outbreak of Crimean-Congo hemorrhagic fever in Pakistan? Public Health Pract (Oxf), 4, 100319.
29. Yadav, P.D., Malhotra, B., Sapkal, G., Nyayanit, D.A., Deshpande, G., Gupta, N., Padinjaremattathil, U.T., Sharma, H., Sahay, R.R., Sharma, P.,Mourya, D.T., 2019. Zika virus outbreak in Rajasthan, India in 2018 was caused by a virus endemic to Asia. Infection, Genetics and Evolution, 69, 199-202.
30. Yousaf, M., Ashfaq, U., Anjum, K.,Fatima, S., 2018. Crimean-Congo Hemorrhagic Fever (CCHF) in Pakistan: The "Bell" is Ringing Silently. Crit Rev Eukaryot Gene Expr, 28(2), 93-100.
31. Zhang, Y., Shen, S., Shi, J., Su, Z., Li, M., Zhang, W., Li, M., Hu, Z., Peng, C., Zheng, X.,Deng, F., 2017. Isolation, characterization, and phylogenic analysis of three new severe fever with thrombocytopenia syndrome bunyavirus strains derived from Hubei Province, China. Virol Sin, 32, 89-96.
32. Zhang, Y., Shen, S., Fang, Y., Liu, J., Su, Z., Liang, J., Zhang, Z., Wu, Q., Wang, C., Abudurexiti, A., Hu, Z., Zhang, Y.,Deng, F., 2018. Isolation, Characterization, and Phylogenetic Analysis of Two New Crimean-Congo Hemorrhagic Fever Virus Strains from the Northern Region of Xinjiang Province, China. Virologica Sinica, 33, 74-86.
33. Zhu, L., Yin, F., Moming, A., Zhang, J., Wang, B., Gao, L., Ruan, J., Wu, Q., Wu, N., Wang, H., Deng, F., Lu, G.,Shen, S., 2019. First case of laboratory-confirmed severe fever with thrombocytopenia syndrome disease revealed the risk of SFTSV infection in Xinjiang, China. Emerg Microbes Infect, 8, 1122-1125.
34. Zohaib, A., Saqib, M., Athar, M.A., Hussain, M.H., Sial, A.U., Tayyab, M.H., Batool, M., Sadia, H., Taj, Z., Tahir, U., Jakhrani, M.Y., Tayyab, J., Kakar, M.A., Shahid, M.F., Yaqub, T., Zhang, J., Wu, Q., Deng, F., Corman, V.M., Shen, S., Khan, I.,Shi, Z.L., 2020a. Crimean-Congo Hemorrhagic Fever Virus in Humans and Livestock, Pakistan, 2015-2017. Emerg Infect Dis, 26, 773-777.
35. Zohaib, A., Zhang, J., Saqib, M., Athar, M.A., Hussain, M.H., Chen, J., Sial, A.U., Tayyab, M.H., Batool, M., Khan, S., Luo, Y., Waruhiu, C., Taj, Z., Hayder, Z., Ahmed, R., Siddique, A.B., Yang, X., Qureshi, M.A., Ujjan, I.U., Lail, A., Khan, I., Sajjad Ur, R., Zhang, T., Deng, F., Shi, Z.,Shen, S., 2020b. Serologic Evidence of Severe Fever with Thrombocytopenia Syndrome Virus and Related Viruses in Pakistan. Emerg Infect Dis, 26, 1513-1516.
Proportional views