Attrition in serum anti-DENV antibodies correlates with high anti-SARS-CoV-2 IgG levels and low DENV positivity in mosquito vectors-Findings from a state-wide cluster-randomized community-based study in Tamil Nadu, India

Sivaprakasam T Selvavinayagam; Sathish Sankar; Yean K Yong; Abdul R Anshad; Samudi Chandramathi; Anavarathan Somasundaram; Sampath Palani; Parthipan Kumarasamy; Roshini Azhaguvel; Ajith B Kumar; Sudharshini Subramaniam; Manickam Malathi; Venkatachalam Vijayalakshmi; Manivannan Rajeshkumar; Anandhazhvar Kumaresan; Ramendra P Pandey; Nagarajan Muruganandam; Natarajan Gopalan; Meganathan Kannan; Amudhan Murugesan; Pachamuthu Balakrishnan; Siddappa N Byrareddy; Aditya P Dash; Vijayakumar Velu; Marie Larsson; Esaki M Shankar; Sivadoss Raju

doi:10.1371/journal.pgph.0003608

Attrition in serum anti-DENV antibodies correlates with high anti-SARS-CoV-2 IgG levels and low DENV positivity in mosquito vectors-Findings from a state-wide cluster-randomized community-based study in Tamil Nadu, India

PLOS Glob Public Health. 2024 Nov 21;4(11):e0003608. doi: 10.1371/journal.pgph.0003608. eCollection 2024.

Authors

Sivaprakasam T Selvavinayagam¹, Sathish Sankar², Yean K Yong³, Abdul R Anshad⁴, Samudi Chandramathi⁵, Anavarathan Somasundaram⁶, Sampath Palani¹, Parthipan Kumarasamy¹, Roshini Azhaguvel¹, Ajith B Kumar¹, Sudharshini Subramaniam⁶, Manickam Malathi⁷, Venkatachalam Vijayalakshmi⁷, Manivannan Rajeshkumar¹, Anandhazhvar Kumaresan¹, Ramendra P Pandey⁸, Nagarajan Muruganandam⁹, Natarajan Gopalan¹⁰, Meganathan Kannan¹¹, Amudhan Murugesan¹², Pachamuthu Balakrishnan¹³, Siddappa N Byrareddy¹⁴, Aditya P Dash¹⁵, Vijayakumar Velu¹⁶, Marie Larsson¹⁷, Esaki M Shankar⁴, Sivadoss Raju¹

Affiliations

¹ State Public Health Laboratory, Directorate of Public Health and Preventive Medicine, DMS Campus, Teynampet, Chennai, Tamil Nadu, India.
² Department of Microbiology, Saveetha Dental College and Hospitals, Saveetha Institute of Medical and Technical Sciences, Centre for Infectious Diseases, Saveetha University, Chennai, Tamil Nadu, India.
³ Laboratory Centre, Xiamen University Malaysia, Sepang, Selangor, Malaysia.
⁴ Department of Biotechnology, Infection and Inflammation, Central University of Tamil Nadu, Thiruvarur, India.
⁵ Faculty of Medicine, Department of Medical Microbiology, University of Malaya, Lembah Pantai, Kuala Lumpur, Malaysia.
⁶ Institute of Community Medicine, Madras Medical College, Chennai, Tamil Nadu, India.
⁷ Institute of Vector Control and Zoonoses, Hosur, Tamil Nadu, India.
⁸ School of Health Sciences and Technology, UPES, Dehradun, Uttarakhand, India.
⁹ Regional Medical Research Centre, Indian Council of Medical Research, Port Blair, Andaman and Nicobar Islands, India.
¹⁰ Department of Epidemiology and Public Health, Central University of Tamil Nadu, Thiruvarur, India.
¹¹ Department of Biotechnology, Blood and Vascular Biology, Central University of Tamil Nadu, Thiruvarur, India.
¹² Department of Microbiology, Government Theni Medical College and Hospital, Theni, Tamil Nadu, India.
¹³ Saveetha Institute of Medical and Technical Sciences, Center for Infectious Diseases, Saveetha Medical College and Hospital, Saveetha University, Chennai, Tamil Nadu, India.
¹⁴ Department of Pharmacology and Experimental Neuroscience, University of Nebraska Medical Center, Omaha, Nebraska, United States of America.
¹⁵ Asian Institute of Public Health University, Bhubaneswar, Odisha, India.
¹⁶ Department of Pathology and Laboratory Medicine, Division of Microbiology and Immunology, Emory University School of Medicine, Emory National Primate Research Center, Emory Vaccine Center, Atlanta, Georgia, United States of America.
¹⁷ Department of Biomedical and Clinical Sciences, Division of Molecular Medicine and Virology, Linköping University, Linköping, Sweden.

Abstract

The decline in dengue incidence and/or prevalence during the COVID-19 pandemic (2020-22) appears to be attributed to reduced treatment-seeking rates, under-reporting, misdiagnosis, disrupted health services and reduced exposure to mosquito vectors due to prevailing lockdowns. There is limited scientific data on dengue virus (DENV) disease during the COVID-19 pandemic. Here, we conducted a community-based, cross-sectional, cluster-randomized survey to assess anti-DENV and anti-SARS-CoV-2 seroprevalence, and also estimated the spatial distribution of DENV-positive aedine mosquito vectors during the COVID-19 pandemic across all the 38 districts of Tamil Nadu, India. Using real-time PCR, the prevalence of DENV in mosquito pools during 2021 was analyzed and compared with the previous and following years of vector surveillance, and correlated with anti-DENV IgM and IgG levels in the population. Results implicate that both anti-DENV IgM and IgG seroprevalence and DENV positivity in mosquito pools were reduced across all the districts. A total of 13464 mosquito pools and 5577 human serum samples from 186 clusters were collected. Of these, 3.76% of the mosquito pools were positive for DENV. In the human sera, 4.12% were positive for anti-DENV IgM and 6.4% for anti-DENV IgG. While the anti-SARS-CoV-2 levels significantly correlated with overall DENV seropositivity, COVID-19 vaccination status significantly correlated with anti-DENV IgM levels. The study indicates a profound impact of anti-SARS-CoV-2 levels on DENV-positive mosquito pools and seropositivity. Continuous monitoring of anti-DENV antibody levels, especially with the evolving variants of SARS-CoV-2 and the surge in COVID-19 cases will shed light on the distribution, transmission and therapeutic attributes of DENV infection.

Copyright: © 2024 Selvavinayagam et al. This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.

Grants and funding

The study was funded by the National Health Mission (https://www.nhm.tn.gov.in/en), Tamil Nadu (680/NGS/NHMTNMSC/ENGG/2021) for the Directorate of Public Health and Preventive Medicine to S.T.S. and S.R. M.L. is supported by grants through AI52731, the Swedish Research Council (https://www.vr.se/english.html), the Swedish, Physicians against AIDS Research Foundation, the Swedish International Development Cooperation Agency, SIDASARC, VINNMER for Vinnova, Linköping University Hospital Research Fund, CALF, and the Swedish Society of Medicine. V.V. is supported by the Office of Research Infrastructure Programs (ORIP/NIH) (https://orip.nih.gov/home) base grant P51 OD011132 to ENPRC. A.M. is supported by Grant No. 12020/04/2018, Department of Health Research, Government of India (https://dhr.gov.in/). The funders of the study had no role in the study design, data collection, data analysis, data interpretation, or writing of the report.