SPECIAL ARTICLE |
https://doi.org/10.5005/jacm-11020-0006 |
Arboviral Diagnostics in India: A Multicentric Survey
1Malabar Medical College and Research Centre, Kozhikode, Kerala, India
2Government Medical College and Hospital, Chandrapur, Maharashtra, India
3Amala Institute of Medical Sciences, Thrissur, Kerala, India
4Dr Moopen’s Medical College, Wayanad, Kerala, India
5Sree Gokulam Medical College and Research Foundation, Thiruvananthapuram, Kerala, India
6Government Medical College, Ernakulam, Kerala, India
7Government Medical College, Thiruvananthapuram, Kerala, India
8Smita Memorial Hospital and Research Centre, Vengalloor, Kerala, India
9ESIC Medical College and Hospital, Chennai, Tamil Nadu, India
10RajaRajeswari Medical College & Hospital, Bengaluru, Karnataka, India
11JSS Medical College and Hospital, Mysuru, Karnataka, India
12Government Medical College, Kollam, Kerala, India
13Mahaveer Institute of Medical Sciences, Vikarabad, Telangana, India
14Baby Memorial Hospital, Kozhikode, Kerala, India
15Government Medical College, Thrissur, Kerala, India
16KMCT Medical College, Kozhikode, Kerala, India
17Vasavi Diagnostic Laboratory, Chitradurga, Karnataka, India
18Basaveshwara Medical College and Hospital, Chitradurga, Karnataka, India
19Jubilee Mission Medical College and Research Institute, Thrissur, Kerala, India
20Tata Medical Center, Kolkata, West Bengal, India
21KIMS Alshifa Super Specialty Hospital, Perinthalmanna, Kerala, India
22Believers Church Medical College Hospital, Thiruvalla, Kerala, India
23PK Das Institute of Medical Sciences, Palakkad, Kerala, India
24Sapthagiri Institute of Medical Sciences & Research Centre (SIMSRC), Bengaluru, Karnataka, India
25Lakeshore Hospital and Research Centre, Ernakulam, Kerala, India
26Maharashtra Institute of Medical Education and Research, Medical College, Talegaon Dabhade, Maharashtra, India
27The Oxford Medical College, Hospital and Research Centre, Jigala, Karnataka, India
28Rainbow Children’s Hospitals, Hyderabad, Telangana, India
29Rainbow Children’s Hospital and BirthRight, Chennai, Tamil Nadu, India
30Trinity Diagnostics, Palakkad, Kerala, India
31Rajagiri Hospital, Ernakulam, Kerala, India
32Narayana Multispeciality Hospital, Ahmedabad, Gujarat, India
33Renai Medicity, Ernakulam, Kerala, India
34Government Medical College, Kozhikode, Kerala, India
35Jorhat Medical College and Hospital, Jorhat, Assam, India
36ESIC Medical College and Hospital, Hyderabad, Telangana, India
37Department of Microbiology, Basavatarakam Indo American Cancer Hospital and Research Institute, Hyderabad, Telangana, India
38Government Medical College and Hospital, Chandigarh, India
39Bangalore Medical College and Research Institute, Bengaluru, Karnataka, India
40Department of Clinical Microbiology, All India Institute of Medical Sciences (AIIMS), Mangalagiri, Guntur, Andhra Pradesh, India
Corresponding Author: Ramakrishna Pai Jakribettu, Department of Clinical Microbiology, All India Institute of Medical Sciences (AIIMS), Mangalagiri, Guntur, Andhra Pradesh, India, Phone: +91 9986415211, e-mail: Ramakrishna.paij@gmail.com
Received: 20 April 2024; Accepted: 09 July 2024; Published on: 26 July 2024
ABSTRACT
Background: Arboviruses are arthropod-borne viruses transmitted during the blood meal of the arthropod. These arboviruses are considered to be emerging and reemerging infections.
Aims and objectives: This survey is being conducted to determine the testing capacity of various hospitals and laboratories for arboviral infections, their testing methods, and positivity rate.
Materials and methods: This questionnaire-based study was conducted after obtaining ethical clearance. The questionnaire was circulated via email, WhatsApp, or other electronic modes to clinical microbiologists in India. Data were collected on testing for dengue, chikungunya, Japanese encephalitis (JE), Kyasanur forest disease (KFD), Zika, and West Nile virus from June 2022 to May 2023 (1 year). The collected data were tabulated and analyzed using frequency and percentages.
Results: A total of 39 testing facilities responded to the questionnaire. Among these facilities, 20 (51.28%) were from Kerala, and 26 (66.6%) were teaching hospitals, of which 15 (38.46%) were private. Two (5.1%) were stand-alone private laboratories. Rapid diagnostic tests (RDTs), immunoglobulin M (IgM) enzyme-linked immunosorbent assay (ELISA), and reverse transcription polymerase chain reaction (RT-PCR) for ribonucleic acid (RNA) detection were the common tests performed. A total of 1,07,535 samples were tested for the six major arboviral infections, with dengue accounting for 93.59% of the tests conducted. All these diseases are reportable under the Integrated Disease Surveillance Programme (IDSP). Facility for viral culture and isolation, considered the gold standard for diagnosing viral diseases, was not available at any of the centers.
Conclusion: This survey is the first of its kind to examine arboviral disease testing capacity across 39 diagnostic facilities in India. Dengue diagnosis was the most common among the arboviral diseases tested. However, paradoxically, tests for potentially fatal viral infections, like Japanese encephalitis virus (JEV), and IgM ELISA for KFD, are only available at referral centers. This study highlights the need for improved capacity building for arboviral disease detection across the country. Early diagnosis is crucial for controlling the spread of these viruses in communities.
Keywords: Arboviral diagnostics, Chikungunya, Dengue, Japanese encephalitis virus, Polymerase chain reaction (PCR), Survey
How to cite this article: John JS, Surpam R, Velayudhan SK, et al. Arboviral Diagnostics in India: A Multicentric Survey. J Acad Clin Microbiol 2024;26(1):29–34.
Source of support: Nil
Conflict of interest: Dr Renu Mathew is associated as the National Editorial Board member of this journal and this manuscript was subjected to this journal’s standard review procedures, with this peer review handled independently of this editorial board member and his research group; Dr Ranganathan Natarajan Iyer is associated as Editorin- Chief of this journal and this manuscript was subjected to this journal’s standard review procedures, with this peer review handled independently of the Editor-in-Chief and his research group.
INTRODUCTION
Arboviruses, ribonucleic acid (RNA) viruses, are transmitted by blood-feeding arthropods to vertebrate hosts, including humans.1 These viruses are primarily transmitted through the bite of infected arthropods during a blood meal. Mosquitoes, ticks, and some endemic flies, such as sandflies, are the main arthropod vectors. Based on the clinical features they produce, arboviruses are classified into three main categories: hemorrhagic fever, encephalitis, and arthritis.2 Common arboviruses causing hemorrhagic fever include dengue, Kyasanur forest disease (KFD), yellow fever, and Omsk hemorrhagic fever. Those causing encephalitis include Japanese encephalitis (JE), West Nile encephalitis virus (WNV), equine encephalitis viruses, and Chandipura virus. Chikungunya virus and Zika virus (ZIKV) primarily cause arthritis.
Globally, arboviral diseases are estimated to cause over one million deaths annually.2 These diseases are primarily found in tropical and subtropical regions. The incidence of arboviral diseases has risen over the past two decades, likely due to factors such as increased global travel, rapid unplanned urbanization, and human encroachment on wild spaces for recreation. Global climate change is also a significant contributor, leading to an increase in vector density, development, survival, and pathogen reproduction within these vectors.3
In India, mosquito-borne arboviral diseases include dengue, chikungunya, ZIKV, and yellow fever, transmitted by Aedes mosquitoes. JE is transmitted by Culex mosquitoes. KFD is the major tick-borne arboviral disease in India.4 India reports over one million arboviral disease cases annually, bearing a high burden of these illnesses.5 Due to late presentation, diagnosis of arboviral diseases in India often occurs at tertiary care facilities like district and teaching hospitals. These hospitals have the specialized testing methods required, such as enzyme-linked immunosorbent assays [ELISAs/enzyme-linked fluorescent assay (ELFA)/chemiluminescent immunoassay (CLIA)] for early antigen and antibody detection, and polymerase chain reaction (PCR) for early viral gene detection. While rapid diagnostic tests (RDTs) offer advantages in ease of use and speed, their lower sensitivity and specificity limit their role.
To diagnose and control these diseases in India, the Ministry of Health and Family Welfare (MoHFW), Government of India, has formulated various programs like the National Vector Borne Disease Control Programme (NVBDCP), and under the Department of Health Research (DHR), funding for the establishment of the Viral Research and Diagnostic Laboratory (VRDL) network has been formulated.5 From time to time, guidelines for the detection of viral diseases are provided by the National Institute of Virology (NIV), Pune. During the coronavirus disease 2019 pandemic, all teaching hospitals established BSL-II RT-PCR labs, which are similar to VRDL, increasing the country’s testing capacity for viral diseases. All notifiable arboviral diseases that are detected are notified through the Integrated Disease Surveillance Programme (IDSP) from both private and public sectors to the health authority on a daily basis.6 Thus, this study was undertaken to determine the testing capacity of various hospitals and laboratories for arboviral infection, the methods of testing and reporting, the approximate number of tests performed, and the positivity rate of the arboviral diseases tested in these laboratories.
MATERIALS AND METHODS
This was a questionnaire-based study conducted after obtaining ethical clearance. The questionnaire (attached below), which was validated by senior members and the editorial board of the journal published by the Academy of Clinical Microbiologists (ACM), was circulated by email, WhatsApp, and other electronic modes to various members of ACM and other clinical microbiologists in India.
The questionnaire (Fig. 1) consisted of questions pertaining to the type of facility, details of the head of the laboratory and reporting personnel, type of test done for detection of antigen or IgM antibody, and the total number of samples tested for dengue, chikungunya, JE, KFD, Zika, and West Nile virus from June 2022 to May 2023 (1 year). The collected data were tabulated and analyzed by frequency and percentage. The participants of the study were given authorship in publication in order of the amount of data submitted, as mentioned in the questionnaire that was circulated. No other incentives were given.
Fig. 1: Month-wise distribution of the positivity of Dengue cases during the survey period
RESULTS
The questionnaire was filled out and submitted by 39 centers across India. Among the 39 centers, 20 (51.28%) were from the state of Kerala, followed by Karnataka (7, 17.95%) and Telangana (4, 10.26%), as depicted in Table 1. Twenty-six (66.6%) centers were teaching hospitals, of which 15 (38.46%) were private and 11 (28.32%) were government medical colleges. There were 11 private hospitals, accounting for 28.2%, and 2 (5.1%) stand-alone private laboratories (Table 2). The diagnostic methods commonly used in these centers were RDT, IgM ELISA, and RT-PCR for RNA detection (Table 3). A total of 1,07,535 samples were tested for six major arboviral infections among the centers, of which dengue accounted for 93.59% (Table 4). As all these diseases were reportable under the Integrated Disease Surveillance Project, all centers reported to the respective district authorities regularly. Viral culture and isolation, the gold standard for the diagnosis of viral diseases, was not available in any of the centers.
| State | Number of center (N = 39) | % |
|---|---|---|
| Kerala | 20 | 51.28 |
| Karnataka | 7 | 17.95 |
| Telangana | 4 | 10.26 |
| Maharashtra | 2 | 5.13 |
| Tamil Nadu | 2 | 5.13 |
| Assam | 1 | 2.56 |
| Chandigarh | 1 | 2.56 |
| Gujarat | 1 | 2.56 |
| West Bengal | 1 | 2.56 |
| Type of facility | Number of center (N = 39) | % |
|---|---|---|
| Government medical college | 11 (9 NIV) | 28.2 |
| Private medical college | 15 | 38.46 |
| Private hospital | 11 | 28.2 |
| Private diagnostic lab | 2 | 5.1 |
| Total | 39 |
| Method of testing | Dengue (N = 39) | Chikungunya | JEV | KFD | Zika | West Nile | |||||||
|---|---|---|---|---|---|---|---|---|---|---|---|---|---|
| N | % | N | % | N | % | N | % | N | % | N | % | ||
| RDT | – | 25 | 64.10 | 4 | 10.26 | – | – | – | – | – | – | – | – |
| ELISA | NS1 | 11 | 28.21 | – | – | – | – | – | – | – | – | – | |
| IgM | 18 | 46.15 | 6 | 15.38 | 4 | 10.26 | 1 | 2.56 | – | – | 2 | 5.1 | |
| ELFA | – | 4 | 10.26 | – | – | – | – | – | – | – | – | – | |
| PCR | – | 4 | 10.26 | 1 | 2.56 | – | – | 1 | 2.56 | 5 | 12.82 | – | – |
| Samples tested (n = 1,07,535) | Positive | % of positivity | |
|---|---|---|---|
| Dengue | 1,00,637 (93.59%) | 13,958 | 13.87 |
| Chikungunya | 4,913 (4.57%) | 946 | 19.26 |
| JE | 996 (0.93%) | 254 | 25.5 |
| KFD | 48 (0.04%) | 0 | 0 |
| Zika Virus | 885 (0.82%) | 1 | 0.11 |
| West Nile | 56 (0.05) | 1 | 1.79 |
Dengue Virus
All 39 centers were testing for dengue virus. Twenty-five centers were performing rapid immunochromatography tests for dengue virus, 11 were performing ELISA for NS1, and 18 and 4 centers were performing IgM antibody tests for dengue by ELISA and ELFA, respectively (Table 3). Nucleic acid detection by RT-PCR for Dengue virus was conducted at only four centers. Among the 25 centers testing with rapid tests, kits from seven different manufacturers were used, with J. Mitra Pvt. Co Ltd. and Tulip Diagnostics being used in 13 and 4 centers, respectively (Table 5). The centers performing ELISA NS1 and IgM antibody tests used kits from six manufacturers. Nucleic acid amplification tests (NAAT) like RT-PCR were conducted in four centers, of which three were government medical colleges with VRDL funded by DHR, and one center performing TruNat (Molbio Pvt. Ltd., Goa) was a private multispecialty hospital. Kits provided by three different manufacturers were used for NAAT (Table 5).
| Dengue | Chikungunya | JE | KFD | Zika | West Nile | ||||||||
|---|---|---|---|---|---|---|---|---|---|---|---|---|---|
| Rapid | ELISA NS1 | ELISA IgM | NAAT | Rapid | ELISA IgM | NAAT | ELISA | NAAT | ELISA IgM | NAAT | NAAT | ELISA | |
| Number of centers performing tests | 25 | 11 | 18 | 4 | 4 | 6 | 1 | 4 | Nil | 1 | 1 | 5 | 2 |
| Number of manufactures | 7 | 6 | 5 | 3 | 2 | 1 | 1 | 1 | 1 | 1 | 1 | 2 | |
| Name of the manufacturer | |||||||||||||
| J Mitra | 13 | 3 | 2 | 3 | |||||||||
| Alpine Biomedicals | 1 | 1 | |||||||||||
| Bioline | 1 | ||||||||||||
| Dengue check (Tulip) | 4 | ||||||||||||
| SD Biosensor | 2 | 1 | 2 | 1 | |||||||||
| Erba | 2 | ||||||||||||
| Meriscreen (Meril Diagnostics) | 1 | 1 | |||||||||||
| Pan Bio | 3 | 5 | |||||||||||
| Qualisa | 2 | ||||||||||||
| NIV | 1 | 9 | 1 | 6 | 4 | 1 | 1 | 5 | |||||
| bioMérieux | 4 | ||||||||||||
| Altona | 2 | ||||||||||||
| Molbio | 1 | 1 | |||||||||||
| Diapro Diagnostics | 1 | ||||||||||||
During the study period, 13,958 (13.87%) samples tested positive for dengue out of 1,00,637 samples (Table 4). It was observed that the positivity rate of dengue cases was lowest in summer (i.e., February–April 2023), with a rise in rates between July and November 2022 corresponding to the monsoon season in India, and a decrease in rates from December 2022 to February 2023 (winter) (Fig. 1).
Chikungunya Virus
Diagnosis of Chikungunya virus infection was conducted using rapid tests and IgM ELISA in four and six laboratories, respectively (Table 3). For rapid testing, kits from only two manufacturers were used. Detection of IgM by ELISA in all six VRDL centers was done using kits from NIV, Pune (Table 5). TruNat was used in only one center in Gujarat for nucleic acid detection. The overall positivity rate was 19.26%, with 946 positive cases among 4,913 samples tested for Chikungunya (Table 4). No seasonal variation was observed in the positivity of Chikungunya cases.
Japanese Encephalitis Virus
The serology for JEV was conducted in only four centers (Table 3). All centers used JEV IgM ELISA kits from NIV Pune (Table 5). Among 996 samples tested, 254 (25.5%) tested positive for JEV IgM ELISA (Table 4). The highest positivity was detected in Jorhat, Assam (32.7%), followed by Bengaluru, Karnataka (13.3%), Thrissur, Kerala (11.7%), and Kozhikode, Kerala (1.65%).
Kyasanur Forest Disease
It was tested only in one center in Kerala using kits for IgM ELISA and RT-PCR from NIV, Pune (Table 3). A total of 48 samples were tested during the study period with no positive cases reported.
Zika Virus
During the study period, only five centers (Thiruvananthapuram, Thrissur, Kozhikode in Kerala, Jorhat in Assam, and Bengaluru in Karnataka) tested for ZIKV using RT-PCR kits from NIV Pune. A total of 885 samples were tested during the study period, with only one reported as positive from Thiruvananthapuram.
West Nile Virus
The testing for WNV was conducted in two centers during the study period, namely Kozhikode, Kerala, and Jorhat, Assam. They tested for IgM using ELISA kits from NIV, Pune, and another manufacturer. Out of 56 samples tested for WNV, only one sample tested positive.
DISCUSSION
This special article focuses on the current diagnostic methodologies used by various centers across India for the diagnosis of arboviral diseases. In India, Dengue, Chikungunya, and JEV diseases are of primary concern. These viral diseases are known to exhibit seasonal variations in incidence due to vector breeding, such as mosquitoes. It is observed that the seasonal variation with increased dengue cases between July and November in the study is similar to national data.5
When analyzing the facilities testing for arboviral diseases, it was found that dengue is tested in all centers. Many government colleges have established VRDLs funded by Indian Council of Medical Research (ICMR) (DHR), equipped with IgM ELISA kits from NIV, Pune for diagnosing Dengue. However, many centers are also using RDTs for NS1, IgM, and IgG detection against Dengue virus. The national program like NVBDCP and internationally World Health Organization (WHO)7 do not recommend the use of RDTs for the diagnosis of Dengue due to lack of proper validation of these kits and variations in sensitivity and specificity among commercially available kits. This is the only testing mode for dengue in 25 (64.1%) centers, and we do not recommend the use of RDTs for the diagnosis of dengue as per WHO guidelines. The test positivity for dengue varied between 3.31 and 23.79%, with an average of 13.86% among the centers. This is lower than the overall seroprevalence of dengue fever based on a systematic review that included seven studies from India.8 This shows that the seroprevalence of dengue in the community and among the cases diagnosed in healthcare settings are different, as our study included patients seeking medical assistance from healthcare settings (Fig. 1).
Chikungunya virus has gained importance in recent years as a re-emerging arboviral disease. This is reflected in the survey, as only 6 out of 39 centers are performing IgM ELISA, all of which are in the public sector. According to guidelines, Chikungunya is diagnosed with direct evidence of the virus by detecting viral RNA using RT-PCR or isolating the virus from the patient’s blood sample, or with indirect evidence by detecting IgM ELISA in the serum. Our survey reported a positivity rate of 19.26% (946 out of 4,913), which is similar to a lab-based survey data showing a 20.5% positivity among 49,380 sera tested between 2016 and 2018 in India.9 An ICMR-funded multicentric seroprevalence study observed a test positivity rate of 18.1% among 12,300 individuals.10
Japanese encephalitis virus (JEV) disease is a zoonotic disease transmitted from animals to birds to humans by mosquitoes. This neurotropic virus causes fever along with varying neurological symptoms ranging from headache to meningitis or encephalitis. It is endemic in many states of India, especially in northeastern states.5 As per national guidelines, IgM ELISA against JEV from serum or cerebrospinal fluid (CSF) is considered to be one of the confirmatory tests for JEV. In our survey, we observed a high positivity rate of 32.7% from a single center in Assam among the four centers performing IgM ELISA using kits from NIV, Pune. The ICMR has established >15 Apex referral laboratories across India for the early diagnosis and control of JE.11
Kyasanur forest disease, a viral hemorrhagic fever, is caused by an arbovirus belonging to the Flaviviridae family. It is transmitted to humans by the bite of ticks and is restricted to districts along the Western Ghats from Goa to Kerala to Tamil Nadu.12 It is one of the pathogens classified under Biosafety level 4 and requires a Biosafety level 3 laboratory for viral culture.13 In India, the NIV in Pune supplies both IgM ELISA and RT-PCR tests for RNA detection to VRDL laboratories located in endemic areas like Karnataka and Kerala. However, no cases were reported from these laboratories during the study period.
Zika virus, an enveloped RNA virus in the Flaviviridae family, is primarily transmitted by Aedes aegypti mosquitoes, similar to dengue and chikungunya. However, ZIKV can also be transmitted through non-vector-borne routes, including mother-to-child transmission, blood transfusion, organ transplantation, sexual intercourse, and even accidental laboratory exposure. In newborns, ZIKV infection is associated with complications like microcephaly, congenital glaucoma, and ventriculomegaly. Adults with ZIKV infection are strongly suspected to be at an increased risk for Guillain–Barré syndrome.14 For early diagnosis of the infection, detection of viral RNA and serological tests like IgM ELISA are recommended methods by WHO. During our study, only one sample tested positive out of 885 samples tested for Zika virus using the RT-PCR kit from NIV Pune.
West Nile Virus (WNV) is an RNA virus transmitted by ornithophilic mosquitoes such as Culex species. Like JE, it is a neurotropic virus that can cause severe diseases like encephalitis. Despite WNV being isolated from vectors in India, no serious epidemics have been reported. It is postulated that the transmission rate is low due to the presence of other flaviviruses among the vectors.15 The laboratories used only IgM ELISA for the diagnosis of WNV, and during the study period, one sample tested positive out of 56 samples tested. No molecular test was available to detect RNA in any of the centers.
This survey has revealed that tests for dengue are available in all participating centers, whereas for other reemerging arboviral diseases, testing was limited to tertiary care centers or referral laboratories. The National Center for Vector Borne Disease Control (NCVBDC), Government of India, has established various sentinel surveillance labs and apex referral labs, providing kits for testing various arboviral diseases.5 India, as the first country to release the National Essential Diagnostic List (NEDL) following the Essential Diagnostics List released by WHO in 2018, has included ELISA for Dengue in all district hospitals and JE in endemic areas.16 In the future, the scope of services provided by these laboratories should be extended to include other endemic arboviruses. This expansion is crucial not only for early diagnosis and treatment but also to reduce complications and mortality caused by these arboviral diseases.
CONCLUSION
This survey on arboviral disease testing capacity across 39 diagnostic facilities in India is the first of its kind. It identifies the various testing facilities available for different arboviral infections. Among these diseases, dengue diagnosis is commonly conducted in most laboratories. However, for fatal viral infections like JEV and KFD, serological tests such as IgM ELISA are only available in referral centers. This study recommends enhancing capacity building for arboviral disease detection nationwide, enabling early diagnosis and control of virus spread within the community.
REFERENCES
1. Eldridge BF, Scott TW, Day JF, et al. Arbovirus diseases. Medical Entomology. 2000. pp. 415–460.
2. Surveillance and control of arboviral diseases in the WHO African region: assessment of country capacities. Geneva: World Health Organization; 2022.
3. Baylis M. Potential impact of climate change on emerging vector-borne and other infections in the UK. Environ Health 2017;16(Suppl 1):112. DOI: 10.1186/s12940-017-0326-1
4. Shanmugam L, Kumaresan M, Kundu R, et al. Arboviruses in human disease: an Indian perspective. Int J Adv Med Health Res 2022;9:69–77. DOI: 10.4103/ijamr.ijamr_237_22
5. National Guidelines for Clinical Management of Dengue Fever 2023. National Center for Vector Borne Diseases Control, Directorate General of Health Services, Ministry of Health & Family Welfare Government of India, New Delhi.
6. Policy and Strategic plan for The India- Integrated Health Information Platform (IHIP), 2023. IDSP/IHIP Division, National Centre for Disease Control, Directorate General of Health Services, MoHFW, Govt of India.
7. Dengue: guidelines for diagnosis, treatment, prevention and control. 2019, WHO France. 2019.
8. Ganeshkumar P, Murhekar MV, Poornima V, et al. Dengue infection in India: a systematic review and meta-analysis. PLoS Negl Trop Dis 2018;12(7):e0006618. DOI: 10.1371/journal.pntd.0006618
9. Murhekar M, Kanagasabai K, Shete V, et al. Epidemiology of chikungunya based on laboratory surveillance data-India, 2016-2018. Trans R Soc Trop Med Hyg 2019;113(5):259–262. DOI: 10.1093/trstmh/try141
10. Kumar MS, Kamaraj P, Khan SA, et al. Seroprevalence of chikungunya virus infection in India, 2017: a cross-sectional population-based serosurvey. The Lancet Microbe 2021;2(1):e41–e47. DOI: 10.1016/S2666-5247(20)30175-0
11. National Programme for Prevention and Control of Japanese Encephalitis/Acute Encephalitis Syndrome. 2014. National Vector Borne Disease Control Programme, Directorate General of Health Services, Ministry of Health & Family Welfare, Government of India, New Delhi.
12. Munivenkatappa A, Sahay RR, Yadav PD, et al. Clinical & epidemiological significance of Kyasanur forest disease. Indian J Med Res 2018;148(2):145–150. DOI: 10.4103/ijmr.IJMR_688_17
13. Banerjee K. Kyasanur forest disease. In: Monath TP (Ed). Arboviruses: Epidemiology and Ecology. Boca Raton, Florida: CRC Press; 1990. pp. 93–116.
14. Sah R, Mohanty A, Paul D, et al. Recent outbreak of zika virus in India amid ongoing COVID-19 and monkeypox outbreak: a call for action. Int J Surg 2023;109(3):601–603. DOI: 10.1097/JS9.0000000000000182
15. Khan SA, Dutta P, Khan AM, et al. West Nile virus infection, Assam, India. Emerg Infect Dis 2011;17(5):947–948. DOI: 10.3201/eid1705.100479
16. National Essential Diagnostics List. 2019. Indian Council of Medical. Research, New Delhi. India.
________________________
© The Author(s). 2024 Open Access. This article is distributed under the terms of the Creative Commons Attribution 4.0 International License (https://creativecommons.org/licenses/by-nc/4.0/), which permits unrestricted use, distribution, and non-commercial reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated.