American Journal of Microbiological Research
ISSN (Print): 2328-4129 ISSN (Online): 2328-4137 Website: http://www.sciepub.com/journal/ajmr Editor-in-chief: Apply for this position
Open Access
Journal Browser
Go
American Journal of Microbiological Research. 2020, 8(4), 117-135
DOI: 10.12691/ajmr-8-4-2
Open AccessArticle

A Comprehensive Prospective Study to Understand Chikungunya Infection in Delhi Region during 2010-2011

Singh Pradeep Kumar1, , Dar Lalit1 and Broor Shobha1

1Department of Microbiology, All India Institute of Medical Sciences, New Delhi, India

Pub. Date: November 02, 2020

Cite this paper:
Singh Pradeep Kumar, Dar Lalit and Broor Shobha. A Comprehensive Prospective Study to Understand Chikungunya Infection in Delhi Region during 2010-2011. American Journal of Microbiological Research. 2020; 8(4):117-135. doi: 10.12691/ajmr-8-4-2

Abstract

INTRODUCTION: Chikungunya is an arbovirus causing febrile illness with high strike rate and is known for outbreaks in more than 60 countries globally. During 2010-2011 unusual high number of suspected Chikungunya infection patients attended AIIMS OPD, Delhi, India. The NCR region with its semiarid geography restricts arbovirus outbreaks to monsoon months and is previously known for Dengue outbreaks although Chikungunya outbreaks were previously unknown to the region. The surge in suspected Chikungunya infection cases indicates a possible outbreak in the NCR region. This comprehensive prospective and follow-up study was designed to understand the Chikungunya infection among patients attending AIIMS OPD during 2010-11. METHOD: During June 2010 to Dec 2011, 2346 blood samples were collected from outpatients and inpatients attending AIIMS OPD, New Delhi. Samples were grouped in acute and chronic cases. Some patients were also enrolled for year-long follow-up study. Serum samples were tested for CHIKV using PCR and for IgM antibodies to chikungunya virus by IgM-capture ELISA. Real-time PCR was performed targeting the E1 gene for viral load determination in patient sera. RESULT: CHIKV positivity of 35% (746/2112) in acute and 67% (156/234) in chronic suspected cases were found by ELISA. most affected patients belonged to the age group >30-45 yrs. and above in both genders. Acute confirmed cases included 383 (51.3%) females and 363 (48.7%) males and chronic includes 92 (58.9%) females and 64 (41.1%) males. Clinical symptoms include polyarthralgia, fever, and rashes. Maximum positivity was seen in Oct-Nov of both years. During follow-up study, 118 patients enrolled, persisting polyarthralgia and anti-CHIKV IgM was detected up to 2 years while circulating CHIKV was detected by PCR up to 3 months in few patients. CONCLUSION: Chikungunya virus has emerged in Delhi during 2010 and contributed to about 30-40% of fever and arthralgia. CHIKV prevalence is highest in post monsoon month of October. The virus can remain in blood circulation for weeks, while anti-CHIKV IgM can persist for more than a year with complaints of periodic polyarthralgia.

Keywords:
Chikungunya India polyarthralgia followup

Creative CommonsThis work is licensed under a Creative Commons Attribution 4.0 International License. To view a copy of this license, visit http://creativecommons.org/licenses/by/4.0/

Figures

Figure of 11

References:

[1]  Robinson, Marion C. “An epidemic of virus disease in Southern Province, Tanganyika territory, in 1952-1953.” Transactions of the Royal Society of Tropical Medicine and Hygiene. 49, no. 1 (1955): 28-32.
 
[2]  Strauss, James H., and Ellen G. Strauss. “The alphaviruses: gene expression, replication, and evolution.” Microbiological reviews 58, no. 3 (1994): 491.
 
[3]  Simizu, B., K. Yamamoto, K. Hashimoto, and T. Ogata. “Structural proteins of Chikungunya virus.” Journal of virology. 51, no. 1 (1984): 254-258.
 
[4]  Diallo, Mawlouth, Joselyn Thonnon, Mumouni Traore-Lamizana, and Didier Fontenille. “Vectors of Chikungunya virus in Senegal: current data and transmission cycles.” The American journal of tropical medicine and hygiene60, no. 2 (1999): 281-286.
 
[5]  Kumar, N. Pradeep, Rajan Joseph, T. Kamaraj, and P. Jambulingam. “A226V mutation in virus during the 2007 chikungunya outbreak in Kerala, India.”Journal of General Virology 89, no. 8 (2008): 1945-1948.
 
[6]  McIntosh, B. M., H. E. Paterson, J. M. Donaldson, and J. De Sousa. “Chikungunya virus: viral susceptibility and transmission studies with some vertebrates and mosquitoes.” S Afr J Med Sci. 28 (1963): 45-52.
 
[7]  Powers, Ann M., and Christopher H. Logue. “Changing patterns of chikungunya virus: re-emergence of a zoonotic arbovirus.” Journal of General Virology. 88, no. 9 (2007): 2363-2377.
 
[8]  Mackenzie, J. S., K. B. Chua, P. W. Daniels, B. T. Eaton, H. E. Field, R. A. Hall, K. Halpin et al. “Emerging viral diseases of Southeast Asia and the Western Pacific.” Emerging infectious diseases. 7, no. 3 Suppl (2001): 497.
 
[9]  Burt, Felicity J., Micheal S. Rolph, Nestor E. Rulli, Suresh Mahalingam, and Mark T. Heise. “Chikungunya: a re-emerging virus.” The Lancet. 379, no. 9816 (2012): 662-671.
 
[10]  Lahariya, Chandrakant, and S. K. Pradhan. “Emergence of chikungunya virus in Indian subcontinent after 32 years: a review.” Journal of vector borne diseases. 43, no. 4 (2006): 151.
 
[11]  Rao, T. Ramachandra. “Immunological surveys of arbovirus infections in South-East Asia, with special reference to dengue, chikungunya, and Kyasanur Forest disease.” Bulletin of the World Health Organization. 44, no. 5 (1971): 585.
 
[12]  Sarkar, J. K., K. M. Pavri, S. N. Chatterjee, S. K. Chakravarty, and C. R. Anderson. “Virological and Serological Studies of Cases of Haemorrhagic Fever in Calcutta. Material Collected by the Calcutta School of Tropical Medicine.”The Indian journal of medical research. 52 (1964): 684-691.
 
[13]  Chretien, Jean-Paul, Assaf Anyamba, Sheryl A. Bedno, Robert F. Breiman, Rosemary Sang, Kibet Sergon, Ann M. Powers et al. “Drought-associated chikungunya emergence along coastal East Africa.” The American journal of tropical medicine and hygiene. 76, no. 3 (2007): 405-407.
 
[14]  Lanciotti, Robert S., Olga L. Kosoy, Janeen J. Laven, Amanda J. Panella, Jason O. Velez, Amy J. Lambert, and Grant L. Campbell. “Chikungunya virus in US travelers returning from India, 2006.” Emerging infectious diseases. 13, no. 5 (2007): 764.
 
[15]  Taubitz, Winfried, Jakob P. Cramer, Anette Kapaun, Martin Pfeffer, Christian Drosten, Gerhard Dobler, Gerd D. Burchard, and Thomas Löscher. “Chikungunya fever in travelers: clinical presentation and course.” Clinical Infectious Diseases. 45, no. 1 (2007): e1-e4.
 
[16]  Hochedez, P., P. Hausfater, S. Jaureguiberry, F. Gay, A. Datry, M. Danis, F. Bricaire, and P. Bossi. “Cases of chikungunya fever imported from the islands of the South West Indian Ocean to Paris, France.” Euro surveillance: bulletin Europeen sur les maladies transmissibles European communicable disease bulletin. 12, no. 1 (2007).
 
[17]  Renault, Philippe, Jean-Louis Solet, Daouda Sissoko, Elsa Balleydier, Sophie Larrieu, Laurent Filleul, Christian Lassalle et al. “A major epidemic of chikungunya virus infection on Reunion Island, France, 2005-2006.” The American journal of tropical medicine and hygiene 77, no. 4 (2007): 727-731.
 
[18]  Borgherini, Gianandrea, Patrice Poubeau, Frederik Staikowsky, Manuella Lory, Nathalie Le Moullec, Jean Philippe Becquart, Catherine Wengling, Alain Michault, and Fabrice Paganin. “Outbreak of chikungunya on Reunion Island: early clinical and laboratory features in 157 adult patients.” Clinical infectious diseases. 44, no. 11 (2007): 1401-1407.
 
[19]  Sanchez, F., Barboza, L.A., Burton, D. and Cintrón-Arias, A., 2018. Comparative analysis of dengue versus chikungunya outbreaks in Costa Rica. Ricerche di Matematica, 67(1), pp.163-174.
 
[20]  Paul, B.J. and Sadanand, S., 2018. Chikungunya Infection: A Re-emerging Epidemic. Rheumatology and therapy, pp.1-10.
 
[21]  Calba, C., Guerbois-Galla, M., Franke, F., Jeannin, C., Auzet-Caillaud, M., Grard, G., Pigaglio, L., Cadiou, B., de Lamballerie, X., Paty, M.C. and Leparc-Goffart, I., 2018. Investigation of an autochthonous chikungunya outbreak, July-September 2017, France. Revue d'Épidémiologie et de Santé Publique, 66, pp.S387-S388.
 
[22]  Venturi, G., Di Luca, M., Fortuna, C., Remoli, M.E., Riccardo, F., Severini, F., Toma, L., Del Manso, M., Benedetti, E., Caporali, M.G. and Amendola, A., 2017. Detection of a chikungunya outbreak in Central Italy, August to September 2017. Eurosurveillance, 22(39).
 
[23]  Delisle, E., Rousseau, C., Broche, B., Leparc-Goffart, I., L’ambert, G., Cochet, A., Prat, C., Foulongne, V., Ferre, J.B., Catelinois, O. and Flusin, O., 2015. Chikungunya outbreak in montpellier, France, September to October 2014. Eurosurveillance, 20(17), p.21108.
 
[24]  Weaver, Scott C. “Arrival of Chikungunya Virus in the New World: Prospects for Spread and Impact on Public Health.” PLOS Neglected Tropical Diseases 8, no. 6 (2014): e2921.
 
[25]  Leparc-Goffart, Isabelle, Antoine Nougairede, Sylvie Cassadou, Christine Prat, and Xavier de Lamballerie. “Chikungunya in the Americas.” Lancet 383, no. 9916 (2014): 514.
 
[26]  Wangchuk, Sonam, Piyawan Chinnawirotpisan, Tshering Dorji, Tashi Tobgay, Tandin Dorji, In-Kyu Yoon, and Stefan Fernandez. “Chikungunya fever outbreak, Bhutan, 2012.” Emerging infectious diseases 19, no. 10 (2013): 1681.
 
[27]  Wu, De, Jie Wu, Qiaoli Zhang, Haojie Zhong, Changwen Ke, and Xiaoling Deng. “Chikungunya outbreak in Guangdong province, China, 2010.” Emerging infectious diseases 18, no. 3 (2012): 493.
 
[28]  Duong, Veasna, Anne-Claire Andries, Chantha Ngan, Touch Sok, Beat Richner, Nima Asgari-Jirhandeh, Steve Bjorge et al. “Reemergence of Chikungunya virus in Cambodia.” Emerging infectious diseases 18, no. 12 (2012): 2066.
 
[29]  Grandadam, Marc, Valérie Caro, Sébastien Plumet, Jean-Michel Thiberge, Yvan Souarès, Anna-Bella Failloux, Hugues J. Tolou et al. “Chikungunya virus, southeastern France.” Emerging infectious diseases 17, no. 5 (2011): 910.
 
[30]  Gould, E. A., P. Gallian, X. De Lamballerie, and R. N. Charrel. “First cases of autochthonous dengue fever and chikungunya fever in France: from bad dream to reality!.” Clinical microbiology and infection 16, no. 12 (2010): 1702-1704.
 
[31]  Rianthavorn, Pornpimol, Kesmanee Prianantathavorn, Norra Wuttirattanakowit, Apiradee Theamboonlers, and Yong Poovorawan. “An outbreak of chikungunya in southern Thailand from 2008 to 2009 caused by African strains with A226V mutation.” International Journal of Infectious Diseases 14 (2010): e161-e165.
 
[32]  Paupy, Christophe, Benjamin Ollomo, Basile Kamgang, Sara Moutailler, Dominique Rousset, Maurice Demanou, Jean-Pierre Hervé, Eric Leroy, and Frédéric Simard. “Comparative role of Aedes albopictus and Aedes aegypti in the emergence of dengue and chikungunya in Central Africa.” Vector-Borne and Zoonotic Diseases 10, no. 3 (2010): 259-266.
 
[33]  Leo, Yee S., Angela LP Chow, Li Kiang Tan, David C. Lye, Li Lin, and Lee C. Ng. “Chikungunya outbreak, Singapore, 2008.” Emerging infectious diseases15, no. 5 (2009): 836.
 
[34]  Ng, Lisa FP, Angela Chow, Yong-Jiang Sun, Dyan JC Kwek, Poh-Lian Lim, Frederico Dimatatac, Lee-Ching Ng et al. “IL-1β, IL-6, and RANTES as biomarkers of Chikungunya severity.” PloS one 4, no. 1 (2009): e4261.
 
[35]  Leroy, Eric M., Dieudoné Nkoghe, Benjamin Ollomo, Chimène Nze-Nkogue, Pierre Becquart, Gilda Grard, Xavier Pourrut et al. “Concurrent chikungunya and dengue virus infections during simultaneous outbreaks, Gabon, 2007.”Emerging infectious diseases 15, no. 4 (2009): 591.
 
[36]  Sam, I., Yoke Fun Chan, Shie Yien Chan, Shih Keng Loong, Hock Khim Chin, Poh Sim Hooi, Rajasekaram Ganeswrie, and Sazaly AbuBakar. “Chikungunya virus of Asian and central/east African genotypes in Malaysia.” Journal of Clinical Virology 46, no. 2 (2009): 180-183.
 
[37]  Schuffenecker, Isabelle, Isabelle Iteman, Alain Michault, Séverine Murri, Lionel Frangeul, Marie-Christine Vaney, Rachel Lavenir et al. “Genome microevolution of chikungunya viruses causing the Indian Ocean outbreak.” PLoS medicine 3, no. 7 (2006): e263.
 
[38]  Charrel, Remi N., Xavier de Lamballerie, and Didier Raoult. “Chikungunya outbreaks-the globalization of vectorborne diseases.” New England Journal of Medicine. 356, no. 8 (2007): 769.
 
[39]  WHO http://www.who.int/csr/don/2006_10_17/en/
 
[40]  Mavalankar, Dileep, Priya Shastri, and Parvathy Raman. “Chikungunya epidemic in India: a major public-health disaster.” The Lancet infectious diseases 7, no. 5 (2007): 306-307.
 
[41]  AbuBakar, Sazaly, I-Ching Sam, Pooi-Fong Wong, NorAziyah MatRahim, Poh-Sim Hooi, and Nuruliza Roslan. “Reemergence of endemic chikungunya, Malaysia.” Emerging infectious diseases 13, no. 1 (2007): 147.
 
[42]  Peyrefitte, Christophe N., Maël Bessaud, Boris AM Pastorino, Patrick Gravier, Sébastien Plumet, Olivier L. Merle, Isabelle Moltini et al. “Circulation of Chikungunya virus in Gabon, 2006-2007.” Journal of medical virology 80, no. 3 (2008): 430-433.
 
[43]  Rezza, G., L. Nicoletti, R. Angelini, R. Romi, A. C. Finarelli, M. Panning, P. Cordioli et al. “Infection with chikungunya virus in Italy: an outbreak in a temperate region.” The Lancet 370, no. 9602 (2007): 1840-1846.
 
[44]  Mizuno, Yasutaka, et al. “Clinical and radiological features of imported chikungunya fever in Japan: a study of six cases at the National Center for Global Health and Medicine.” Journal of Infection and Chemotherapy 17.3 (2011): 419-423.
 
[45]  Hoarau, Jean-Jacques, Marie-Christine Jaffar Bandjee, Pascale Krejbich Trotot, Trina Das, Ghislaine Li-Pat-Yuen, Bérengère Dassa, Mélanie Denizot et al. “Persistent chronic inflammation and infection by Chikungunya arthritogenic alphavirus in spite of a robust host immune response.” The Journal of Immunology 184, no. 10 (2010): 5914-5927.
 
[46]  Sissoko, Daouda, Khaled Ezzedine, Amrat Moendandzé, Claude Giry, Philippe Renault, and Denis Malvy. “Field evaluation of clinical features during chikungunya outbreak in Mayotte, 2005-2006.” Tropical Medicine & International Health 15, no. 5 (2010): 600-607.
 
[47]  Chhabra, M., V. Mittal, D. Bhattacharya, U. V. S. Rana, and S. Lal. “Chikungunya fever: a re-emerging viral infection.” Indian Journal of Medical Microbiology 26, no. 1 (2008): 5.
 
[48]  Win, M. K., A. Chow, F. Dimatatac, C. J. Go, and Y. S. Leo. “Chikungunya fever in Singapore: acute clinical and laboratory features, and factors associated with persistent arthralgia.” Journal of Clinical Virology 49, no. 2 (2010): 111-114.
 
[49]  Pistone, Thierry, Khaled Ezzedine, Marie Boisvert, Marie‐Catherine Receveur, Isabelle Schuffenecker, Hervé Zeller, Marie‐Edith Lafon, Hervé Fleury, and Denis Malvy. “Cluster of chikungunya virus infection in travelers returning from Senegal, 2006.” Journal of travel medicine 16, no. 4 (2009): 286-288.
 
[50]  Chopra, Arvind, V. Anuradha, V. Lagoo-Joshi, V. Kunjir, S. Salvi, and M. Saluja. “Chikungunya virus aches and pains: an emerging challenge.” Arthritis & Rheumatism 58, no. 9 (2008): 2921-2922.
 
[51]  Rolle, A., Schepers, K., Cassadou, S., Curlier, E., Madeux, B., Hermann-Storck, C., Fabre, I., Lamaury, I., Tressieres, B., Thiery, G. and Hoen, B., 2016. Severe sepsis and septic shock associated with chikungunya virus infection, Guadeloupe, 2014. Emerging infectious diseases, 22(5), p.891.
 
[52]  Powers, Ann M. “Chikungunya.” Clinics in laboratory medicine30, no. 1 (2010): 209-219.
 
[53]  Staples, J. Erin, Robert F. Breiman, and Ann M. Powers. “Chikungunya fever: an epidemiological review of a re-emerging infectious disease.” Clinical Infectious Diseases 49, no. 6 (2009): 942-948.
 
[54]  Josseran, Loïc, Christophe Paquet, Abdelkrim Zehgnoun, Nadège Caillere, Alain Le Tertre, Jean-Louis Solet, and Martine Ledrans. “Chikungunya disease outbreak, Reunion Island.” Emerging infectious diseases 12, no. 12 (2006): 1994.
 
[55]  Ramful, Duksha, Magali Carbonnier, Marlene Pasquet, Brahim Bouhmani, Jamal Ghazouani, Tahir Noormahomed, Gilles Beullier et al. “Mother-to-child transmission of Chikungunya virus infection.” The Pediatric infectious disease journal 26, no. 9 (2007): 811-815.
 
[56]  Ravi, V. “Re-emergence of chikungunya virus in India.” Indian journal of medical microbiology 24, no. 2 (2006): 83.
 
[57]  Dandawate, C. N., K. V. Thiruvengadam, V. Kalyanasundaram, J. Rajagopal, and T. R. Rao. “Serological survey in Madras city with special reference to chikungunya.” The Indian journal of medical research 53, no. 8 (1965): 707-714.
 
[58]  Jadhav, M., M. Namboodripad, R. H. Carman, D. E. Carey, and R. M. Myers. “Chikungunya disease in infants and children in Vellore: a report of clinical and haematological features of virologically proved cases.” The Indian journal of medical research. 53, no. 8 (1965): 764.
 
[59]  Thiruvengadam, K. V., V. Kalyanasundaram, and J. Rajgopal. “Clinical and pathological studies on chikungunya fever in Madras city.” (1965).
 
[60]  Pialoux, Gilles, Bernard-Alex Gaüzère, Stéphane Jauréguiberry, and Michel Strobel. “Chikungunya, an epidemic arbovirosis.” The Lancet infectious diseases 7, no. 5 (2007): 319-327.
 
[61]  Dash, P. K., et al. “East Central South African genotype as the causative agent in reemergence of Chikungunya outbreak in India.” Vector-Borne and Zoonotic Diseases 7.4 (2007): 519-528.
 
[62]  Chahar, Harendra S., Preeti Bharaj, Lalit Dar, Randeep Guleria, Sushil K. Kabra, and Shobha Broor. “Co-infections with chikungunya virus and dengue virus in Delhi, India.” Emerging infectious diseases 15, no. 7 (2009): 1077.
 
[63]  Kukreti, Himani, Artee Chaudhary, R. S. Rautela, Ranjana Anand, Veena Mittal, Mala Chhabra, D. Bhattacharya, Shiv Lal, and Arvind Rai. “Emergence of an independent lineage of dengue virus type 1 (DENV-1) and its co-circulation with predominant DENV-3 during the 2006 dengue fever outbreak in Delhi.” International journal of infectious diseases 12, no. 5 (2008): 542-549.
 
[64]  NVBDCP http://www.nvbdcp.gov.in/Chikun-main.html.
 
[65]  Hasebe, F., M. C. Parquet, B. D. Pandey, E. G. M. Mathenge, K. Morita, V. Balasubramaniam, Z. Saat et al. “Combined detection and genotyping of Chikungunya virus by a specific reverse transcription-polymerase chain reaction.” Journal of medical virology 67, no. 3 (2002): 370-374.
 
[66]  Santhosh, S. R., et al. “Comparative full genome analysis revealed E1: A226V shift in 2007 Indian Chikungunya virus isolates.” Virus Research 135.1 (2008): 36-41.
 
[67]  Edwards, Carolyn J., et al. “Molecular diagnosis and analysis of Chikungunya virus.” Journal of clinical virology 39.4 (2007): 271-275.
 
[68]  Santhosh, S. R., P. K. Dash, M. M. Parida, M. Khan, M. Tiwari, and P. V. Lakshmana Rao. “Comparative full genome analysis revealed E1: A226V shift in 2007 Indian Chikungunya virus isolates.” Virus research 135, no. 1 (2008): 36-41.
 
[69]  Sambrook, Joseph, Edward F. Fritsch, and Tom Maniatis. Molecular cloning: a laboratory manual. No. Ed. 2. Cold spring harbor laboratory press, 1989.
 
[70]  Ray, Pratima, Vinod H. Ratagiri, Sushil K. Kabra, Rakesh Lodha, Sumit Sharma, B. S. Sharma, Mani Kalaivani, and Naveet Wig. “Chikungunya infection in India: results of a prospective hospital based multi-centric study.”PloS one 7, no. 2 (2012): e30025.
 
[71]  Suryawanshi, S. D., A. H. Dube, R. K. Khadse, S. V. Jalgaonkar, P. S. Sathe, S. D. Zawar, and M. P. Holay. “Clinical profile of chikungunya fever in patients in a tertiary care centre in Maharashtra, India.” (2009).
 
[72]  Kaur, Prabhdeep, Manickam Ponniah, Manoj V. Murhekar, Vidya Ramachandran, Ramakrishnan Ramachandran, Hari Kishan Raju, Vanamail Perumal, Akhilesh C. Mishra, and Mohan D. Gupte. “Chikungunya outbreak, south India, 2006.” Emerging infectious diseases 14, no. 10 (2008): 1623-1625.
 
[73]  Yergolkar, Prasanna N., Babasaheb V. Tandale, Vidya A. Arankalle, Padmakar S. Sathe, Sudeep AB, Swati S. Gandhe, Mangesh D. Gokhle, George P. Jacob, Supriya L. Hundekar, and Akhilesh C. Mishra. “Chikungunya outbreaks caused by African genotype, India.” Emerging infectious diseases 12, no. 10 (2006): 1580.
 
[74]  Chopra, Arvind, and Anuradha Venugopalan. “Persistent rheumatic musculoskeletal pain and disorders at one year post-chikungunya epidemic in south Maharashtra—a rural community based observational study with special focus on naïve persistent rheumatic musculoskeletal cases and selected cytokine expression.” Indian Journal of Rheumatology 6, no. 1 (2011): 5-11.
 
[75]  Selvavinayagam, T. S. “Chikungunya fever outbreak in Vellore, south India.”Indian Journal of community medicine 32, no. 4 (2007): 286.
 
[76]  Shrinet, Jatin, Shanu Jain, Anil Sharma, Shashi Shekhar Staikowsky Staikowsky, Kalika Mathur, Vandita Rana, Raj K. Bhatnagar et al. “Genetic characterization of Chikungunya virus from New Delhi reveal emergence of a new molecular signature in Indian isolates.” Virol J 9 (2012): 100.
 
[77]  Win, M. K., et al. “Chikungunya fever in Singapore: acute clinical and laboratory features, and factors associated with persistent arthralgia.” Journal of Clinical Virology 49.2 (2010): 111-114.
 
[78]  Panning, Marcus, Klaus Grywna, Marjan Van Esbroeck, Petra Emmerich, and Christian Drosten. “Chikungunya fever in travelers returning to Europe from the Indian Ocean region, 2006.” Emerging infectious diseases 14, no. 3 (2008): 416.
 
[79]  CDC http://wwwnc.cdc.gov/eid/article/14/10/07-0569_article.
 
[80]  Lewthwaite, Penny, Ravi Vasanthapuram, Jane C. Osborne, Ashia Begum, Jenna LM Plank, M. Veera Shankar, Roger Hewson et al. “Chikungunya virus and central nervous system infections in children, India.” Emerging infectious diseases 15, no. 2 (2009): 329.
 
[81]  Soni, Manisha, Anil Kumar Singh, Shashi Sharma, Ankita Agarwal, Natarajan Gopalan, P. V. Rao, Manmohan Parida, and Paban Kumar Dash. “Molecular and Virological Investigation of a Focal Chikungunya Outbreak in Northern India.” The Scientific World Journal 2013 (2013).
 
[82]  Singh, Priyanka, Veena Mittal, Moshahid A. Rizvi, Dipesh Bhattacharya, Mala Chhabra, Devendra S. Rawat, Rattan L. Ichhpujani, Lakhvir S. Chauhan, and Arvind Rai. “Northward movement of East Central South African genotype of Chikungunya virus causing an epidemic between 2006-2010 in India.” The Journal of Infection in Developing Countries 6, no. 07 (2012): 563-571.
 
[83]  Lambrechts, Louis, Thomas W. Scott, and Duane J. Gubler. “Consequences of the expanding global distribution of Aedes albopictus for dengue virus transmission.” PLoS neglected tropical diseases 4, no. 5 (2010): e646.
 
[84]  Hawman, David W., Kristina A. Stoermer, Stephanie A. Montgomery, Pankaj Pal, Lauren Oko, Michael S. Diamond, and Thomas E. Morrison. “Chronic joint disease caused by persistent Chikungunya virus infection is controlled by the adaptive immune response.” Journal of virology 87, no. 24 (2013): 13878-13888.
 
[85]  Labadie, Karine, Thibaut Larcher, Christophe Joubert, Abdelkrim Mannioui, Benoit Delache, Patricia Brochard, Lydie Guigand et al. “Chikungunya disease in nonhuman primates involves long-term viral persistence in macrophages.”The Journal of clinical investigation 120, no. 3 (2010): 894-906.
 
[86]  Staikowsky, Frederik, François Talarmin, Philippe Grivard, Abdel Souab, Isabelle Schuffenecker, Karin Le Roux, Marc Lecuit, and Alain Michault. “Prospective study of Chikungunya virus acute infection in the Island of La Réunion during the 2005-2006 outbreak.” PLoS One 4, no. 10 (2009): e7603.
 
[87]  Bouquillard, E., Fianu, A., Bangil, M., Charlette, N., Ribéra, A., Michault, A., Favier, F., Simon, F. and Flipo, R.M., 2018. Rheumatic manifestations associated with Chikungunya virus infection: A study of 307 patients with 32-month follow-up (RHUMATOCHIK study). Joint Bone Spine, 85(2), pp.207-210.
 
[88]  Bonifay, T., Lienne, J.F., Bagoée, C., Santa, F., Vesin, G., Walter, G., Nacher, M., Vaserman, N., Djossou, F. and Epelboin, L., 2018. Prevalence and risk factors of post chikungunya rheumatic musculoskeletal disorders: a prospective follow-up study in French Guiana. European Journal of Clinical Microbiology & Infectious Diseases, pp.1-6.
 
[89]  Rodriguez-Morales, A.J., Restrepo-Posada, V.M., Acevedo-Escalante, N., Rodríguez-Muñoz, E.D., Valencia-Marín, M., Castrillón-Spitia, J.D., Londoño, J.J., Bedoya-Rendón, H.D., de Jesús Cárdenas-Pérez, J., Cardona-Ospina, J.A. and Lagos-Grisales, G.J., 2017. Impaired quality of life after chikungunya virus infection: a 12-month follow-up study of its chronic inflammatory rheumatism in La Virginia, Risaralda, Colombia. Rheumatology international, 37(10), pp.1757-1758.
 
[90]  Rodríguez-Morales, A.J., Calvache-Benavides, C.E., Giraldo-Gómez, J., Hurtado-Hurtado, N., Yepes-Echeverri, M.C., García-Loaiza, C.J., Patiño-Barbosa, A.M., Sabogal-Roman, J.A., Patiño-Valencia, S., Hidalgo-Zambrano, D.M. and Vásquez-Serna, H., 2016. Post-chikungunya chronic arthralgia: results from a retrospective follow-up study of 131 cases in Tolima, Colombia. Travel medicine and infectious disease, 14(1), pp.58-59.
 
[91]  Feldstein, L.R., Rowhani-Rahbar, A., Staples, J.E., Weaver, M.R., Halloran, M.E. and Ellis, E.M., 2017. Persistent arthralgia associated with chikungunya virus outbreak, US Virgin Islands, December 2014-February 2016. Emerging infectious diseases, 23(4), p.673.
 
[92]  Chow, Angela, Zhisheng Her, Edward KS Ong, Jin-miao Chen, Frederico Dimatatac, Dyan JC Kwek, Timothy Barkham et al. “Persistent arthralgia induced by Chikungunya virus infection is associated with interleukin-6 and granulocyte macrophage colony-stimulating factor.” Journal of Infectious Diseases 203, no. 2 (2011): 149-157.
 
[93]  Larrieu, Sophie, Nicolas Pouderoux, Thierry Pistone, Laurent Filleul, Marie-Catherine Receveur, Daouda Sissoko, Khaled Ezzedine, and Denis Malvy. “Factors associated with persistence of arthralgia among Chikungunya virus-infected travellers: report of 42 French cases.” Journal of Clinical Virology 47, no. 1 (2010): 85-88.
 
[94]  Borgherini, Gianandrea, Patrice Poubeau, Annie Jossaume, Arnaud Gouix, Liliane Cotte, Alain Michault, Claude Arvin-Berod, and Fabrice Paganin. “Persistent arthralgia associated with chikungunya virus: a study of 88 adult patients on reunion island.” Clinical Infectious Diseases 47, no. 4 (2008): 469-475.
 
[95]  Simon, Fabrice, Philippe Parola, Marc Grandadam, Sabrina Fourcade, Manuela Oliver, Philippe Brouqui, Pierre Hance et al. “Chikungunya infection: an emerging rheumatism among travelers returned from Indian Ocean islands. Report of 47 cases.” Medicine 86, no. 3 (2007): 123-137.
 
[96]  Brighton, S. W., O. W. Prozesky, and A. L. De La Harpe. “Chikungunya virus infection.” A retrospective study of 107 (1983): 313-315.
 
[97]  Ramachandran, V., P. Kaur, K. Kanagasabai, S. Vadivoo, and M. V. Murhekar. “Persistent arthralgia among Chikungunya patients and associated risk factors in Chennai, South India.” Journal of postgraduate medicine 60, no. 1 (2014): 3.
 
[98]  Vijayakumar, Krishna Pillai, Thekkumkara Surendran Nair Anish, Biju George, Tony Lawrence, Sujina C. Muthukkutty, and Reshmi Ramachandran. “Clinical profile of chikungunya patients during the epidemic of 2007 in Kerala, India.”Journal of global infectious diseases 3, no. 3 (2011): 221.
 
[99]  Mohan, Alladi, D. H. N. Kiran, I. Chiranjeevi Manohar, and D. Prabath Kumar. “Epidemiology, clinical manifestations, and diagnosis of Chikungunya fever: lessons learned from the re-emerging epidemic.” Indian journal of dermatology55, no. 1 (2010): 54.
 
[100]  Ganu, Mohini A., and A. S. Ganu. “Post-chikungunya chronic arthritis—our experience with DMARDs over two year follow up.” J Assoc Physicians India 59 (2011): 83-6.
 
[101]  Dupuis-Maguiraga, Laurence, Marion Noret, Sonia Brun, Roger Le Grand, Gabriel Gras, and Pierre Roques. “Chikungunya disease: infection-associated markers from the acute to the chronic phase of arbovirus-induced arthralgia.”PLoS neglected tropical diseases 6, no. 3 (2012): e1446.
 
[102]  de Andrade, Daniel C., Sylvain Jean, Pierre Clavelou, Radhouane Dallel, and Didier Bouhassira. “Chronic pain associated with the Chikungunya Fever: long lasting burden of an acute illness.” BMC infectious diseases 10, no. 1 (2010): 31.
 
[103]  Parola, Philippe, Xavier De Lamballerie, Jacques Jourdan, Clarisse Rovery, Véronique Vaillant, Philippe Minodier, Philippe Brouqui, Antoine Flahault, Didier Raoult, and Rémi N. Charrel. “Novel chikungunya virus variant in travelers returning from Indian Ocean islands.” Emerging infectious diseases. 12, no. 10 (2006): 1493.
 
[104]  Parida, M. M., S. R. Santhosh, P. K. Dash, N. K. Tripathi, V. Lakshmi, N. Mamidi, A. Shrivastva et al. “Rapid and real-time detection of Chikungunya virus by reverse transcription loop-mediated isothermal amplification assay.” Journal of clinical microbiology. 45, no. 2 (2007): 351-357.
 
[105]  Carletti, Fabrizio, Licia Bordi, Roberta Chiappini, Giuseppe Ippolito, Maria R. Sciarrone, Maria R. Capobianchi, Antonino Di Caro, and Concetta Castilletti. “Rapid detection and quantification of Chikungunya virus by a one-step reverse transcription-polymerase chain reaction real-time assay.” The American journal of tropical medicine and hygiene 77, no. 3 (2007): 521-524.
 
[106]  Laurent, Philippe, Karin Le Roux, Philippe Grivard, Gérard Bertil, Florence Naze, Miguel Picard, Frédérik Staikowsky, Georges Barau, Isabelle Schuffenecker, and Alain Michault. “Development of a sensitive real-time reverse transcriptase PCR assay with an internal control to detect and quantify chikungunya virus.” Clinical chemistry. 53, no. 8 (2007): 1408-1414.
 
[107]  Dhanwani, Rekha, Mohsin Khan, Vinay Lomash, Putcha Venkata Lakshmana Rao, Hinh Ly, and Manmohan Parida. “Characterization of Chikungunya Virus Induced Host Response in a Mouse Model of Viral Myositis.” PloS one. 9, no. 3 (2014): e92813.
 
[108]  Inamadar, Arun C., Aparna Palit, V. V. Sampagavi, S. Raghunath, and N. S. Deshmukh. “Cutaneous manifestations of chikungunya fever: observations made during a recent outbreak in south India.” International journal of dermatology47, no. 2 (2008): 154-159.