www.jogh.org • *Contributed equallytothiswork. 5 4 3 2 1 Sandip Banerjee Abhishek Pandey from theinitialvaccinerollout vaccination inIndia:Lessons Challenges facingCOVID-19 J © 2021THEAUTHOR(S) The onlineversionofthisarticlecontainssupplementarymaterial. Electronic material: supplementary National SchoolofTropical , BaylorCollegeofMedicine,Houston, Texas,USA Department ofMathematics,IndianInstituteTechnologyRoorkee,Uttarakhand, India Indian CouncilofMedicalResearch,NewDelhi,India Agent-Based ModellingLaboratory,YorkUniversity,Toronto,Ontario,Canada Center forInfectiousDiseaseModelingandAnalysis(CIDMA),YaleSchool ofPublicHealth,NewHaven,Connecticut,USA o GH ©2021IS equitable distributionofvaccines. tancy andmisinformation, andensuringan VID-19 vaccines,overcoming vaccinehesi healthcare professionalsto administerCO panding healthcare capacity, staffing more will dependonboostingvaccinesupply,ex India’s abilitytoacceleratevaccinerollout overcoming theCOVID-19pandemiccrisis. Accelerating vaccinationinIndiaiskeyto o GH doi: 10.7189/jogh.11.03083 and thecountryisnowfacingshortagesduetoaninadequate scale-upofvaccineproductionsofar. Herewe oritized 30millionhealthcareandfrontlineworkers.Vaccine rollouthoweverhasbeenslowerthanexpected an ultimatetarget ofvaccinating300millionpeoplebyAugust2021[ (ICMR) and the National Institute of Virology The vaccination drive in India started on January 16, 2021 with traZeneca andCovaxindevelopedbyBharatBiotechincollaborationwithIndianCouncilforMedicalResearch authorized theemergency useoftwovaccines,eachrequiringdoses–CovishielddevelopedbyOxford/As variant thatmaybemoretransmissible[ 400 W 000 reportedcasesinasingledayatthepeak.Theresurgence coincideswiththeemergence oftheDelta 4 , PeterJHotez 1 *, PrathaSah ber 2020, India is now battling a devastating second wave, reaching a global record of more than ber 2020,Indiaisnowbattlingadevastatingsecondwave,reachingglobalrecordofmorethan tries worsthitbytheCOVID-19pandemic.AftermonthsofsteadydeclineincasessinceSeptem ith morethan28millionreportedcasesasofJune5,2021,Indiacontinuestobeonethecoun

5 1 , AlisonPGalvani *, SeyedMMoghadas - - - 1 80% inAndhra PradeshandWestBengalto lessthan40%inNa ( tion phase.Wefoundstarkdifferences invaccinerolloutacrossstates ing atleastthefirstdoseofvaccine bytheendoffirstvaccina individuals registered for vaccination and using data of those receiv vaccine uptakeforeachstateby estimatingthepercentageofeligible marily responsibleforvaccinedistribution.Wecalculatedthe rateof management inIndiaisdecentralized,thestategovernments arepri dose, translatingtoanuptakerateof8%nationally.As public health first dose.Only2.46millionpeoplereceivedthesecond vaccine million registeredforvaccinationand11.1received their Out ofthe30millionindividualsprioritizedforfirstphase, 18 state-level vaccination data during the initial stage of vaccine rollout. discuss thechallengesfacingCOVID-19vaccinationinIndia using ]. In an attempt to control the COVID-19 , India initially ]. InanattempttocontroltheCOVID-19pandemic,Indiainitially Figure 1 1

) . Registrationofeligibleindividuals rangedfromover 1 2 , SandipMandal from theinitialvaccinerollout.JGlobHealth2021;11:03083. Galvani AP. Challenges facing COVID-19 vaccination in India: Lessons Cite as: 2 ]. Thefirstphaseofvaccineroll-outpri Pandey A, Sah P, Moghadas SM, Mandal S, Banerjee S, Hotez PJ, 3 ,

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VIEWPOINTS VIEWPOINTS 2021 •Vol. 11 • 03083 cases inthestateonFebruary27,2021. vaccination byFebruary28,2021.Pointsizeisproportionaltothe numberofactiveCOVID-19 (horizontal dashedline)and58.06%registered(vertical ofthoseeligibleforPhaseI tered andvaccinatedacrossstates.Dashedlinesindicatenationalaverages –35.44%vaccinated that thenationaltotaladdeduptotarget of30million.( ber ofhealthcareandfrontlineworkers[3-5],normalizingthetotaleligibleacrossstatesso 1, 2021.Wecalculatedthestate-levelnumberofeligibleindividualsbyusingdataonnum chose February28,2021astheendtimepointbecausePhaseIIvaccinationsstartedonMarch for vaccinationand( 1. Figure Fig1c A C Phase 1vaccinerolloutinIndia.Percentageofeligibleindividualsthat( Percentage registered technical glitches in the online registration platform. in India was fuelled by concerns about technical glitches in the online registration platform. Vaccine hesitancy in India was fuelled byconcerns about vaccination campaign,likelybecause ofvaccinehesitancy,misinformationpropagatedby socialmedia,and India grappledwithlowrates ofbothregistrationandvaccineadministrationduringthe initialstagesofthe achieve vaccinationcoverageof 28%. 64%; whereaswithlessthan1 vaccinationclinicper1000eligibleindividuals,Maharashtra wasonlyableto Gujarat withmorethan3vaccination clinicsper1000eligibleindividualsachievedavaccination coverageof vaccination coveragebytheendofinitialphase ( states thathadahighernumberofvaccinationclinicsper1000 eligibleindividualswereabletoachievehigher those eligible.Vaccinationuptakewaspositivelycorrelated with vaccinedeliveryinfrastructuresuchthatthe Pradesh andBiharwithlessthan20eligibleindividualsper 1000population,vaccinatedmorethan40%of than 75eligibleindividualsper1000population,butvaccinated lessthan20%ofthoseeligible,whereasUttar ure 2 B ) received at least the first dose of vaccine by February 28, 2021. We ) receivedatleastthefirstdoseofvaccinebyFebruary28,2021.We , PanelA,

P

< 0.010). NortheasternstatesofNagaland,MizoramandManipur, forinstance, hadmore B C ) Comparisonofpercentageregis Percentage vaccinated 2

A ) registered ) registered Figure 2 - - 1 these highburdenstates tional average of 35% in each of initial phasewaslessthanthena vaccination coverageduringthe February. ExceptforKarnataka, active casesinIndiabytheendof counted formorethan80%ofall nataka, Punjab and Tamil Nadu ac states of Maharashtra, Kerala, Kar registered han vaccinatedover80%ofthose jarat, Madhya Pradesh and Rajast Manipur. Incontrast,statesofGu Tamil Nadu, Mizoram, Goa, and in the states of Nagaland, Punjab, igible individuals were vaccinated the firstdose.Lessthan20%ofel at leasthalfofthoseeligiblewith tarakhand) wereabletovaccinate Rajasthan, Chhattisgarh andUt ary 2021, only four states (Gujarat, Tamil Nadu. By the end of Febru galand, Punjab,Goa,Mizoramand ble for vaccinations per capita ( higher numberofindividualseligi tion coveragewasassociatedwitha [ the governments’websiteCoWin cination datawasobtainedfrom viduals nationally.State-levelvac to match 30millioneligibleindi on staff[ ers [ on thenumberofhealthcarework nation phaseusingstate-leveldata viduals eligiblefortheinitialvacci infrastructure. Weestimatedindi population andvaccinedelivery of eligibleindividualsper1000 states withrespecttothenumber between vaccinationeffortsacross dia, weexaminedtheassociation ities invaccinedistributionIn To understand the heterogene 6 , , PanelB, PanelC www.jogh.org • ]. Wefoundthatlowervaccina 3 ], policestrength[ 5 ] and normalized the data ] andnormalizedthedata ( ) P Figure 1 . 0.010). For example, example, For <0.010). doi: 10.7189/jogh.11.03083 , PanelC 4 ] andpris ( Figure ) . The . The Fig ------www.jogh.org • of activeCOVID-19casesinthestateonFebruary27,2021. Pointsizeisproportionaltothenumber represents the95%confidenceinterval. per eligibleindividual.Thesolidlineistheregressionandshadedarea (A) numberofeligibleindividualspercapitaand(B)vaccinationsites 2. Figure 2 Figure Fig2b Speed of initial vaccine rollout varied Speed ofinitialvaccinerolloutvaried larger targetedpopulation. vaccine deliveryinfrastructure and/or er vaccination coverage had weaker widely acrossstates.States withlow Percentage vaccinated Percentage vaccinated 20 40 60 80 20 40 60 80 0 0 Maharashtra Madhya Pradesh Odisha Rajasthan B A Bihar Association between percentage vaccinated with at least one dose and Association betweenpercentagevaccinatedwithatleastonedoseand Punjab West Bengal Jharkhand Telangana Nagaland Assam West Bengal Jharkhand Tamil Nadu doi: 10.7189/jogh.11.03083 Sikkim Chhattisgarh Gujarat Manipur Tamil Nadu Haryana years ofageonMay1stwouldinevitablyrequireexpansion ofvaccinesupplyandvaccinationcenterstoac for vaccineproductionbytheUnitedStates.Extensionofeligibility criteriatoincludeallindividualsabove18 up productionduetofinancialconstraintsaswell embargo ontheexportofrawmaterialsneeded mestic use,thescaleofproductionhasbeeninadequate.Indian vaccinemanufacturershavestruggledtoramp vaccine developmentandmanufacturinghubprovidingthecountry anedgeforprocurementofvaccinesdo variants underscorestheurgency toacceleratethevaccinerollout.AlthoughIndiahasemerged asaCOVID-19 continue vaccination.Theresurgence ofcases,coincidingwiththespreadhighlytransmissibleSARS-CoV-2 age ofessentialmedicalsuppliesandbattlingamulti-pronged wartocontainthesecondwaveaswell Uttarakhand Himachal Pradesh 25 1 Maharashtra Bihar Uttarakhand Kerala Andhra Pradesh Vaccination sites(per1000eligible individuals) Karnataka Eligible individuals(per1000population) Punjab Tripura Assam Goa Odisha Meghalaya Arunachal Pradesh Arunachal Chhattisgarh Madhya Pradesh Uttar Pradesh Kerala Meghalaya Uttar Pradesh Mizoram

2 50 Haryana Tripura Andhra Pradesh Himachal Pradesh Arunachal Pradesh Arunachal Goa Telangana - Rajasthan 3 Manipur Johnson, would facilitate efforts in rapidly expanding vaccine coverage. To Johnson, would facilitate efforts in rapidly expanding vaccine coverage. To manufacture single-dosevaccines, suchasthoseproducedbyJohnson& domestic andinternationalmanufacturers. Effortstoprocureand locally supplement their vaccine supplybyimporting doses directlyfromboth cal bridgingtrial.Thestategovernments andIndiancorporatescannow from elsewhere intheworld,India has removed the requirement of a lo To facilitatetheimportationofvaccineswithemergency useauthorization commodate thesubstantialincreaseinindividualstargeted forvaccination. 75 Sikkim Gujarat 3 Mizoram Karnataka

Nagaland 4 100 allowing public health officials to effectively track allowing publichealthofficialstoeffectivelytrack registration platformhavelargely beenresolved, some ofthechallenges.Initialglitchesinonline India improved in pace as the country addressed Despite theslowstart,vaccinationcampaignin care infrastructure. cal budgetaryconstraintsanddisparityinhealth of vaccinationacrossstateslikelyreflectingthelo Our results showed large differences in the pace population doesnothaveaccesstotheinternet. vaccination ratesasmorethanhalfoftheIndian for receivingvaccinesmayhavecontributedtolow ence. Moreover, therequirementtoregisteronline watch approach,contributingtovaccineindiffer may haveencouragedpeopletoadoptawaitand The steadydeclineincasesformonthsIndia cine sentiments[ cerns, togetherwithrisinganti-COVID-19vac ropean andAfricancountriesduetosafetycon Ensuing suspensionofCovishieldinmultipleEu the completionofPhaseIIIclinicaltrial[ of theCovaxinvaccinethatwasapprovedbefore vaccine safetyandskepticismabouttheefficacy infrastructure. Thecountryisnowfacingashort analready strainedhealthcare has overwhelmed The devastatingsecondCOVID-19waveinIndia celerate vaccinationrollout. private sector[ in Indiaareprovidedbythe of healthcareservices vaccinate individuals.Giventhatmorethan80% clinics, statesarenowutilizingprivatehospitalsto which vaccineswereavailableonlyatgovernment Unlike the initial stageof the campaign,during tions [ cine efficacyof81%against symptomatic infec Covaxin clinicaltrialshavedemonstratedavac without pre-registration.Interimresultsforthe uals aged45ormorecannowreceivevaccines Along withonlineregistrations,eligibleindivid and planlogisticsforthevaccinationcampaign. 9 ] alleviatingconcernsaboutitsefficacy. 10 ], privatehospitalscangreatlyac 8 ] mayhaveelevateddistrust. 2021 •Vol. 11 • 03083 7 ]. ]. ------

VIEWPOINTS VIEWPOINTS 2021 •Vol. 11 • 03083 Photo: From thecollectionofAshishJain,usedwithpermission. REFERENCES

4  3  2  1  7  6  5  userfiles/file/201607121235174125303FinalDATABOOKSMALL2015.pdf Bureau ofPoliceResearch&Development. DataonPoliceOrganisations, 2016.Available: force_India.pdf Anand S,FanV. TheHealthWorkforceinIndia,WHO;2016.Available: virus-india-vaccine-idUSKBN2AG1IZ Reuters. Indiatomultiplyvaccinationsamidcoverageconcerns.Available: epidemiological-update-on-covid-19—27-april-2021 Weekly epidemiologicalupdateonCOVID-19-27April2021.Available: 2021;372:n196. Thiagarajan K. Covid-19: India is at centre of global vaccine manufacturing, but opacity threatens public trust. BMJ. Government ofIndia.CoWinDashboard. Available: fault/files/PSI-2018.pdf National CrimeRecordsBureauMinistry ofHomeAffairs.PrisonStatisticsIndia,2019.Available: the correspondingauthor)anddeclarenoconflictsofinterest. Competing interests: analysis. AP, PS and APGwrote the first draftof the manuscript. Allauthorsedited the manuscriptfor final submission. vided theirinsightsregardingtheevolvingpandemicsituationinIndia.Allauthorscontributedtointerpretationofdata Authorship contributions: Research [OV4–170643,COVID-19RapidResearch]. and the Notsew Orm Sands Foundation. SMM, SM, and SB acknowledge support from the Canadian Institutes of Health Science FoundationgrantRAPID-2027755,CentersforInfectiousDiseaseControlandPreventionU01IP001136 Funding: table distributionofvaccines. to administerCOVID-19vaccines,overcomingvaccinehesitancyandmisinformation,ensuringanequi depend onboostingvaccinesupply,expandinghealthcarecapacity,staffingmoreprofessionals India’sabilitytoachieveitsobjectivesofvaccinationcampaignswill reached byAugust2021.Goingforward, by earlyOctober2021.Ifthevaccinationrateisincreasedto3.37milliondosesperday,goalcouldbe lion doseswereadministered.Atthisrate,thegoalofvaccinating300millionpeoplecouldonlybeachieved

APG acknowledges funding from NSF Expeditions grant 1918784, NIH grant 1R01AI151176-01, National APGacknowledgesfundingfromNSFExpeditionsgrant1918784,NIH1R01AI151176-01,National . Accessed:22April2021.

Medline:33509837 . Accessed:20March2021. The authors completed the ICMJE Unified Competing Interest form (available upon request from The authors completed the ICMJE Unified Competing Interest form (available upon request from APandPSconductedliteraturereviewperformeddataanalysis.SMM,SBPJHpro

doi:10.1136/bmj.n196 . Accessed:27April2021. production of Covishield. The United States has also decided to provide production ofCovishield.TheUnitedStateshasalsodecidedtoprovide the United States has agreed to supply raw materials critical for scaling up of Indiaismakingadvancepaymentstothelocalmanufacturers.Moreover, alleviate thefinancialstrainandboostdomesticcapacity,Government nation rateof325 doses perday,whichisover6timeshigherthantheaveragedailyvacci vaccine rolloutended,correspondingtoanationalaverageof2.2million a totalof118.45milliondoseshavebeenadministeredsincetheinitial exacerbation ofCOVID-19outbreakinthecountry.AsApril22,2021, August 2021, while challenging, is both feasible and essential to avert an Achieving theambitioustarget ofvaccinating300millionindividualsby the transmissioneffectivelyandsavemillionsoflives. certed internationaleffortisthereforeimperativetoassistIndiacurtail slow paceofthevaccinationdrivesinmanylow-incomecountries.Acon halt ofCOVID-19vaccineexportsfromIndiahasimpactedthealready escape variantstoarise,whichcouldprolongthepandemic.Moreover, the Elevated communitytransmissionprovidesmoreopportunitiesforvaccine scores thevulnerabilityofcountrieswithweakhealthcareinfrastructure. in Indiacouldthreatentheprogressmadeothercountriesandunder The ongoing humanitarian crisis posed bythe second wave of COVID-19 the vaccinationdriveinIndia. tries, includingIndia[ up to60millionvaccinedosesoftheAstraZenecaothercoun https://www.cowin.gov.in/ . Accessed:5May2021. 4

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