Outbreak of 2009 Pandemic Influenza A (H1N1) Virus on a University Campus – Delaware, April-May 2009 A. Danielle Iuliano, PhD MPH Division of HIV/AIDS

Outbreak of 2009 Pandemic Influenza A

(H1N1) Virus on a University Campus –

Delaware, April-May 2009

A. Danielle Iuliano, PhD MPHDivision of HIV/AIDS Prevention

May 27, 2010

Outline

• Background• Description of the Outbreak• Epi-Aid objectives• Studies• Conclusions• Recommendations

Influenza• RNA virus

– Common types A and B– Affects 5-20% of the U.S. population– 200,000 hospitalizations– 36,000 deaths

• Virus spread: person-to-person via respiratory droplet

• Prevention– Seasonal influenza vaccine– Post-exposure prophylaxis– Non-pharmaceutical interventions

Spectrum of Influenza Illness

• Several case definitions for surveillance • Duration of Illness

– 4 – 7 days– Some symptoms may linger

• Symptoms– Fever (≥ 100º F)– Feverish (chills/sweats)– Sore throat– Runny nose/nasal

congestion– Cough– Shortness of breath– Abdominal Pain

• – Diarrhea– Nausea/vomiting– Headache– Muscle/joint aches– Ear pain/pressure– Fatigue

2009 Pandemic Influenza A (H1N1)

• Swine-origin influenza virus• April 15, 2009

– First identified human infection

H1N1 Diagnosis• Reverse transcriptase polymerase

chain reaction (RT-PCR)– Used to subtype influenza viruses– H1N1 initially unsubtypeable at state

labs – Early samples sent to CDC for

confirmation

• Rapid influenza test– Can determine influenza type (A or

B)

H1N1 Treatment• Treatment

– Oseltamivir (Tamiflu®)– Zanamivir (Relenza®)

• Most effective within 48 hours of onset

University of Delaware (UD)

• Campus: Newark• University Population

– 18,872 students– 5,871 faculty/staff

• University health clinic– Located on campus– Open 24 hrs/day, 7

days/week

The Outbreak

April 27

University clinic saw rapid increase in student visits

4 samples sent to state for subtyping

The Outbreak

April 27 April 28

4 probable H1N1 cases identified

Campus wide H1N1 alert issued



The Outbreak

April 27 April 28 April 29

Overflow clinic opened

University cancels social/academic events

Epi-AID Requested





The Outbreak

April 27 April 28 April 29 April 30

4 H1N1 cases confirmed by CDC

Athletic events canceled thru weekend

CDC arrives

Overflow clinic opened

University cancels social/academic events

Epi-AID Requested





Headlines

At the time of this investigation

• H1N1 unknown characteristics– Severity of illness– Attack rate– Age distribution of illness– Effectiveness of seasonal influenza

vaccine– Risk factors for transmission– Use of community mitigation

measures

Epi-Aid Investigation Objectives

• Examine increase in clinic visits at the UD health clinic

• Describe the epidemiology of H1N1 in the university community

• Identify risk factors for transmission on campus

Studies Conducted• Review of health clinic visit data

• Clinical chart abstraction

• Online H1N1 survey

• Qualitative study: focus groups and individual case interviews

Health Clinic Data

Review of Health Clinic Data

• Objectives– Describe the number of respiratory

illness visits (ICD-9)

– Compare visits: 2008 and 2009

Respiratory Illness• Defined by diagnostic code (ICD-9):

– Upper and/or lower respiratory infection– Influenza– Otitis media– Respiratory failure – Respiratory distress– Asthma/chronic obstructive pulmonary

disease– Fever– Pneumonia– Pharyngitis– Laryngitis – Sore throat– Nasal congestion or rhinorrhea – Cough

Student Health Clinic Respiratory Visits,

March 22 – May 9, 2009

0

20

40

60

80

100

120

140

160

180

200

Date

Num

ber

of V

isit

s

April 29

Spring Break

UD Health Clinic Visits (2008 vs. 2009)

Number of VisitsApril 27 – May

3, 2008April 26 – May

2, 2009

All Visits 960 1,430

Overflow Clinic -- 300

Visits for Respiratory Illness

325 1,080

Rapid Influenza Tests -- 92

Oseltamivir distributed -- > 500

• Increase in respiratory illness visits:– More than four times the number of

respiratory visits compared with 2008.

Online H1N1 Survey

Online H1N1 Survey

• Objectives– Estimate attack rates

– Examine health seeking behaviors

– Measure risk factors for ILI

Survey Methods• Cross sectional survey • Conducted May 10 to May 18, 2009• Online survey: University emailed link

to entire university population • Included questions on:

– Illness and symptoms since March 27, 2009

– Health seeking behaviors– Risk factors for transmission– Community mitigation measures– Messages about H1N1

Analytic Methods• Demographic characteristics provided

by UD• Respiratory illness definitions

– Acute respiratory illness (ARI)• Reported fever, cough, sore throat or nasal congestion/rhinorrhea

• Between March 27 – May 9, 2009– Influenza-like illness (ILI)

• Fever plus cough or sore throat

Survey Response

StudentsN=18,872

n (%)

Faculty/StaffN=5,871

n (%)

Respondents 6049 (32%) 1401 (24%)

GenderMen

Women2050 (34%)3999 (66%)

518 (37%)883 (63%)

Age Median (IQR)21 (18-23)

Survey ResponseStudentsN=18,872

n (%)

Faculty/StaffN=5,871

n (%)

Respondents 6049 (32%) 1401 (24%)

GenderMen

Women2050 (34%)3999 (66%)

518 (37%)883 (63%)

Age20-2930-3940-4950-59> 60

Median (IQR)21 (18-23) 66 (5%)

232 (17%)334 (24%)488 (39%)281 (20%)

Attack Rates for ILI

StudentsN=6049

Faculty/Staff

N=1401

Acute respiratory illness (ARI)

1545 (26%) 194 (14%)

Influenza-like illness (ILI) 604 (10%) 73 ( 5%)


Risk Factor

TotalILI

N (%)RR

95% CI P-value

Age18-1920-2930-3940-4950-59> 60

16093941534479576311

168 (10)412 (11)

31 (6)19 (4)34 (6)12 (4)

referent1.0 (0.8-

1.2)0.6 (0.4-

0.8)0.4 (0.2-

0.6)0.5 (0.4-

0.8)0.3 (0.2-

0.6)

0.990.003

<0.0010.0020.002RR=Relative Risk, 95% CI=95% Confidence Interval


Risk Factor

TotalILI

N (%)RR

95% CI P-value

Age18-1920-2930-3940-4950-59> 60

16093941534479576311

168 (10)412 (11)

31 (6)19 (4)34 (6)12 (4)

referent1.0 (0.8-

1.2)0.6 (0.4-

0.8)0.4 (0.2-

0.6)0.5 (0.4-

0.8)0.3 (0.2-

0.6)

0.99

0.003<0.001

0.002

0.002

RR=Relative Risk, 95% CI=95% Confidence Interval


Risk Factor TotalILI

N (%)RR

95% CI P-value

Seasonal Influenza Vaccine

YesNo

19315196

173 (9)461 (9)

1.0 (0.8-1.2)

referent0.91RR=Relative Risk, 95% CI=95% Confidence Interval

ILI Characteristics and Healthcare

(N=677)n (%)

Median duration of illness (IQR) 6 (4-9)

Missed Work/Class 403 (60)

Median days missed (IQR) 2 (1-3)

Visited a healthcare provider 395 (58)

Stayed overnight in hospital 4 (<1)

Onset of Reported ILI, Students (n=604)

0

5

10

15

20

25

30

35

40

45

50

Campus wide alert issued

Overflow Clinic OpensPeak in reported

illness

Date

Cases

Student Risk Factors for ILI


Risk Factor

TotalILI

N (%)RR

95% CIP-

value

HousingOn CampusOff Campus

24103639

261 (11)343 (9)

1.2 (1.0-1.4)referent

0.08

Travel to MexicoYesNo

955954

22 (23)582 (10)

2.4 (1.6-3.4)referent

<0.001

‘Greek’ Society Member

YesNo

7705258

129 (17)475 (9)

2.0 (1.6-2.5)referent

<0.001

‘Greek Week’ Participation

YesNo

5895402

107 (18)491 (9)

2.2 (1.8-2.8)referent

<0.001

Student Risk Factors for ILI


Risk Factor

TotalILI

N (%)RR

95% CIP-

value


24103639

261 (11)343 (9)

1.2 (1.0-1.4)referent 0.08


955954

22 (23)582 (10)

2.4 (1.6-3.4)referent <0.001

‘Greek’ Society Member

YesNo

7705258

129 (17)475 (9)

2.0 (1.6-2.5)referent <0.001


YesNo

5895402

107 (18)491 (9)

2.2 (1.8-2.8)referent <0.001


0

5

10

15

20

25

30

35

40

45

50

3/27

3/29

3/31 4/

24/

44/

64/

84/

104/

124/

144/

164/

184/

204/

224/

244/

264/

284/

30 5/2

5/4

5/6

5/8

ILI - Other

ILI - Mexico Travelers

Peak in reported illness

Spring Break Travel to Mexico

Cases

Date


0

5

10

15

20

25

30

35

40

45

50

3/27

3/29

3/31 4/

24/

44/

64/

84/

104/

124/

144/

164/

184/

204/

224/

244/

264/

284/

30 5/2

5/4

5/6

5/8

ILI - Other

ILI - Mexico Travelers


Spring Break Travel to Mexico

Cases

Date

13 of 20 travelers became sick during trip or within 7 days of

returning

Student Risk Factors for ILIRisk Factor

Total

ILIN (%)

RR95% CI

P-value


24103639

261 (11)343 (9)

1.2 (1.0-1.4)referent 0.08


955954

22 (23)582 (10)

2.4 (1.6-3.4)referent <0.001

‘Greek’ Society MemberYesNo

7705258

129 (17)475 (9)

2.0 (1.6-2.5)referent <0.001


YesNo

5895402

107 (18)491 (9)

2.2 (1.8-2.8)referent <0.001



0

5

10

15

20

25

30

35

40

45

50

3/27

3/29

3/31 4/

24/

44/

64/

84/

104/

124/

144/

164/

184/

204/

224/

244/

264/

284/

30 5/2

5/4

5/6

5/8

Spring Break

‘Greek Week’


Cases

Date

ILI Rate by ‘Greek Week’ Participation

0

5

10

15

20

25

30

35'Greek-Week' Participants

non-Participants

‘Greek Week’

Rat

e p

er 1

000

peo

ple

per

day

Date

Limitations• H1N1 confirmatory testing for small subset

– Unknown how many positive for H1N1

• Low response rate to online survey

• Self-reported responses

• Generalizability– May not be representative of university

population– May be different than non-participants

Conclusions• Large outbreak of respiratory infections

on UD campus in April and May 2009

• Outbreak overwhelmed health system

• Attack rate: two times higher for students compared with faculty/staff

• No deaths were reported

Conclusions

• Risk of ILI decreased in older age groups

• No difference in the risk of ILI by seasonal influenza vaccine

• Risk factors for transmission– Travel to Mexico– ‘Greek Week’ participation

Investigation helped to answer

• H1N1 unknown characteristics– Severity of illness– Attack rate– Age distribution of illness– Effectiveness of seasonal influenza

vaccine– Risk factors for transmission– Use of community mitigation

measures

University of Delaware: AR: 10%

CFR: 0%

1918 pandemic AR: 30%

CFR: 2 %

1968 pandemicAR: 37%

CFR: 0.2 %

Population 18,872 18,872 18,872

ILI 1,887 5,662 6,882

Healthcare visits 1,132

Hospitalizations 11

Deaths 0 113 14

Severity of Illness, Delaware, 2009

AR: Attack Rate, CFR: Case Fatality Rate

Recommendations• Provide information to the university

community– Signs/symptoms– How virus spreads– Prevention methods– Who should seek care – When to seek care

• Distribute through multiple media sources

• Provide regular updates

Recommendations

• Prepare for surge in individuals seeking care– Developed in conjunction with local

health authorities– Plan for additional clinic location and

staff– Call center

• CDC guidance for universities– http://www.cdc.gov/h1n1flu/institutions/

guidance/

AcknowledgmentsUniversity of

Delaware– Sharon Bathon– Steve Grasson– Richard Sacher– Joseph Siebold– Sheryl Whitlock– Marcia Nichol

Delaware Health and Social Services– Paul Silverman– Paula Eggers– Leroy Hathcock– Ashley Love– Rick Hong– Karyl Rattay– Sue Shore– Crystal Webb

CDC– Dave Swerdlow– Carrie Reed– Alice Guh– Deborah Dee– Tarissa Mitchell– Greg Armstrong– Kathy Byrd– Mitesh Desai– Hannah Gould– Preeta Kutty– Roni Werman– Gavin Grant

– Mark Lamias– Lyn Finelli– Victor Babalban– Harvey Lipman– Mehran

Massoudi– Dan Fishbein– Micah Milton– Carolyn Bridges– Michael Lynch– Mark Sotir– Joan Brunkard– Phil Ricks

Thank you!

Extra Slides

University Challenges

• Health system overwhelmed– Unexpected and rapid increase in

visits

• Decision to cancel or not cancel classes– Students may leave campus– Community spread of the virus– Classes not canceled

H1N1 Case Definitions

• Probable case:– Positive influenza A, but

unsubtypeable on RT-PCR at state laboratories

• Confirmed case:– Positive for H1N1 on RT-PCR at CDC

Clinic Visit Data

Student Health Service Visits, March 27 – May 9 2008 & 2009

0

50

100

150

200

250

300

350

400

3/27

3/29

3/31 4/

24/

44/

64/

84/

104/

124/

144/

164/

184/

204/

224/

244/

264/

284/

30 5/2

5/4

5/6

5/8

Date

Fre

qu

en

cy

of

Clin

ic V

isit

s

2008 2009

Student Health Services Visits For Respiratory Illness, 2008-2009

0

20

40

60

80

100

120

140

160

180

200

3/27

3/29

3/31 4/

24/

44/

64/

84/

104/

124/

144/

164/

184/

204/

224/

244/

264/

284/

30 5/2

5/4

5/6

5/8

Date

Nu

mb

er

of

Vis

its

fo

r R

es

pir

ato

ry Il

lne

ss

2008 2009

Onset of Illness, Confirmed Cases (n=24)

0

1

2

3

4

5

6

7

8

9

10

3/3

03/3

14/1

4/2

4/3

4/4

4/5

4/6

4/7

4/8

4/9

4/1

04/1

14/1

24/1

34/1

44/1

54/1

64/1

74/1

84/1

94/2

04/2

14/2

24/2

34/2

44/2

54/2

64/2

74/2

84/2

94/3

0

Onset Date

Num

ber

of Confirm

ed C

ase

s

Chart Abstraction

Clinical Chart Abstraction

Clinical Chart Abstraction

• Objectives– Describe the spectrum of illness in

students seeking medical care• Who were the students presenting? • Were they worried ill or worried well?• Did they likely have H1N1?

– Examine severity of H1N1 – Compare confirmed H1N1 cases to

• Afebrile respiratory illness (Non ILI)• Seasonal influenza A

Clinical Chart Abstraction • Reviewed electronic medical charts• From April 5 – May 8, 2009:

– All confirmed Influenza A (H1N1)– Random sample of other respiratory

illness • Afebrile (25% sample abstracted)• Febrile (50% sample abstracted)

– Influenza-like illness (ILI)

• From February – March, 2009– Seasonal influenza A

Fever

+ cough or sore throat

Flow Chart for Selection of Charts

Student Health Clinic

With Fever n = 492

Without Fever n = 610

241 abstracted 132 abstracted

*Data for 6 patients from external sources (CCHS, State DPH interviews)

4/5/2009–5/8/2009 Respiratory Illness

n = 1102

2/1/2009–3/21/2009

Seasonal Influenza A n = 44

ILI: n = 237 Confirmed H1N1: n = 24*

Confirmed H1N1 vs. ILI

Clinical Characteristics and Outcome

ConfirmedN=24 (%)

ILIN=213 (%) P-

value

Symptoms Cough Sore throat Nasal congestion / rhinorrhea Gastrointestinal symptoms nausea, vomiting, diarrhea Myalgia Headache Fatigue

24 (100)15 (63)19 (79)

8 (33)14 (58)15 (63)12 (50)

158 (74)174 (82)142 (67)

36 (17)98 (46)90 (42)91 (43)

0.0020.030.21

0.050.250.060.50

Underlying Medical Conditions Asthma 1 (4) 32 (15) 0.22*

Hospitalizations / Deaths 0 (0) 0 (0) -* Fisher’s Exact Test

Confirmed H1N1 vs. Afebrile Illness


ConfirmedN=24 (%)

Afebrile N=136

(%)P-

value

Symptoms Cough Sore throat Nasal congestion / rhinorrhea Gastrointestinal symptoms nausea, vomiting, diarrhea Myalgia Headache Fatigue

24 (100)15 (63)19 (79)

8 (33)14 (58)15 (63)12 (50)

83 (61)103 (76)89 (65)

7 (5)18 (13)39 (29)21 (15)

<0.001

0.170.19

<0.001

<0.001

0.001<0.00

1

Underlying Medical Conditions Asthma 1 (4) 25 (18) 0.13*

Hospitalizations / Deaths 0 (0) 0 (0) -

* Fisher’s Exact Test


ConfirmedN=24 (%)

SeasonalN=44 (%)

P-value

Symptoms Fever Cough Sore throat Nasal congestion / rhinorrhea Gastrointestinal symptoms nausea, vomiting, diarrhea Myalgia Headache Fatigue

24 (100)24 (100)15 (63)19 (79)

8 (33)14 (58)15 (63)12 (50)

42 (95)40 (91)33 (75)38 (86)

9 (20)34 (77)28 (64)22 (50)

0.550.280.50

0.240.100.930.99

Underlying Medical Conditions Asthma

1 (4)

9 (20)

0.09*

Hospitalizations / Deaths 0 (0) 0 (0) -

Confirmed H1N1 vs. Seasonal Influenza A

* Fisher’s Exact Test

Clinical Chart Abstraction • Reviewed patient medical charts:

– Confirmed Influenza A (H1N1)– Acute febrile respiratory illness (AFRI)

• Fever (100°F or feverishness or chills) plus• Cough, sore throat, nasal congestion, or

rhinorrhea• ILI: fever plus cough or sore throat

– Other upper respiratory infection (URI)– Seasonal influenza A, February/March

2009

Flow Chart for Selection of Charts

Student Health Clinic

Febrile n = 492

Afebrile n = 610

241 abstracted 132 abstracted

*Data for 6 patients from external sources (CCHS, State DPH interviews)

Respiratory Illness 4/5/2009–5/8/2009

n = 1102

2/1/2009–3/21/2009

Seasonal Influenza A n = 44

ILI n = 213

Confirmed H1N1 n = 24*

Summary• Individuals seeking care

– Worried ill– Presented with spectrum of illnesses– Many same symptoms reported

• Possible H1N1

• Severity of H1N1 illness– Mostly mild– Similar clinical illnesses between

H1N1 and seasonal influenza although the numbers were small

Survey Data

Methods

– Examined demographic characteristics

– Calculated attack rates for ILI– Identified factors associated with

transmission among students– Examined community mitigation

measures

Survey Response

• Students– 6,049 (26%) participants

• Faculty/Staff– 1,401 (24%) participants

0

10

20

30

40

50

60

70

Students Faculty/ StaffSurvey Respondent Type

Perc

ent

Men Women

Student Symptoms Reported

Symptoms

ILI (n=604)

N (%)

Other respiratory illness (n=941)

N (%)

FeverSore ThroatCoughRunny Nose/Nasal CongestionHeadacheNausea/VomitingDiarrheaShortness of BreathMuscle AchesFatigue

604 (100)509 (84)475 (79)

508 (84)426 (71)118 (20)131 (22)204 (30)361 (60)470 (78)

61 (6.5)625 (66)609 (65)

771 (82)402 (43)80 (9)99 (11)

171 (16)169 (18)397 (42)

Attack Rates for ILIRisk Factor

Total

ILIN (%)

RR95% CI P-

value

Underlying Health Condition*

YesNo

1995 5455

193 (10)

484 (9)

1.1 (0.9-1.3)

referent

0.29

AsthmaYesNo

11956255

133 (11)

544 (9)

1.3 (1.1-1.6)

referent

0.007RR=Relative Risk, 95% CI=95% Confidence Interval

* Underlying health conditions include: Asthma, chronic lung disease, chronic heart or circulatory disease (including diabetes); kidney disease, recent cancer, immunosuppressive condition, neurologic/neuromuscular disorder

Attack Rates for ILIRisk Factor

Total

ILIN (%)

RR95% CI P-

value

Underlying Health Condition*

YesNo

1995 5455

193 (10)

484 (9)

1.1 (0.9-1.3)

referent

0.29

AsthmaYesNo

11956255

133 (11)

544 (9)

1.3 (1.1-1.6)

referent0.007


* Underlying health conditions include: Asthma, chronic lung disease, chronic heart or circulatory disease (including diabetes); kidney disease, recent cancer, immunosuppressive condition, neurologic/neuromuscular disorder

Health Seeking Behaviors

0

10

20

30

40

50

60

70

Sought healthcare

Per

cent

ILI ARI

P < 0.0001


0

10

20

30

40

50

60

70

Visited healthcare

ILI Other Respiratory Illness

0

10

20

30

40

50

60

70

80

Reasons for Seeking Health Care,ILI

Very SickConcerned about H1N1Advice from Family/ FriendsMedia Coverage


0

10

20

30

40

50

60

70

Visited healthcare

ILI Other Respiratory Illness

0

10

20

30

40

50

60

Reasons for Seeking Health Care,Other Respiratory Illness

Very SickConcerned about H1N1Advice from Family/ FriendsMedia Coverage

Self-Protective Measures:All Students

• 43% concerned about catching H1N1• 65% did something to protect

themselves from catching H1N1• Most common self-protective

measures– Increased hand washing (96%)– Avoided sick people (69%)– Did not share drinks/utensils (58%)

H1N1 Survey Summary: Students and Faculty/Staff

• Illness on campus widespread – Student attack rate higher than

faculty/staff– Older age associated with decreased

risk of ILI

• No protective effect of seasonal influenza vaccine

• H1N1 media coverage and fear influenced decision to seek care

H1N1 Survey Summary:Students

• Risk factors for transmission– ILI risk increased with travel to Mexico

• Associated with early transmission

– ILI risk increased with ‘Greek Week’ participation• Likely to be associated with peak in illness

Measures Taken:Students with Respiratory Illness

• Respiratory illness– Cough, sore throat, nasal congestion– With or without other symptoms– Since May 1, 2009

• To assess behaviors following recommendations provided by UD

Measures Taken:Students with Respiratory Illness

• Increased personal hygiene measures– 75% increased hand washing – 68% covered cough/sneeze – 51% did not share drinks/utensils– 11% wore face mask

• Disregard for isolation measures– 95% left household during 7 days after

illness onset – 77% attended class– 39% attended social events

Qualitative study

Confirmed Case Interview Findings

• Followed recommendations to prevent transmission– Practiced social isolation– Washed hands often– Some reported wearing masks

• Compliant with antiviral medication• Many attributed disease spread on

campus to ‘Greek Week’ activities or travel to Mexico

H1N1 Prevention

• H1N1 Vaccine• Wash hands often with soap and

water or alcohol-based hand rub• Avoid touching eyes, nose or mouth• Avoid close contact with sick people

Conclusions• Risk factors for transmission

– Travel to Mexico– ‘Greek Week’ participation

• Community Mitigation Efforts– All student participants used some

protective measures to prevent illness– Students with acute respiratory illness

• Practiced good hygiene measures• Did not follow isolation recommendations

Recommendations• Prepare for surge in individuals seeking

care– Truly ill and worried well– Use gymnasiums or other large open

venues as emergency clinic space• Set up an call center• Consider cancelling large social events • In the event of another outbreak

– Provide information early with clear, easily accessible and concise

– Provide rationale behind university decisions• Increase student awareness about

university health system

CDC Recommendations• Experiencing ILI

– Facilitate self-isolation of residential students – Promote self-isolation of non-resident

students, faculty and staff– Discourage attendance at campus events

• General recommendations– Increase hand washing – Cover cough or sneeze– Seasonal influenza vaccine– Seek medical advice if experience illness– Complete routine cleaning of high touch areas

http://www.cdc.gov/h1n1flu/institutions/guidance/

http://www.udel.edu/healthalert/

IT recommends technology options for course continuity in event of H1N1 outbreak

Documents

Outbreak of 2009 Pandemic Influenza A (H1N1) Virus on a University Campus – Delaware, April-May 2009 A. Danielle Iuliano, PhD MPH Division of HIV/AIDS