UNDER EMBARGO UNTIL OCTOBER 20, 2009, 12:01 AM LOCAL TIME Novel Influenza A (H1N1) Outbreak at the U.S. Air
Force Academy
Epidemiology and Viral Shedding Duration

Catherine Takacs Witkop, MD, MPH, Mark R. Duffy, DVM, MPH, Elizabeth A. Macias, PhD,Thomas F. Gibbons, PhD, James D. Escobar, MPH, Kristen N. Burwell, MPH, Kenneth K. Knight, MD, MPH The U.S. Air Force Academy is an undergraduate institution that educates and trains cadetsfor military service. Following the arrival of 1376 basic cadet trainees in June 2009,surveillance revealed an increase in cadets presenting with respiratory illness. Specimensfrom ill cadets tested positive for novel influenza A (H1N1 [nH1N1])–specific ribonucleicacid (RNA) by real-time reverse transcriptase–polymerase chain reaction.
The outbreak epidemiology, control measures, and nH1N1 shedding duration are described.
Case patients were identified through retrospective and prospective surveillance. Symp-toms, signs, and illness duration were documented. Nasal-wash specimens were tested fornH1N1-specific RNA. Serial samples from a subset of 53 patients were assessed for presenceof viable virus by viral culture.
A total of 134 confirmed and 33 suspected cases of nH1N1 infection were identified withonset date June 25–July 24, 2009. Median age of case patients was 18 years (range, 17–24years). Fever, cough, and sore throat were the most commonly reported symptoms. Theincidence rate among basic cadet trainees during the outbreak period was 11%. Twenty-nine percent (31/106) of samples from patients with temperature Ͻ100°F and 19%(11/58) of samples from patients reporting no symptoms for Ն24 hours contained viablenH1N1 virus. Of 29 samples obtained 7 days from illness onset, seven (24%) containedviable nH1N1 virus.
In the nH1N1 outbreak under study, the number of cases peaked 48 hours after a socialevent and rapidly declined thereafter. Almost one quarter of samples obtained 7 days fromillness onset contained viable nH1N1 virus. These data may be useful for future investiga-tions and in scenario planning.
(Am J Prev Med 2009;xx(x):xx) Published by Elsevier Inc. on behalf of American Journal ofPreventive Medicine 6 months or longer to establish worldwide distribution;however, the nH1N1 virus strain established worldwide In April 2009, Department of Defense–affiliated labo- distribution within 6 On June 11, 2009, the ratories in San Diego and San Antonio recovered raised the influenza pandemic alert status to unsubtypeable influenza A virus from patient samples.
Level 6 in response to established global human-to- The viral specimens were transported to the CDC human transmission. By July 2009, more than 40,000 influenza laboratory, where both viral samples were nH1N1 cases had been confirmed, and 263 deaths in determined to be a novel influenza A virus of swine origin (nH1N1), consistent with virus isolated from Characterizing virus– host interactions and the epide- patients in a Mexico influenza outbreak that began in miology of nH1N1 is important in both assumptions March Previous novel influenza strains required made during planning and in defining effective controlmeasures. of seasonal influenza suggest thatviral shedding occurs for as long as 7 days after symp- From the U.S Air Force Academy (Witkop, Knight), Colorado tom onset. No similar studies on shedding of nH1N1 Springs, Colorado; and the U.S. Air Force School of Aerospace Medicine Epidemiology Consult Service (Duffy, Macias, Gibbons,Escobar, Burwell), Brooks City Base, Texas published studies of the epidemiology of nH1N1 Address correspondence and reprint requests to: Catherine Takacs infection among military training populations or Witkop, MD, MPH, 10 AMDS/SGPF, 2355 Faculty Drive, Room institutions of higher education. With the 2009 influ- 2N286, U.S. Air Force Academy, Colorado Springs CO 80840. E-mail: enza season upon us, characterization of the epide- Published by Elsevier Inc. on behalf of American Journal of Preventive Medicine miology and duration of shedding for the nH1N1 On July 10, the USAFSAM epidemiology laboratory re- ported that of the first 18 nasal washes tested for the presence In July 2009, the U.S. Air Force Academy (USAFA) of nH1N1 by rRT-PCR, 15 (83%) yielded positive results. By experienced an outbreak of nH1N1 illness. An investi- this time, 88 BCTs were already in the separated dorm area.
gation was initiated to (1) describe the outbreak epide- Case Definition and Finding
miology, (2) define and implement control measures tolimit transmission, and (3) determine the duration of A confirmed nH1N1 case patient was defined as a BCT, a
viral shedding from patients in the outbreak.
cadet involved with BCT training, or a preparatory (prep)school student with symptom onset from June 25 to July 24,2009, who had a nasal-wash specimen with nH1N1 virus identified by rRT-PCR. A suspected case patient also be-
longed to the groups mentioned above and presented with
respiratory complaint onset from June 25 to July 24, 2009; had The USAFA, located west of Colorado Springs CO is a 4-year a highest recorded temperature of Ն100.5°F; and had no academic undergraduate institution that educates and trains cadets for active-duty military service as officers. Incoming Electronic medical records were reviewed to retrospectively students are known as basic cadet trainees (BCTs) during the identify cases with dates of onset between June 25 and July 6.
summer prior to the commencement of the first academic Case patients presenting for medical care starting on July 6 year. BCTs are organized into squadrons of 135–140 individ- through July 24 were prospectively identified. Demographic uals. On June 25, a total of 1376 BCTs arrived at the USAFA and clinical data from confirmed and suspect patients were to begin a 6-week military training program. On July 6, active obtained from electronic medical records and from a stan- surveillance of diagnostic codes for respiratory illnesses dem- dard influenza surveillance questionnaire. The 10th Medi- onstrated an increase in the number of visits for respiratory cal Group pharmacy supplied information related to oselta- complaints that surpassed levels from the two previous years.
By July 7, two cadets evaluated at outside facilities wereidentified as positive for influenza A by rapid antigen test.
Additional Outbreak Control Measures
Because of a strong suspicion that the responsible virus was Patients were prescribed oseltamivir at the treating physi- nH1N1, identification, treatment, and containment efforts cian’s discretion, but were generally given 75 mg of oseltami- were begun immediately. Moreover, the USAFA does not use vir two times daily for 5 days if the patients indicated onset of rapid antigen testing because of its modest sensitivity. Instead, symptoms no more than 72 hours prior to presentation.
nasal-wash specimens were collected from patients with influ- Upper-class cadets ensured meal delivery to patient rooms.
enza like illness (ILI) by saline wash (2– 4 mL) of the Healthcare providers made daily rounds of the separated nasopharynx repeated through each ILI was initially dorm and approved release to the BCT population when a defined as having an oral temperature Ն100.5°F and respira- cadet had reached the end of the 7-day exclusion period and tory symptoms. Specimens were transported to the U.S. Air had been asymptomatic for Ն24 hours.
Force School of Aerospace Medicine (USAFSAM) epidemiol- Healthcare providers and staff caring for patients with ogy laboratory, Brooks City Base TX (near San Antonio), and respiratory illness were offered oseltamivir prophylaxis and tested for the presence of nH1N1-specific ribonucleic acid advised to wear a protective mask while in the same room as (RNA) by real-time reverse transcriptase–polymerase chain the patient exhibiting respiratory symptoms. Healthcare pro- reaction All specimens were tested for influenza viders and technicians were fitted for and provided N95 A; influenza B; respiratory syncytial virus; parainfluenza 1, 2, masks. Technicians collecting nasal-wash samples wore a mask, a and 3; and adenovirus. However, only nH1N1 was identified Screening events were conducted during the outbreak Beginning on July 7, all cadets meeting the ILI case period. On July 13, BCTs marched to a location 3 miles north definition were sent to a separate dorm area to convalesce of the main campus to participate in 12 days of field-training until they were 7 days from symptom onset and were symptom activities. BCTs had their temperature measured with a paper free for 24 hours. On July 10, an additional dorm area was oral thermometer (Tempadot) approximately 1 hour after designated for those presenting with similar respiratory arrival, and those with a temperature Ն99.6°F were referred complaints but with a temperature of 99.0°F to 100.4°F.
for physician evaluation. On July 15, a cohort of 239 students Patients in this group also remained isolated for 7 days and arrived at the USAFA to start a 1-year prep school course. The until 24 hours after symptom resolution, but they were prep school students were screened for temperature Ն99.6°F separated from those with temperatures Ն100.5°F. The sep- on arrival and were screened again on July 19. Students aration of this group, in addition to preventing potential meeting the screening criteria were referred to a physician for transmission, allowed characterization of the spectrum of disease. Interim analysis of data revealed that approximately The third screening event occurred on August 1 after the 50% of individuals with highest recorded temperatures be- remainder of the student body (Ͼ3000 cadets) returned to tween 100.0°F and 100.4°F were positive for nH1N1, with a campus. Upon arriving on campus, each cadet completed a lower incidence of positive nH1N1 results in those with screening questionnaire (Do you feel like you have a fever or have temperatures Ͻ100.0°F. These findings led to a change in the you had a fever in the past 5 days? and Do you have a cough or sore criterion for isolation in the second area to having a temper- throat?). A cadet answering yes to both questions required ature in the range of 100.0°F to 100.4°F.
immediate evaluation by a provider. All cadets were given an American Journal of Preventive Medicine, Volume xx, Number x descriptive results, categor-ical variables were given as Descriptive
firmed and 33 suspectednH1N1 cases identified for a total of 167 incidentcases. Onset dates ranged on July 6, with 37 case pa-tients reporting symptom onset, and the countsdeclined over the re- Figure 1. Confirmed (rRT-PCR positive) and suspect (respiratory complaint, temperature
Ն100.5°F, and no specimen obtained) cases of novel influenza A (H1N1) virus infection at the U.S. Air Force Academy, by date of illness onset, from June 25 through July 24, 2009 education sheet on H1N1 that listed recommendations on mately 48 hours after a 4th of July event where Ͼ1300 BCTs socialized with members of other squadrons.
Public health personnel initiated an intense infection con- Among the 134 confirmed cases, 115 (86%) were BCTs; trol and education campaign within the first 24 hours of ten (7%) were prep school students; and nine (7%) were detecting the outbreak. Mass briefings were conducted on proper cough and hand hygiene, and educational materials Of the 115 confirmed cases among BCTs, 20% (23) were provided for the base newspaper, incoming upper-classcadets, and parents of cadets. Cadets and USAFA personnel were women compared to 21% women in the total BCT also received e-mails detailing the current situation and population. The median age of case patients among recommendations for prevention of transmission. Hand sani- BCTs was 18 years (range 17–24 years), consistent with tizers were placed throughout the dorms and at the entrances the median age of BCTs. The most frequently reported signs and symptoms included cough, chills, sore throat,headache, and fatigue Among 86 confirmed Duration of nH1N1 Shedding
Patients transferred to the separate dorm were requested toprovide a nasal-wash sample approximately every 48 to 72 hours Table 1. Clinical characteristics of 86 patients with
until release. Samples were collected by medical technicians complete clinical information and confirmed nH1N1 according to standard and specimens were shipped on ice the following day to the USAFSAM epidemiology labora-tory. Temperature and presence or absence of symptoms were Sign or symptom
No. of patients (%)
documented for each cadet at every sample collection, and the date of symptom resolution was noted for each cadet. To determine presence of viable virus, specimens were inoculated onto primary monkey kidney Shell vials were stained at 24 – 48 hours for respiratory viruses, including influenza A.
Tubes were incubated at 35°C for 10 days and assessed for cytopathic effect followed by immunofluorescent staining for influenza A. Cultures negative at 10 days were tested by hemad- sorption to rule out influenza virus growth. Viable virus shed- ding was defined as culture-positive results at any time (24 – 48- hour shell vial or 10-day tissue culture).
Statistical Analysis
Data were accumulated in a spreadsheet program and ana- lyzed using SPSS, version 14.0, and Epi Info 3.3.2. For Among 29 samples obtained 7 days from symptom Table 2. Outbreak period incidence (attack rate) of
nH1N1 infection by squadron among basic cadet trainees
onset, seven (24%) contained viable nH1N1 virus Among 106 samples obtained from patients with Confirmeda and
Attack rate
suspected cases
(per 100)
a temperature Ͻ100°F at the time of sample collection,31 (29%) contained viable nH1N1 virus, and 11 (19%) of 58 samples obtained from patients who had been symptom free for Ն24 hours at the time of collection On June 25, an incoming class of BCTs reported to the USAFA originating from all 50 states and 11 foreign countries. In July, the BCT class experienced a novel aReal-time reverse transcriptase–polymerase chain reaction positive H1N1 outbreak representing one of the largest recog-nized nH1N1 clusters at a U.S. college to date. Theoutbreak period incidence rate (attack rate) of con- patients with complete clinical information, the highest firmed and suspected cases among the BCT class was recorded temperature for each patient ranged from 98.4°F to 104.6°F, with a mean of 101.3°F. Among a No deaths or hospitalizations were associated with group of 53 BCTs with confirmed nH1N1 infection and this outbreak. BCTs undergo extensive medical screen- for whom date of symptom resolution was recorded, the ing prior to acceptance to the USAFA (e.g., asthma is a mean duration of symptoms was 5.6 days (range, 1–12 disqualifying medical condition). Therefore, mild dis- days). Disease severity was moderate to mild, and no ease severity and lack of adverse outcomes during this deaths or hospitalizations were attributed to nH1N1 outbreak may be attributable to the stringent physical during the outbreak period. Among these 53 BCTs, 40 requirements for acceptance at the USAFA. The mean received oseltamivir treatment, and their mean dura- duration of illness, however, was greater than 5 days, tion of illness was 5.8 days (95% CIϭ4.9, 6.7 days; and a small subset of cadets was subsequently diagnosed range, 1–12 days) compared to a mean of 5.0 days (95% with bronchitis and pneumonia. Furthermore, college CIϭ4.0, 6.0 days; range 3– 8 days; pϭ0.36) in the 13 who student populations with more heterogeneous health did not receive oseltamivir treatment. The primary conditions could experience more severe disease, in- difference between these two groups was that they cluding possible mortality in those with major underly- presented either in the first 48 hours of their symptoms Outbreak period incidence rates (attack rates) for Table 3. Proportion of nasal-wash samples with viable
confirmed and suspected cases among the ten training nH1N1 by temperature, symptoms, and days from symptom squadrons ranged from 6.8/100 BCTs to 17.9/100 T2 BCTs The overall attack rate for confirmed
and suspected cases among BCTs was 11.0/100 BCTs.
Outbreak Control Measures
A total of 228 cadets (213 BCTs) were placed in separated dorm areas during the outbreak period. The July 15 screening of approximately 1250 BCTs who completed the march to field training resulted in Day from symptom onset
referral of eight (Ͻ1%) BCTs to a physician for further (including day of
evaluation; four were diagnosed with ILI and sent to symptom onset)
the separate dorm. There were no confirmed or suspect Duration of nH1N1 Shedding
A total of 159 serial nasal-wash specimens were col- lected from 53 cadets. The proportion of samples containing viable nH1N1 virus was highest in those obtained on Days 1–3 from symptom onset and de- clined with each proceeding day, beginning on Day 2.
American Journal of Preventive Medicine, Volume xx, Number x Individuals experiencing nH1N1 disease may shed treatment selection bias may have played a role in the virus up to 24 hours prior to onset of symptoms; therefore, it is possible that nH1N1 was introduced by The USAFA outbreak provided a unique opportunity one or more BCTs or trainers before being aware of to gain valuable information about the natural behavior illness themselves. A retrospective records review iden- of the nH1N1 virus. Findings from serial nasal washes tified low levels of patients presenting with ILI in BCTs indicated viable virus shedding on Day 7 from symptom prior to a 4th of July event where BCTs socialized with onset among approximately one quarter of confirmed members of other squadrons. On July 6, cadet clinic cases. Furthermore, being afebrile and asymptomatic personnel recognized an increase in BCTs presenting did not guarantee that the patient was no longer for medical care. The number of BCTs presenting for shedding viable nH1N1 virus; in fact, 19% of those who care increased during the next 2 days and peaked when reported being symptom free for more than 24 hours 130 presented with complaints of respiratory symptoms were still found to shed viable virus. Quantitative anal- on July 8. A surveillance system that used coding data yses of culture results obtained in this study were felt was in place at the USAFA; this system can compare to be inappropriate because of the potential for daily visits for respiratory illnesses with historical data variability in specimen-collection techniques among from the previous 2 years. Such surveillance, if not staff, in specimen-handling procedures, and in transit already in place at colleges and universities, can be a times to the diagnostic laboratory. The lack of quanti- useful tool for early detection of an outbreak.
tative analyses is a limitation of this study. Detection of The outbreak, as defined by date of symptom onset, virus by culture may not necessarily indicate that trans- peaked on July 6, when 37 confirmed and suspect case mission is still possible. Recommended avenues for patients reported onset. Onset date counts of con- future investigation include detailed quantitative anal- firmed and suspect cases declined during the next 14 yses of viral titer during the follow-up period and the days. The outbreak was likely propagated by the mixing identification of specific symptoms associated with via- event on July 4. The interval between the mixing event and peak reported symptom onset is consistent withreported incubation periods for nH1N1, ranging from Novel H1N1 is now endemic in all 50 U.S. states.
1 to 5 days.In addition, all ten BCT squadrons University- and college-based outbreaks of H1N1 have experienced nH1N1 transmission in a short time pe- already occurred and more can be expected as students riod, suggesting that the outbreak was initially propa- gather from diverse geographic areas, reside in dorm settings, and attend mass gatherings such as football The rapid peak of the outbreak and subsequent games, pep rallies, and student assemblies. The combi- decline indicate the effectiveness of response and mit- nation of aggressive separation of ill BCTs, public igation efforts enacted immediately on outbreak recog- health education, and prompt implementation of nition. Communication was critical during the out- healthcare infection control practices limited the dura- break. Timely risk communication allowed for isolation tion and scope of the nH1N1 infection at the USAFA.
of sick BCTs within 24 hours of identification of the Comprehensive plans and rapid implementation are critical. Isolation procedures implemented at the US- Other interventions that potentially contributed to AFA may not be practical in other university settings; the relatively rapid containment of this large out- however, preparedness planning, public health education break included a public health campaign that began activities, and healthcare infection control practices im- within 48 hours of the first suspected cases. This plemented at the USAFA can be adopted in other univer- effort involved e-mails to students, staff, and other military personnel and publication of an article inthe base newspaper to educate the population about We would like to thank the members of the USAFSAM nH1N1 and how to reduce transmission. It also Epidemiology Lab and Consult Services and the 10th Medical included increased distribution of hand sanitizers to Group for their outstanding support in this investigation.
students and placement of hand sanitizers through- Specifically we would like to thank Col (Dr.) Paul Sjoberg, Lt out the dorms and the dining facility. Real-time use Col (Dr.) Victor MacIntosh, Genny Maupin, and Alicia Guer- of data from this population to make interim changes rero from the Epidemiology Consult Service and Madison to the screening and management of the cadet Green and providers and medical technicians from the 10th population probably contributed to containment as Medical Group. We would also like to thank Dr. Gregory well. Infection control among healthcare workers Poland for his review of an earlier version of the manuscript.
also potentially limited virus transmission and fur- The views expressed are those of the authors and do not necessarily represent the views of the U.S. Air Force or the ther spread as no nH1N1 transmission was recog- nized among them. There was no significant differ- No financial disclosures were reported by the authors of ence in duration of illness between those treated and those not treated with oseltamivir; furthermore, in adult patients hospitalized with influenza. J Infect Dis 2009;200:492–500.
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patients with suspected swine-origin influenza A (H1N1) virus infection.
2. WHO. Pandemic (H1N1) 2009 briefing note 3 (revised). Changes in report- ing requirements for pandemic (H1N1)2009 virus infection. 8. Canas LC, Lohman K, Pavlin JA, et al. The Department of Defense laboratory-based global influenza surveillance system. Mil Med 2000;165(7S 3. Pandemic alert Level 6: scientific criteria for an influenza pandemic fulfilled. Euro Surveill 2009;14:19237.
9. Robinson CC. Respiratory viruses. In: Specter S, Hodinka RL, Young SA, Wiedbrauk DL, eds. Virology manual. 4th ed. Washington DC: ASM Press, 5. Sato M, Hosoya M, Kato K, Suzuki H. Viral shedding in children with influenza virus infections treated with neuraminidase inhibitors. Pediatr 10. Thacker E, Janke B. Swine influenza virus: zoonotic potential and vaccina- tion strategies for the control of avian and swine influenzas. J Infect Dis 6. Lee N, Chan PK, Hui DS, et al. Viral loads and duration of viral shedding American Journal of Preventive Medicine, Volume xx, Number x



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