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Cruise Ships: High-Risk Passengers and the Global Spread of New Influenza Viruses

  1. Joy M. Miller1,
  2. Theresa W. S. Tam3,
  3. Susan Maloney1,
  4. Keiji Fukuda2,
  5. Nancy Cox2,
  6. James Hockin3,
  7. Daniel Kertesz4,
  8. Alexander Klimov2, and
  9. Martin Cetron1
  1. 1Division of Quarantine, Atlanta, Georgia, USA
  2. 2Division of Viral and Rickettsial Diseases, National Center for Infectious Diseases, Centers for Disease Control and Prevention, Atlanta, Georgia, USA
  3. 3Field Epidemiology Training Program, Ottawa, Ontario, Canada
  4. 4Division of Respiratory Diseases, Bureau of Infectious Diseases, Laboratory Centre for Disease Control, Health Canada, Ottawa, Ontario, Canada
  1. Reprints or correspondence: Dr. Martin Cetron, Division of Quarantine, MS E03, National Center for Infectious Diseases, Centers for Disease Control and Prevention, Atlanta, GA 30333 (mzc4{at}cdc.gov).
 
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Abstract

In 1997, passengers on North American cruises developed acute respiratory illnesses (ARIs); influenza was suspected. We reviewed 1 ship's medical records for 3 cruises: cruise 1 (31 August to 10 September 1997), cruise 2 (11–20 September 1997), and cruise 3 (20–30 September 1997). Medically attended ARI was defined as any 2 of the following symptoms: fever (temperature, ≥37.8°C) or feverishness, sore throat, cough, nasal congestion, chills, myalgia, and arthralgia. During cruise 2, we collected nasopharyngeal swabs for viral culture from people with ARI and surveyed passengers for self-reported ARI (defined as above except feverishness was substituted for fever). The outbreak probably began among Australian passengers on cruise 1 (relative risk, 3.3; 95% confidence interval, 1.89–5.77). Of 1284 passengers on cruise 2, 215 (17%) reported ARI, 994 (77%) were aged ≥65 years, and 336 (26%) had other risk factors for respiratory complications. An influenza strain not previously identified in North America was isolated. We concluded that an “off-season” influenza outbreak occurred among international travelers and crew on board this cruise ship.

In 1996, ∼5 million people took North American cruise vacations [1]. The rapidly growing North American cruise industry attracts many international travelers, and approximately one-third of cruise passengers are senior citizens. Elderly travelers and other persons with underlying health problems are at increased risk for complications of influenza virus infection [2–5]. During a cruise, passengers and crew from several nations intermingle for extended periods in semienclosed compartments. Shipboard activities such as dining, games, and movies increase the likelihood of contact between passengers and crew. The average cruise lasts 6 days, well within the period for incubation and transmission of many infectious diseases. After their cruise vacation, travelers disperse and may spread acquired infections after leaving the cruise.

On 10 September 1997, Health Canada (Ottawa, Ontario, Canada) was notified by local health authorities that 6 of 1445 passengers who had disembarked from a cruise ship that had travelled from New York City to Montreal had been hospitalized for acute respiratory illnesses (ARIs). Initially, legionellosis was suspected, but urine specimens from the hospitalized passengers and from 33 crew with respiratory illnesses were negative for Legionella pneumophila serotype 1 soluble antigens. An immunofluorescent antibody assay (IFA) of a throat swab specimen from a hospitalized passenger was positive for influenza A virus. Because of continued ARI activity among passengers and crew on the return cruise from Montreal to New York City, the Centers for Disease Control and Prevention (CDC) and Health Canada were invited by the cruise line to investigate the outbreak. Influenza outbreaks on cruise ships have rarely been reported [6–8], and, to our knowledge, this investigation is the first to use control measures similar to those recommended for outbreaks among high-risk populations in other semiclosed environments (e.g., nursing homes) [2].

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Methods

Objectives. The objectives of this investigation were to characterize the outbreak, to determine the number of passengers and crew at risk for respiratory complications, and to recommend interventions.

Epidemiological investigation. In 1997, the cruise ship traveled from New York City to Montreal from 31 August to 10 September (cruise 1), from Montreal to New York City from 11–20 September (cruise 2), and from New York City to Montreal from 20–30 September (cruise 3). The cruise line provided data on the total number of passengers (cruise 1, 1445; cruise 2, 1448; and cruise 3, 1443) and crew (631). New passengers embarked at each destination city, while composition of the crew remained relatively unchanged. The cruise line provided the ship's manifest or marketing survey data on the nationalities of passengers on cruises 1 and 2; no data were provided on nationalities for passengers on cruise 3. For cruise 2, we collected data on the age and sex of the passengers during our investigation.

Information on passengers and crew with respiratory illnesses was obtained from 3 sources: review of medical records for persons presenting to the ship's infirmary (cruises 1–3), self-administered surveys of ill and healthy passengers (cruise 2), and active surveillance for ARI among crew (cruises 2 and 3). Data were collected on demographic characteristics, symptoms of respiratory illness, and risk factors for severe complications of influenza (i.e., cardiac and pulmonary diseases, diabetes, renal insufficiency, chronic liver disease, cancer [not in remission], and immunosuppression).

We defined medically attended ARI as an illness that occurred during the period from 3 days before the start of a cruise to the end of the cruise among passengers and crew who presented to the ship's infirmary with ≥2 of the following symptoms: fever (temperature, ≥37.8°C) or feverishness, cough, sore throat, nasal congestion, chills, myalgia, and arthralgia. Medically attended influenza-like illness (ILI), a subset of ARI, was defined as documented fever (temperature, ≥37.8°C) and either sore throat or cough [9]. No follow-up was performed to identify passengers who developed ARI after the end of each cruise. All results reported herein refer to medically attended ARI or ILI unless stated otherwise.

On 17 and 18 September 1997 (during cruise 2), we provided all passengers and crew a self-administered survey that asked about symptoms and risk factors for respiratory complications of ARI. For analysis of survey data, we defined self-reported ARI and ILI using the case definitions for medically attended ARI and ILI described above, except a self-reported history of fever (feverishness) was substituted for documented fever. We included in the analysis respiratory illnesses with onset dates ≤3 days from the start date of the cruise (7 September for passengers and 28 August for crew) to the date of the survey.

The crew also were surveyed about their job duties and smoking habits (supervisors interpreted the survey for crew who did not speak English). During cruises 2 and 3, supervisors actively surveyed crew daily for respiratory illnesses by asking “in the past 24 hours, have you had any fever, runny nose, sore throat, cough, joint pain, muscle aches, or chills?” Crew with these symptoms were required to report to the ship's infirmary for examination and were asked to complete the patient questionnaire. For analysis of crew data, we assumed that crew with onset of ARI during a previous cruise were no longer susceptible and therefore removed them from the number of crew at risk. Because crew turnover was low (<20 new crew per cruise), we did not adjust the number of crew at risk to account for new crew who boarded the ship after cruises 1 or 2.

Laboratory methods. Of the 6 passengers on cruise 1 who presented to the hospital in Montreal, 5 were admitted and had nasopharyngeal swabs (NPSs) or throat swabs obtained for virus testing. Specimens were tested for influenza virus by IFA; IFA-positive specimens were cultured for influenza virus using standard techniques. Health Canada further identified influenza A virus (H3N2) isolates by hemagglutination inhibition testing [10].

During cruise 2, NPSs were obtained from 11 passengers and 22 crew who presented to the ship's infirmary for ARI; specimens were inoculated into viral transport media. NPSs from the 11 passengers and 1 crew member were tested for influenza A virus nucleo-protein antigen by using an EIA (Directogen FLU-A, Becton Dickinson Microbiology Systems, Cockeysville, MD). The CDC cultured all 33 NPSs for influenza virus and performed influenza virus strain identification by means of a hemagglutination inhibition assay. An NPS from 1 passenger on cruise 2 was tested for influenza A virus at a New York City hospital by means of a rapid antigen assay. Passengers on cruise 3 who reported to the infirmary with ARI or ILI were not asked to provide an NPS and were treated with an antiviral, as described below.

Statistical analysis. Relative risk and 95% CIs were estimated by using Epi-Info statistical software (version 6.04, CDC). Yates' corrected χ2 statistics were used to compare 2 proportions. χ2 tests for linear trend were used to evaluate differences in risk for ARI and ILI by cruise [11]. A P value of ≤.05 was considered statistically significant.

Interventions. During cruise 2, control measures were instituted to interrupt virus transmission (figure 1). Passengers who presented to the ship's infirmary with ARI received 5-day courses of antiviral therapy (rimantadine) and were advised to limit contact with other passengers. All passengers without ARI were offered rimantadine prophylaxis for 10 days. In a passenger survey, 929 (72%) of 1284 passengers reported attending a counseling session on the risks and benefits of antiviral prophylaxis, and 1016 (81%) of 1262 passengers reported taking rimantadine prophylaxis.

Figure 1
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Figure 1

Number of medically attended acute respiratory illnesses (ARIs) and influenza-like illnesses (ILIs) among passengers and crew on 3 cruises of 1 ship during August and September 1997, by date of onset. ARIs included any 2 of the following symptoms: fever (temperature, ≥37.8°C) or feverishness, sore throat, cough, chills, nasal congestion, myalgia, and arthralgia. The date of illness onset was unknown for 8 of 74 passengers with ARI on cruise 1 and 1 of 27 passengers with ARI on cruise 3. The date of illness onset was known for all 47 passengers with ARI on cruise 2. ILIs, a subset of ARI, included documented fever (temperature, ≥37.8°C) and either sore throat or cough. For the purposes of the figure, other ARIs are compatible respiratory illnesses in which fever was not recorded or reported. Date of illness onset was unknown for 3 of 39 passengers with ILI on cruise 1. The date of illness onset was known for the 19 passengers with ILI on cruise 2 and the 3 passengers with ILI on cruise 3.

During cruises 2 and 3, crew identified as having ARI through active surveillance for cases were confined and treated with 5-day courses of rimantadine. Ill crew were moved to rooms with other ill crew and served meals in their cabin. Starting on 17 September 1997, all crew received rimantadine prophylaxis for 10 days, and most crew (597 [95%] of 631) received the 1997–1998 influenza virus vaccine (A/Johannesburg/82/96 [H1N1], A/Nanchang/933/95 [H3N2], B/Harbin/07/94).

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Results

Description of the outbreak. Passengers on cruises 1 and 2 were from many different countries and from both hemispheres (table 1). Of 1445 passengers on cruise 1, 74 (5%) presented to the ship's infirmary for ARI (table 2); of these 74 passengers, 57 (77%) were aged ≥65 years, and 32 (43%) had at least 1 chronic health condition. Six passengers from cruise 1 were hospitalized for respiratory complications of influenza, and all of these passengers were aged ≥65 years and had at least 1 chronic health condition. Of 1448 passengers on cruise 2, 47 (3%) had ARI, and of these 47 passengers, 44 (94%) were aged ≥65 years, and 29 (62%) had chronic health conditions. One passenger on cruise 2, a 75-year-old woman, was hospitalized for ARI. Of 1443 passengers on cruise 3, 27 (2%) had ARI, and none were hospitalized.

Table 1
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Table 1

Country of residence for passengers on 2 North American cruises, 1997.

Table 2
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Table 2

Medically attended acute respiratory illnesses (ARIs) and influenza-like illnesses (ILIs) and hospitalizations in passengers who presented to the ship's infirmary on 3 North American cruises, 1997.

Three percent (21) of 631 crew had ARI that developed 3 days before or during cruise 1. For cruises 2 and 3, the attack rates for ARI among crew were 47 (8%) of 610 and 6 (1%) of 563), respectively (χ2 statistic, 29.91; degree of freedom [df], 1; P < .0001). ILI in crew followed a similar pattern: 7 (1%) of 631 crew had developed ILI 3 days before or during cruise 1, 14 (2%) of 624 crew developed ILI during cruise 2, and none of 610 crew developed ILI during cruise 3. Assuming that ill crew may have remained susceptible did not significantly change the analysis.

The course of the outbreak among passengers and crew is illustrated in figure 1. Date of illness onset was known for 66 of 74 passengers with ARI (36 of 39 passengers with ILI) on cruise 1, 47 of 47 passengers with ARI (19 of 19 passengers with ILI) on cruise 2, and 26 of 27 passengers with ARI (3 of 3 passengers with ILI) on cruise 3. During cruise 1, symptoms in 7 passengers began 3 days before the start of the cruise. The number of cases of ARI in passengers on cruise 1 peaked toward the end of the cruise. Cases of ARI in crew began to occur in late August, and the number of cases peaked during the period 12–15 September, 5 days after the peak of cases in passengers on cruise 1. During cruise 2, the peak of cases of ARI in passengers occurred 5 days into the voyage. The number of cases of ARI in crew and passengers on cruise 2 declined after control measures were implemented. Only 27 passengers and 6 crew had an onset of ARI during cruise 3.

Studies of risks for ARI or complications of influenza. We analyzed risks of ARI, which paralleled the pattern for ILI. During cruise 1, the attack rate for ARI was higher among Australian passengers than among non-Australian passengers (13 of 87 vs. 60 of 1324, respectively; RR, 3.3; 95% CI, 1.89–5.77). Australian passengers also were more likely than other passengers to develop ARI symptoms before or on the day of boarding the cruise ship (7 of 87 vs. 3 of 1324, respectively; RR, 35.5; 95% CI, 9.34–134.94).

Approximately 1284 (90%) of 1448 passengers and 493 (78%) of 631 crew responded to the surveys distributed during cruise 2. Of respondents, 215 (17%) of 1284 passengers and 92 (19%) of 493 crew had self-reported ARI (table 3). In addition, most surveyed passengers were elderly (994 [77%] of 1284), and many reported one or more risk factors, other than age, for complications of influenza (336 [26%] of 1284). Crew who reported smoking tobacco within the last 12 months were more likely to have self-reported ARI than were nonsmokers (47 of 179 vs. 45 of 314, respectively; RR, 1.83; 95% CI, 1.27–2.64). Of crew, those with close passenger contact (e.g., administration, concessionaires, food and beverage service, infirmary, and housekeeping) were more likely to develop ARI than were crew with nautical, technical, or food preparation jobs (59 of 432 vs. 16 of 182, respectively; RR, 1.69; 95% CI, 1.00–2.86).

Table 3
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Table 3

Demographics and medical histories of passengers and crew on a North American cruise based on a self-administered surveys distributed to passengers and crew on 17–18 September 1997.

Laboratory testing results. Respiratory specimens from 4 of 6 passengers on cruise 1 who were hospitalized in Montreal were positive for influenza A virus by IFA. Influenza A virus was isolated from 3 of these specimens; 2 were characterized as A/Sydney/5/97 (H3N2)-like viruses, and 1 was an A/Wuhan/359/95 (H3N2)-like virus. One of 11 NPSs from passengers on cruise 2 was positive for influenza virus by EIA, and 1 of 1 NPS from crew on cruise 2 was negative; cultures of 6 NPSs from passengers and 7 NPSs from crew were positive for influenza A virus, and all isolates were A/Sydney/5/97 (H3N2)-like viruses. An NPS from the passenger on cruise 2 who was hospitalized in New York City was positive for influenza A virus by direct antigen testing, but viral culture was negative.

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Discussion

This investigation highlights that cruise ships are a travel destination for the elderly and that early recognition of an influenza outbreak in this setting aided in minimizing respiratory complications. Our findings suggest that during this outbreak, influenza cases began among Australian passengers and rapidly spread to crew who had close passenger contact. The crew probably served as a reservoir for influenza virus infection and as a source of transmission to subsequent passengers. During cruises 1 and 2, 74 (5%) of 1448 and 47 (3%) of 1445 passengers presented to the ship's infirmary for acute respiratory illnesses, respectively. Seven of these passengers were hospitalized for respiratory complications of influenza. Although substantial, the number of persons who presented to the ship's infirmary represented the “tip of the iceberg.” The self-administered surveys distributed during cruise 2 demonstrated that 215 (17%) of 1284 passengers and 92 (19%) of 493 crew had self-reported ARI symptoms but that only 47 (3%) of 1448 passengers and 47 (8%) of 610 crew presented to the infirmary. In addition, an unknown number of passengers may also have developed ARI or serious complications of influenza after they returned home from their cruise. Therefore, respiratory illnesses reported to the ship's infirmary greatly underestimated the impact of the outbreak.

This investigation also illustrated that cruise ships can present infection control issues similar to those in nursing homes. Cruise ships often serve high-risk passengers and offer extended medical services (e.g., oxygen therapy and onboard renal dialysis units) for their passengers. The survey of passengers on the ship in this investigation showed that about three-fourths were elderly and about one-fourth reported having at least 1 additional risk factor for respiratory complications of influenza. Several passengers on the ship traveled with portable oxygen, 36 passengers reported having cancer (not in remission), and 3 passengers were undergoing onboard renal dialysis. During the cruise, frequent group activities (e.g., bingo, movies, dining, and tours) were held in semiclosed compartments (e.g., meeting rooms, ballrooms, and cinemas) that increased passenger and crew contacts and facilitated the spread of influenza. In addition, passengers who disembarked from cruise 1 and incoming passengers for cruise 2 probably stayed in the same Montreal area hotels. Cruise travel packages tend to include airline flights and hotels, which facilitated contacts between passengers before and during the cruise. These factors may contribute to transmission of influenza and increase the number of people harboring illness before boarding the ship.

To interrupt the transmission of influenza and prevent further morbidity during this outbreak, we recommended interventions similar to those used to control outbreaks in institutional settings such as nursing homes [2]. Beginning midway through cruise 2, ill crew were confined to their cabins and provided antiviral therapy, while healthy crew were provided antiviral prophylaxis. Immunization of the crew against influenza also was recommended, primarily to eliminate them as reservoirs for influenza viruses and to decrease their role in transmitting influenza to passengers and other crew. The diminished effectiveness of the 1997–1998 influenza virus vaccine against the A/Sydney strain was not known at the time of the outbreak [12]. Ill passengers were offered antiviral therapy for 5 days, and nonsymptomatic passengers were offered antiviral prophylaxis. We documented that 1016 (81%) of 1262 passengers on cruise 2 reported taking antiviral prophylaxis.

Because passengers on cruise 2 disembarked shortly after antiviral prophylaxis was started, we were unable to assess fully the impact of this control measure. However, the control measures instituted during cruises 2 and 3 appeared to interrupt transmission between passengers and crew. After cruise 2, 1 passenger was hospitalized for respiratory complications of ARI; 6 passengers were hospitalized after cruise 1. During cruise 3, significantly fewer passengers presented with respiratory illnesses (2% with ARI and <1% with ILI), and none were hospitalized. In addition, <1% of the crew developed ARI during cruise 3, and none developed ILI. The cruise ship took on a large group of new passengers every 10 days and crew may have continued to be a reservoir for influenza virus infections. Therefore, without control measures, it is possible that the outbreak of influenza would have continued for several weeks. During a 1998 summertime influenza outbreak among land and cruise ship travelers in Alaska and the Yukon Territory, influenza transmission persisted for 5 months [13].

We also recommended several preventive measures to help prevent future outbreaks. First, we recommended that the cruise lines establish surveillance for febrile respiratory illnesses, including onboard use of rapid diagnostic assays for detection of influenza. Second, we recommended that cruise lines operating in North American waters vaccinate their crew against influenza, recognizing the fact that the optimal timing of when (early summer or during the fall) and how often (once or twice a year) to vaccinate the crew remain undetermined. Finally, we recommended that high-risk persons consult with their health care providers before travel to determine whether they need influenza virus vaccination or need antiviral prophylaxis if they will be traveling during periods of influenza activity. These recommendations were provisional and general because much about the epidemiology of influenza outbreaks on board cruise ships remains unclear and discussions on the availability and formulation of vaccine are ongoing.

Although outbreaks of influenza in the Northern Hemisphere most frequently occur in the winter months (December to April) [14], the timing of this outbreak illustrates that influenza can occur at any time of year. Summertime influenza outbreaks have been reported, but unusual timing may delay identification of the etiology and therefore delay intervention [15]. In our investigation, rapid diagnostic assays helped reduce this delay. Urine assays of specimens obtained during cruise 1 demonstrated that legionella pneumonia was an unlikely etiology. IFA and direct antigen assays for influenza A virus provided rapid diagnosis and confirmed that influenza virus infections were ongoing.

In the Southern Hemisphere, seasonal influenza epidemics occur from May to September and may predict (or follow) the virus that will circulate in the Northern Hemisphere [16]. During July and August 1997, outbreaks caused by influenza A/Sydney/5/97-like viruses first were detected in Australia, New Zealand, and other parts of the Southern Hemisphere. During August 1997, a group of 87 passengers flew from Sydney, Australia, to New York City and then boarded a cruise ship, all within in a few days time. Early in the outbreak, the attack rate of ARI among these passengers was significantly higher than that among passengers from other countries, and they may have been harboring influenza before boarding the ship. This outbreak was the first outbreak in North America associated with this virus. The A/Sydney variant contributed to substantial morbidity and mortality during the 1997–1998 North American influenza season [17]. This report highlights the potential role of international travel in the rapid dissemination and global spread of new influenza viruses and the need to maintain adequate surveillance and response capabilities for travel-related emerging infections.

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Acknowledgments

We acknowledge the contributions of the following: C. Afife, M.S. (US Public Health Service, New York Quarantine Station, New York); J. R. Miller, M.D. (New York City Department of Health, New York); N. Schowengerdt, R. Peterson, J. Anderson, J. Frazier, G. Howerton, M.D., and C. Hill, M.D. (Holland America Line Westours, Seattle); K. F. Gensheimer, M.D. (Maine Department of Health, Portland, ME); M. A. Barry, M.D. (Boston Public Health Commission, Boston); U. A. Bandy, M.D. (Rhode Island Department of Public Health, Providence, RI); M. Miller, M.D. (SMBD-Jewish General Hospital, Montreal); M. Libman, M.D. (Montreal General Hospital); P. Ren, M.D. (Royal Victoria Hospital, Montreal); La Direction de la Santé Publique de Montréal-Centre / Montreal-Centre Public Health Department; the Office of Special Health Initiatives, Quarantine Health Services and Occupational Health and Safety Agency, Health Canada, Ottawa, Ontario, Canada; Divisions of Quarantine and Viral and Rickettsial Diseases, Centers for Disease Control and Prevention, Atlanta.

  • Received September 13, 1999.
  • Revision received December 30, 1999.
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References

  1. ↵
    Cruise Lines International Association. The cruise industry: an overview. New York: Cruise Lines International Association; 1997.
  2. ↵
    Centers for Disease Control and Prevention. Prevention and control of influenza: recommendations of the Advisory Committee on Immunization Practices (ACIP). MMWR Morb Mortal Wkly Rep 1999;48(RR-4):1-28.
    Medline
    1. Barker WH,
    2. Mullooly JP
    . Impact of epidemic type A influenza in a defined adult population. Am J Epidemiol 1980;112:798-811.
    Abstract/FREE Full Text
    1. Eickhoff TC,
    2. Sherman IL,
    3. Serfling RE
    . Observations on excess mortality associated with epidemic influenza. JAMA 1961;176:776-82.
    Abstract/FREE Full Text
  5. ↵
    1. Glezen WP,
    2. Decker M,
    3. Perrotta DM
    . Survey of underlying conditions of persons hospitalized with acute respiratory disease during influenza epidemics in Houston, 1978–1981. Am Rev Respir Dis 1987;136:550-5.
    MedlineWeb of Science
  6. ↵
    1. Christenson B,
    2. Lidin-Janson G,
    3. Kallings I
    . Outbreak of respiratory illness on board a ship cruising to ports in southern Europe and northern Africa. J Infect 1987;14:247-54.
    CrossRefMedlineWeb of Science
  7. Centers for Disease Control. Outbreak of influenza-like illness in a tour group: Alaska. MMWR Morb Mortal Wkly Rep 1987;36:697-98. 704.
    Medline
  8. ↵
    Centers for Disease Control. Acute respiratory illness among cruise-ship passengers: Asia. MMWR Morb Mortal Wkly Rep 1988;37:63-6.
    Medline
  9. ↵
    1. Brammer L,
    2. Fukuda K,
    3. Arden N,
    4. Schmeltz LM,
    5. Simonsen L,
    6. Khan A,
    7. Regnery HL,
    8. Schonberger LB,
    9. Cox NJ
    . Influenza surveillance-United States, 1992–93 and 1993–94. MMWR Morb Mortal Wkly Rep 1999;46:1-12.
  10. ↵
    1. Kendal AP,
    2. Pereira MS,
    3. Skehel J
    . Concepts and procedures for laboratory-based influenza surveillance. Geneva, Switzerland: World Health Organization; 1982. p. B19-B35.
  11. ↵
    1. Schlesselman JJ
    . Case-control studies: design, conduct, analysis. New York: Oxford University Press; 1982. p. 203-6.
  12. ↵
    Centers for Disease Control and Prevention. Update: influenza activity—United States, 1997–98 season. MMWR Morb Mortal Wkly Rep 1998;47:196-200.
    Medline
  13. ↵
    Centers for Disease Control and Prevention. Update: outbreak of influenza A infection: Alaska and the Yukon Territory, July–August 1998. MMWR Morb Mortal Wkly Rep 1998;47:685-8.
    Medline
  14. ↵
    1. Mandell GL,
    2. Bennett JE,
    3. Dolin R
    1. Betts RF
    . Influenza virus. In: Mandell GL, Bennett JE, Dolin R, editors. Mandell, Douglas and Bennett's principles and practice of infectious diseases. 4th ed. New York: Churchill Livingstone; 1995. p. 1546-67.
  15. ↵
    1. Kohn MA,
    2. Farley TA,
    3. Sundin D,
    4. Tapia R,
    5. McFarland LM,
    6. Arden NH
    . Three summertime outbreaks of influenza. J Infect Dis 1995;172:246-9.
    Abstract/FREE Full Text
  16. ↵
    1. Kilbourne ED,
    2. Kilbourne ED
    . Influenza viruses and influenza. New York: Academic Press; 1975. Epidemiology of influenza; p. 483-538.
  17. ↵
    Centers for Disease Control and Prevention. Update: influenza activity—United States and worldwide, 1997–98 season and composition of the 1998–99 influenza vaccine. MMWR Morb Mortal Wkly Rep 1998;47:280-4.
    Medline
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  1. Clin Infect Dis. (2000) 31 (2): 433-438. doi: 10.1086/313974
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