Disease transmission and passenger behaviors during a high morbidity Norovirus outbreak on a cruise ship, January 2009.

BACKGROUND: Norovirus continues to pose a significant burden on cruise ships, causing an average of 27 confirmed outbreaks annually over the past 5 years. In January 2009, the report of a suspected norovirus outbreak among passengers on a cruise ship prompted an investigation. METHODS: A retrospective cohort study among passengers was conducted on board the ship. Questionnaires about health care-seeking behaviors, hygiene practices, and possible norovirus exposures were placed in every cabin. Stool samples from several ill passengers were tested for norovirus by quantitative reverse-transcriptase polymerase chain reaction (RT-qPCR) and confirmed by sequence analysis. RESULTS: Of 1842 passengers, 1532 (83.2%) returned questionnaires, and 236 (15.4% of participants) met the case definition. Of these, 95 (40%) did not report to the infirmary. Case passengers were significantly more likely to have an ill cabin mate (relative risk [RR] = 3.0; P < .01) and to have witnessed vomiting during boarding (RR = 2.8; P = .01). Over 90% of all passengers reported increased hand hygiene practices following the outbreak; 38% of ill passengers and 11% of well passengers decreased participation in public activities. Of 14 samples tested, 12 were positive for norovirus by RT-qPCR; 5 of these were confirmed by sequence analysis and typed as GII.4 Minerva. CONCLUSIONS: Person-to-person transmission, including an incident of public vomiting during boarding, likely contributed to this high morbidity outbreak. Infirmary surveillance detected only 60% of acute gastroenteritis (AGE) cases involved in this outbreak. Adjustments to outbreak reporting thresholds may be needed to account for incomplete voluntary AGE reporting and to more rapidly implement control measures.

Shipshape: sanitation inspections on cruise ships, 1990-2005, Vessel Sanitation Program, Centers for Disease Control and Prevention.

In the course of a successful collaboration between the Centers for Disease Control and Prevention (CDC) and the cruise ship industry on reducing common-source outbreaks, CDC's Vessel Sanitation Program (VSP) has expanded its training, education, and cruise ship inspection programs. The study reported here evaluated 15 years of ship sanitation inspection data from the National Center for Environmental Health and assessed performance in specific sanitation categories from 1996 to 2005. During the period 1990-2005, scores from cruise ship environmental sanitation inspections steadily improved. The percentage of inspections with violations decreased among five of nine categories. Those five categories were Washing Facilities, Contact Surfaces, Facility Maintenance, Food Handling, and Communicable Disease Practices. Inspection violations increased proportionally in the categories of Swimming Pools and Water System Protection/Chart Recording. Overall continued good performance in most sanitation categories is likely attributable to on-site training during inspections, improvements in ship construction, and a switch from hot-holding temperatures to time limits as a public health control for foods on display.

Epidemiology of gastroenteritis on cruise ships, 2001-2004.

BACKGROUND: The incidence of diarrheal disease among cruise ship passengers declined from 29.2 cases per 100,000 passenger days in 1990 to 16.3 per 100,000 passenger days in 2000. In 2002, the Vessel Sanitation Program of the Centers for Disease Control and Prevention reported 29 outbreaks (3% or more passengers ill) of acute gastroenteritis on cruise ships, an increase from 3 the previous year. This analysis of gastroenteritis on cruise ships, conducted in 2005, details the increase in outbreak incidence rates during 2001 through 2004. METHODS: Using Gastrointestinal Illness Surveillance System data, investigators evaluated incidence rates of gastroenteritis on cruise ships calling on U.S. ports, carrying 13 or more passengers, by cruise length and reporting region during the study period. The investigators also evaluated the association between inspection scores, and gastroenteritis incidence and the frequency of outbreaks in 2001 through 2004. RESULTS: During the study period, the background and outbreak-associated incidence rates of passengers with acute gastroenteritis per cruise were 25.6 and 85, respectively. Acute gastroenteritis outbreaks per 1000 cruises increased overall from 0.65 in 2001 to 5.46 in 2004; outbreaks increased from 2 in 2001 to a median of 15 per year in 2002-2004. Median ship inspection scores remained relatively constant during the study period (median 95 on a 100-point scale), and were not significantly associated with either gastroenteritis incidence rates (risk ratio, 1.00; 95% confidence interval, 0.98-1.02) or outbreak frequency (Spearman's coefficient, 0.01, p=0.84). CONCLUSIONS: Despite good performance on environment health sanitation inspections by cruise ships, the expectation of passenger cases of gastroenteritis on an average 7-day cruise increased from two cases during 1990-2000 to three cases during the study period. This increase, likely attributable to noroviruses, highlights the inability of environmental programs to fully predict and prevent risk factors common to person-to-person and fomite spread of disease.

Diarrheal disease on cruise ships, 1990-2000: the impact of environmental health programs.

BACKGROUND: In 1975, the then-Center for Disease Control (CDC) established the Vessel Sanitation Program (VSP) to minimize the risk for diarrheal disease among passengers and crew aboard ships by assisting the cruise ship industry in developing and implementing comprehensive environmental health programs. OBJECTIVES: To evaluate the relationship between cruise ship sanitation scores and diarrheal disease incidence and outbreaks among cruise ship passengers. METHODS: Retrospective cohort study of ship inspection and diarrheal disease data from 1990 through 2000 from the National Center for Environmental Health, CDC database, for cruise ships entering the United States. OUTCOMES: Yearly trends in number of ships inspected, number of inspections conducted, inspection scores, and risks of failing inspections; rates of diarrheal disease among passengers, by inspection year, cruise duration, incidence of outbreaks, and passing- or failing-score status of the associated ship. RESULTS: From 1990 through 2000, inspection scores gradually increased from a median of 89 in 1990 to 93 in 2000 (p<0.001), with an associated statistically significant 21% increase in likelihood of passing. The total baseline level of diarrhea among passengers was 2.0 cases per cruise (13243/6485), or 23.6 cases per 100,000 passenger-days (13243/56129096). The latter rate declined significantly from 29.2 in 1990 to 16.3 in 2000 (p<0.0001). Diarrheal disease incidence rates among passengers sailing on ships that passed environmental inspections were significantly lower than rates among passengers sailing on ships that failed inspections (21.7 vs 30.1; RR = 1.39; 95% CI: 1.31-1.47). Diarrheal disease outbreak-related illnesses decreased from 4.2 to 3.5 per 100000 passenger-days from 1990-1995 to 1996-2000. CONCLUSIONS: Environmental sanitation inspections conducted among ships sailing into the United States appear to continue to decrease diarrheal disease rates and outbreaks among passengers.

A review of outbreaks of foodborne disease associated with passenger ships: evidence for risk management.

OBJECTIVE: Foodborne disease outbreaks on ships are of concern because of their potentially serious health consequences for passengers and crew and high costs to the industry. The authors conducted a review of outbreaks of foodborne diseases associated with passenger ships in the framework of a World Health Organization project on setting guidelines for ship sanitation. METHODS: The authors reviewed data on 50 outbreaks of foodborne disease associated with passenger ships. For each outbreak, data on pathogens/toxins, type of ship, factors contributing to outbreaks, mortality and morbidity, and food vehicles were collected. RESULTS: The findings of this review show that the majority of reported outbreaks were associated with cruise ships and that almost 10,000 people were affected. Salmonella spp were most frequently associated with outbreaks. Foodborne outbreaks due to enterotoxigenic E. coli spp, Shigella spp, noroviruses (formally called Norwalk-like viruses), Vibrio spp, Staphylococcus aureus, Clostridium perfringens, Cyclospora sp, and Trichinella sp also occurred on ships. Factors associated with the outbreaks reviewed include inadequate temperature control, infected food handlers, contaminated raw ingredients, cross-contamination, inadequate heat treatment, and onshore excursions. Seafood was the most common food vehicle implicated in outbreaks. CONCLUSIONS: Many ship-associated outbreaks could have been prevented if measures had been taken to ensure adequate temperature control, avoidance of cross-contamination, reliable food sources, adequate heat treatment, and exclusion of infected food handlers from work.

A review of outbreaks of waterborne disease associated with ships: evidence for risk management.

OBJECTIVE: The organization of water supply to and on ships differs considerably from that of water supply on land. Risks of contamination can arise from source water at the port or during loading, storage, or distribution on the ship. The purpose of this article is to review documented outbreaks of waterborne diseases associated with passenger, cargo, fishing, and naval ships to identify contributing factors so that similar outbreaks can be prevented in the future. METHODS: The authors reviewed 21 reported outbreaks of waterborne diseases associated with ships. For each outbreak, data on pathogens/toxins, type of ship, factors contributing to outbreaks, mortality and morbidity, and remedial action are presented. RESULTS: The findings of this review show that the majority of reported outbreaks were associated with passenger ships and that more than 6,400 people were affected. Waterborne outbreaks due to Enterotoxigenic Escherichia coli, noroviruses, Salmonella spp, Shigella sp, Cryptosporidium sp, and Giardia lamblia occurred on ships. Enterotoxigenic E. coli was the pathogen most frequently associated with outbreaks. One outbreak of chemical water poisoning also occurred on a ship. Risk factors included contaminated port water, inadequate treatment, improper loading techniques, poor design and maintenance of storage tanks, ingress of contamination during repair and maintenance, cross-connections, back siphonage, and insufficient residual disinfectant. CONCLUSIONS: Waterborne disease outbreaks on ships can be prevented. The factors contributing to outbreaks emphasize the need for hygienic handling of water along the supply chain from source to consumption. A comprehensive approach to water safety on ships is essential. This may be achieved by the adoption of Water Safety Plans that cover design, construction, operation, and routine inspection and maintenance.

Practice patterns of naturopathic physicians: results from a random survey of licensed practitioners in two US States.

BACKGROUND: Despite the growing use of complementary and alternative medicine (CAM) by consumers in the U.S., little is known about the practice of CAM providers. The objective of this study was to describe and compare the practice patterns of naturopathic physicians in Washington State and Connecticut. METHODS: Telephone interviews were conducted with state-wide random samples of licensed naturopathic physicians and data were collected on consecutive patient visits in 1998 and 1999. The main outcome measures were: Sociodemographic, training and practice characteristics of naturopathic physicians; and demographics, reasons for visit, types of treatments, payment source and visit duration for patients. RESULT: One hundred and seventy practitioners were interviewed and 99 recorded data on a total of 1817 patient visits. Naturopathic physicians in Washington and Connecticut had similar demographic and practice characteristics. Both the practitioners and their patients were primarily White and female. Almost 75% of all naturopathic visits were for chronic complaints, most frequently fatigue, headache, and back symptoms. Complete blood counts, serum chemistries, lipids panels and stool analyses were ordered for 4% to 10% of visits. All other diagnostic tests were ordered less frequently. The most commonly prescribed naturopathic therapeutics were: botanical medicines (51% of visits in Connecticut, 43% in Washington), vitamins (41% and 43%), minerals (35% and 39%), homeopathy (29% and 19%) and allergy treatments (11% and 13%). The mean visit length was about 40 minutes. Approximately half the visits were paid directly by the patient. CONCLUSION: This study provides information that will help other health care providers, patients and policy makers better understand the nature of naturopathic care.

Is naturopathy as effective as conventional therapy for treatment of menopausal symptoms?

BACKGROUND: Although the use of alternative medicine in the United States is increasing, no published studies have documented the effectiveness of naturopathy for treatment of menopausal symptoms compared to women receiving conventional therapy in the clinical setting. OBJECTIVE: To compare naturopathic therapy with conventional medical therapy for treatment of selected menopausal symptoms. DESIGN: A retrospective cohort study, using abstracted data from medical charts. SETTING: One natural medicine and six conventional medical clinics at Community Health Centers of King County, Washington, from November 1, 1996, through July 31, 1998. PATIENTS: Women aged 40 years of age or more with a diagnosis of menopausal symptoms documented by a naturopathic or conventional physician. MAIN OUTCOME MEASURES: Improvement in selected menopausal symptoms. RESULTS: In univariate analyses, patients treated with naturopathy for menopausal symptoms reported higher monthly incomes ($1848.00 versus $853.60), were less likely to be smokers (11.4% versus 41.9%), exercised more frequently, and reported higher frequencies of decreased energy (41.8% versus 24.4%), insomnia (57.0% versus 33.1%), and hot flashes (69.6% versus 55.6%) at baseline than those who received conventional treatment. In multivariate analyses, patients treated with naturopathy were approximately seven times more likely than conventionally treated patients to report improvement for insomnia (odds ratio [OR], 6.77; 95% confidence interval [CI], 1.71, 26.63) and decreased energy (OR, 6.55; 95% CI, 0.96, 44.74). Naturopathy patients reported improvement for anxiety (OR, 1.27; 95% CI, 0.63, 2.56), hot flashes (OR, 1.40; 95% CI, 0.68, 2.88), menstrual changes (OR, 0.98; 95% CI, 0.43, 2.24), and vaginal dryness (OR, 0.91; 95% CI, 0.21, 3.96) about as frequently as patients who were treated conventionally. CONCLUSIONS: Naturopathy appears to be an effective alternative for relief of specific menopausal symptoms compared to conventional therapy.

Flight related tuberculosis contact investigations in the United States: comparative risk and economic analysis of alternate protocols.

BACKGROUND: In-flight transmission risk of Mycobacterium tuberculosis is not well defined, although studies suggest it is low. The impact of flight-related tuberculosis (TB) contact investigations (TBCIs) on TB prevention and control is not well established, and they compete for resources with activities with established benefits. We sought to determine the risks and cost-benefits of using more restrictive criteria in comparison to the Centers for Disease Control and Prevention (CDC) 2008 protocol for TBCIs. METHODS: The risk-benefits of a modified CDC protocol were analyzed in comparison to the 2008 CDC protocol using data from flight-related TBCIs conducted in the United States from 2007 through 2009. We predicted the numbers and characteristics of case-travelers that would be identified using each protocol's criteria, and results of the associated passenger-contacts' TB screening tests. The economic analysis compared the costs of TBCIs to avoided costs of TB treatment and mortality using a Return on Investment model. RESULTS: The estimated in-flight transmission risk using a modified CDC protocol was 1.4%-19% versus 1.1%-24% for the 2008 protocol. Numbers of TBCIs and immediate costs to health departments were reduced by half. Long-term cost-benefits were comparable. CONCLUSIONS: CDC's modified protocol appears to be a feasible alternative that will conserve public health resources without jeopardizing the public's health.

Influenza A(H1N1)pdm09 during air travel.

The global spread of the influenza A(H1N1)pdm09 virus (pH1N1) associated with travelers from North America during the onset of the 2009 pandemic demonstrates the central role of international air travel in virus migration. To characterize risk factors for pH1N1 transmission during air travel, we investigated travelers and airline employees from four North American flights carrying ill travelers with confirmed pH1N1 infection. Of 392 passengers and crew identified, information was available for 290 (74%) passengers were interviewed. Overall attack rates for acute respiratory infection and influenza-like illness 1-7 days after travel were 5.2% and 2.4% respectively. Of 43 individuals that provided sera, 4 (9.3%) tested positive for pH1N1 antibodies, including 3 with serologic evidence of asymptomatic infection. Investigation of novel influenza aboard aircraft may be instructive. However, beyond the initial outbreak phase, it may compete with community-based mitigation activities, and interpretation of findings will be difficult in the context of established community transmission.

Management and control of varicella on cruise ships: a collaborative approach to promoting public health.

BACKGROUND: In most years varicella is the vaccine-preventable disease most frequently reported to Centers for Disease Control and Prevention (CDC) by cruise ships. Since 2005, CDC has received numerous isolated case reports of varicella among crew members and has investigated varicella outbreaks aboard vessels sailing into and from US seaports. METHODS: CDC investigators reviewed electronic varicella case reports from 2005 to 2009 and outbreak reports from 2009 to characterize the response and control efforts implemented by cruise ships in accordance with CDC protocols. Outbreak reports from 2009 were manually reviewed for details of case identification, contact investigations, isolation and restriction of cases and contacts, respectively, and number of contacts administered varicella vaccine post-exposure by cruise lines. RESULTS: During 2005 to 2009, cruise ships reported 278 cases of varicella to CDC among predominantly male (80%) crew members, three-quarters of whom were residents of Caribbean countries, Indonesia, the Philippines, or India, and whose median age was 29 years. Cases were more commonly reported during spring and winter months. During 2009, cruise ships reported 94 varicella cases among crew members of which 66 (70%) were associated with 18 reported varicella outbreaks. Outbreak response included isolation of 66 (100%) of 66 cases, restriction of 66 (26%) of 255 crew-contacts, and administration of post-exposure vaccine to 522 close contacts and other susceptible crew members per standard CDC recommendations. DISCUSSION: Most cases reported to CDC during 2005 to 2009 were among non-US resident crew members. Overall, cruise lines sailing into North America have the onboard capability to manage varicella cases and outbreaks and appear responsive to CDC recommendations. Cruise lines should continue to implement CDC-recommended response protocols to curtail outbreaks rapidly and should consider whether pre-placement varicella immunity screening and vaccination of crew members is a cost-effective option for their respective fleet operations.

Three air travel-related contact investigations associated with infectious tuberculosis, 2007-2008.

BACKGROUND: The potential for transmission of Mycobacterium tuberculosis during air travel has garnered considerable attention in the media and among public health authorities due to high-profile cases of international travelers with infectious tuberculosis (TB). METHODS: During 2007 and 2008, state and local health officials were asked to locate and conduct diagnostic follow-up for airline passengers considered contacts of three travelers, two with multidrug-resistant (MDR) TB and one considered highly contagious, who undertook air travel while infectious with TB disease. RESULTS: Public health departments in 21 states located and evaluated 79 (60%) of the 131 passenger contacts identified; 52 (40%) were lost to follow-up. Eight (10%) contacts had a history of TB disease or latent TB infection and were not retested. Sixteen (23%) of 71 contacts tested had positive TB test results suggesting latent TB infection, 15 of whom were from countries reporting estimated TB disease rates of greater than 200 cases/100,000 persons. CONCLUSIONS: Passenger contacts' positive test results may represent prior TB infection acquired in their countries of residence or may be a result of new TB infection resulting from exposure during air travel.

Passenger behaviors during norovirus outbreaks on cruise ships.

BACKGROUND: Norovirus causes a majority of outbreaks of gastrointestinal (GI) illness on cruise ships calling on the United States. Control measures include patient isolation, hand washing, and facility closure. Little is known about the behaviors and practices of people who have become ill with norovirus GI illness compared to those who remained well during an outbreak. METHODS: Passenger surveys were distributed during three cruise ship outbreaks caused by norovirus. Surveys inquired about illness symptoms, ill contacts, illness reporting status, hand sanitation beliefs and practices, and availability of public hand sanitizer. A case was a passenger reporting three or more episodes of loose stool in a 24-hour period, three or more episodes of vomiting in a 24-hour period, or one or more episodes each of loose stool and vomiting in a 24-hour period. Controls reported that they were not ill during the cruise. RESULTS: In total, 1,323 responses were compared. All ships had passengers who were ill prior to embarkation. Most cases delayed or did not report their illness to the ship's infirmary because they did not believe it was serious (43%-70% of responses). Cases were less likely to believe that isolation was effective in preventing disease spread [Mann-Whitney-Wilcoxon (MWW) p value <0.0001]. Cases were less likely to believe that hand washing or hand sanitizer are effective means of preventing disease spread (MWW p values 0.002 and 0.04, respectively), wash their hands after restroom use (MWW p value 0.02), or believe that hand sanitizer was available for public use prior to/after knowing about an outbreak (MWW p values 0.002 and 0.03, respectively). CONCLUSIONS: Prevention and control of norovirus GI illness may be improved by routine screening of embarking passengers, education about GI illness and its impact on public health, a focus on improving hand-washing practices, and identification of public hand sanitizer dispensing locations.

Norovirus transmission on cruise ship.

An outbreak of norovirus gastroenteritis affected passengers on two consecutive cruises of ship X and continued on 4 subsequent cruises despite a 1-week sanitization. We documented transmission by food and person-to-person contact; persistence of virus despite sanitization onboard, including introductions of new strains; and seeding of an outbreak on land.

Outbreaks of acute gastroenteritis on cruise ships and on land: identification of a predominant circulating strain of norovirus--United States, 2002.

In 2002, a sharp increase in outbreaks of norovirus-associated illness, both on cruise ships and on land, encouraged us to examine the molecular epidemiology of detected noroviruses, to identify a common strain or source. Of 14 laboratory-confirmed outbreaks on cruise ships, 12 (86%) were attributed to caliciviruses; among these 12, outbreak characteristics included continuation on successive cruises in 6 (50%), multiple modes of transmission in 7 (58%), and high (>10%) attack rates in 7 (58%). Eleven of the 12 calicivirus outbreaks were attributed to noroviruses, 7 (64%) of which were attributed to a previously unreported lineage, provisionally named "the Farmington Hills strain." From May 2002 to December 2002, 10 (45%) of 22 land-based outbreaks also were attributed to this strain. Nucleotide-sequence analysis provided insights into norovirus transmission, by documenting links among outbreaks, the introduction of strains onto ships, and viral persistence on board (despite cleaning). Control measures for outbreaks should address all routes of transmission. Better outbreak surveillance and collection of data on sequences will help to monitor norovirus strains and to identify common sources.