Insights on Coronavirus Disease 2019 Epidemiology From a Historic Cruise Ship Quarantine

(See the Major Article by Plucinski et al on pages e448–57.)

On 20 January 2020, the Diamond Princess left Yokoyama, Japan, with >3700 passengers and crew members on board and embarked on a 2-week voyage. During the cruise, a severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2) outbreak occurred among the passengers and crew members, ultimately resulting in 712 confirmed coronavirus disease 2019 (COVID-19) cases with 13 deaths [1], the largest disease outbreak involving a cruise ship to date. As the ship docked in Yokohama on 3 February and subsequently entered ship-based quarantine, a massive public health response operation was initiated. A clinic was set up to manage and test symptomatic passengers and crew members. Transportation of critically ill passengers to hospitals across the metro area had to be arranged promptly, and medications for quarantined passengers needed to be reconciled before personal supplies ran out.

Some of the difficulties were unique to a cruise ship. Information on background health conditions was not available for all the passengers and crew members. Infection prevention and control training for crew members who continued to cater to the passengers during the quarantine proved to be a significant challenge. Furthermore, the ship needed to be moved offshore every 3 days to treat human waste, which interfered with multiple elements of the response operation. Despite these challenges, the event provided an unprecedented opportunity to gain insights into the epidemiology and transmission dynamics of SARS-CoV-2 in the context of a well-defined, isolated outbreak.

In this issue of Clinical Infectious Diseases, Plucinski and colleagues [2] highlight aspects of the SARS-CoV-2 epidemiology through detailed analyses of Americans aboard the ship, using in-depth surveys and viral genome sequencing methods. A key finding of the investigation is the rate of intracabin transmission during the quarantine period through careful observation of event timelines. Network/phylogeny analysis supported cabinmates as the primary source of transmission [3]. It can be inferred from this study that the ship-based quarantine that required passengers to stay inside their cabin limited further spread of the virus through intercabin, but not intracabin transmission.

The ideal approach to reduce the risk of intracabin transmission by isolating each person individually was deemed physically and operationally impossible, given the number of passengers and crew members aboard the ship. When individual isolation is not an option in the face of a large-scale outbreak like the one described here, the best alternative would be to isolate passengers or crew members in their own cabins with proper guidance on hand hygiene and droplet precaution to prevent intercabin transmission to the extent possible. On the Diamond Princess, announcements were made regularly to urge handwashing, and surgical masks were provided to all passengers and crew members by the quarantine team.

The report by Plucinski and colleagues [2] also supports probable SARS-CoV-2 transmission from asymptomatic cases. Because the analysis was conducted close to 2 weeks after repatriation, these asymptomatic cases can be ascertained to be truly asymptomatic, as opposed to presymptomatic. In this population, 21% of cases (14 of 66) were asymptomatic. Although the directionality of transmission among cabinmates was not clear because testing occurred only once in most instances, SARS-CoV-2 transmission from asymptomatic cases was strongly suggested, based on the attack rate for those with asymptomatic SARS-CoV-2–positive cabinmates (63%), which was significantly higher than that for those in single-person cabins or without SARS-CoV-2–positive cabinmates (18%), and closer to that for those with symptomatic SARS-CoV-2–positive cabinmates (81%).

Overall, the findings indicate that asymptomatic transmission through droplet played an important role in the outbreak, possibly in combination with environmental contamination [4], although the risk of asymptomatic tranmission may have been higher on the cruise ship than in other circumstances because of the nature of close contacts in small cabins for prolonged periods of time. Transmission from asymptomatic cases have previously been suggested, albeit at smaller scales [5]. From the public health perspective, the possibility that transmission of SARS-CoV-2 from asymptomatic cases is almost as likely as transmission from symptomatic cases necessitates reconsideration of how epidemiological links are established, which typically relies on testing of symptomatic people around the index case patient.

Investigation into the Diamond Princess outbreak provides further evidence of the case fatality ratio (CFR) of COVID-19 in isolation. The overall CFR reported from the outbreak was 1.8% (13 of 712). CFRs among hospitalized patients or those admitted to intensive care units have been reported previously but only in specific populations [6]. CFRs studied in the community are variable and rely heavily on active case finding of suspected cases and the testing strategy used [7]. The universal testing strategy in a closed cohort like the Diamond Princess should reflect the true case fatality rates of this disease in this population, which was older, multicultural, and active enough to travel on board compared with the population at large.

Epidemiological findings on COVID-19 are increasingly linked to information from whole-genome sequencing of SARS-CoV-2. In the current report, Plucinski and colleagues [2] found that the viruses from case patients in the same cabin only had 0–2 single-nucleotide variants, which supports the hypothesis of intracabin transmission, with transmission from a common source before quarantine also possible. The use of whole-genome sequencing analyses is critical in uncovering hidden links and their chronology within a transmission event. As documented in this report, field epidemiology and genomics are now fundamental components of outbreak investigation, and investment in both disciplines is needed if a country is to prepare for the next wave of emerging pathogens.

SARS-CoV-2 outbreaks have occurred on cruise ships after the Diamond Princess [8], which underscores the likelihood that we will continue to see cruise ship infectious disease events in the future, whether due to SARS-CoV-2 or to other emerging pathogens. Guidelines from the World Health Organization [9] and the US Centers for Disease Control and Prevention [10] are useful tools to prepare for and address cruise ship events, although they do not fully address how the recommendations should be implemented.

Some practical steps that could help cruise ships better prepare for future large-scale infectious disease events when they are allowed to sail again include requesting passengers and crew members to register their health conditions, including underlying diseases and medications before embarkation, stockpiling sufficient personal protective equipment on board, and providing essential knowledge and training on infection prevention and control to crew members. The accumulating knowledge on the historic Diamond Princess outbreak brings new insights into the epidemiology of COVID-19 and should guide improved readiness toward future infectious disease events involving cruise ships.

Notes

Financial support. This work was supported by the National Institutes of Health (grants R01AI104895, R21AI151362, and R21AI135522 to Y. D.).

Potential conflicts of interest. Y. D. has consulted for Gilead, Shionogi, Janssen, Entasis, VenatoRx, and bioMerieux; received speaking fees from Merck Sharp & Dohme; and received research funding from Merck Sharp & Dohme, Astellas, Shionogi, Pfizer, Janssen, bioMerieux, and Kanto Chemical. T. Y. certifies no potential conflicts of interest. Both authors have submitted the ICMJE Form for Disclosure of Potential Conflicts of Interest. Conflicts that the editors consider relevant to the content of the manuscript have been disclosed.