3

Disease Control and Response Efforts

The core function of the Division of Global Migration and Quarantine (DGMQ) and its network of quarantine stations is the control of communicable human disease. Infectious disease threats are extremely varied in terms of virulence, severity, transmission potential, epidemic potential, and potential public health consequences. Disease control tools used by the DGMQ have common themes, but also are tailored to the specific threats based on these variables. Over the past two decades, the pace and variance of infectious disease threats to the United States have been accelerating at an alarming rate. This likely reflects a range of factors including greater ease of travel, increasing speed and range of international travel, escalating emergence of novel pathogens, and improved communication and diagnostic tools.

THE DGMQ’S ROLES AND RESPONSIBILITIES IN COMMUNICABLE DISEASE CONTROL

The DGMQ has a range of domestic and international roles in its responsibility for controlling the spread of communicable diseases at both international air and maritime ports of entry and at land-border crossings.¹ The DGMQ’s day-to-day responsibilities focus on responding to travelers, animals, human remains, and products that may have specific communicable diseases of public health concern upon their entry to the United

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¹ More information about the DGMQ’s roles and responsibilities is available from https://www.cdc.gov/ncezid/dgmq/how-we-serve.html (accessed March 15, 2022).

States by air, sea, or land.² When major communicable disease threats emerge within the United States or abroad—such as outbreaks of potential or definite pandemic potential—the DGMQ can leverage its existing partnerships and expand its ordinary operations and activities as part of the emergency response to help prevent the introduction and spread of disease into the United States or across its borders. In recent decades, the DGMQ has supported infection control efforts for a broad range of communicable diseases, such as tuberculosis (TB)—including both multidrug-resistant tuberculosis (MDR-TB) and extensively drug-resistant TB (XDR-TB)—Ebola virus disease, Zika virus disease, Lassa fever, measles, chikungunya virus disease, monkeypox, rabies, extensively drug-resistant typhoid, the 2009 H1N1 influenza pandemic, Middle East respiratory syndrome (MERS)CoV, SARS-CoV-1 (the virus that causes severe acute respiratory syndrome [SARS]), SARS-CoV-2 (the virus that causes COVID-19), and cholera.

The DGMQ’s Day-to-Day Activities

The DGMQ’s day-to-day responsibilities generally pertain to individual travelers and are primarily aimed at responding to communicable diseases of public health concern in arriving travelers, as well as importations that pose a potential public health threat. For individual travelers, the DGMQ’s suite of infectious disease control tools includes public health travel restrictions—specifically the Do Not Board (DNB) list and the Public Health Lookout—and contact investigations, and issuance of public health orders for quarantine, isolation, or conditional release when necessary. Though the DGMQ’s overall mission encompasses many areas of prevention, including travel health advice and vaccine recommendations, this section will focus on disease control measures.

Air Travel Responsibilities

Airlines and U.S. Customs and Border Protection (CBP) also play critical roles in detecting and responding to ill travelers and containing the spread of communicable diseases. These activities are maintained between outbreak or pandemic periods and may be scaled up during a global pandemic. Staff at quarantine stations may be notified of potentially ill travelers before, during, or after travel. When quarantine station staff are notified of an ill traveler, they communicate with quarantine medical officers, who guide staff on the actions necessary to appropriately mitigate communicable diseases risks. The appropriate steps to mitigate this risk will depend on

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² This text was modified after release of the report to the study sponsor to correctly represent the division’s responsibilities.

whether the CDC is notified before, during, or after travel. Quarantine station staff enter the information regarding the ill traveler(s) and any actions taken into the secure Quarantine Activity Reporting System (QARS).

For passengers identified before travel or during travel, health departments may ask to have travelers added to the DNB list and the Public Health Lookout if they meet established criteria—that is, if they are reasonably believed to be infectious with or at risk of becoming infectious with a communicable disease of public health importance that poses a risk to the traveling public and are at risk for travel, or are not adherent to public health recommendations, or are unaware of their diagnosis. More information is provided in the Travel Restrictions section, which follows.

Ill (or dead) travelers identified during travel can include passengers or crew identified while on board conveyances or travelers identified at transportation hubs by federal and nonfederal partners. If an air passenger is observed with signs of illness that meet the Centers for Disease Control and Prevention’s (CDC’s) regulatory definition, or a death occurs on board, the pilot of the aircraft must report the situation to the CDC quarantine station with jurisdiction for the arrival airport.³ Before the aircraft lands, the pilot must provide details such as aircraft identification, the departure airport, the destination airport, estimated time of arrival, number of persons on board the aircraft, number of suspected case(s) on board, and the nature of the public health risk if it is known. If the CBP or other partners identify an ill traveler upon arrival, they may also notify the quarantine station with jurisdiction. The CDC provides CBP officers and other airport partners, including emergency medical services, with job aids (i.e., “RING” cards that remind CBP officers to Recognize, Isolate, Notify, and Give support) to support this function. This partnership is especially important at airports where the DGMQ does not have staff on site.

The Quarantine and Border Health Services Branch (QBHSB) also works closely with CBP personnel at designated foreign airports where travelers are inspected by the CBP prior to boarding U.S.-bound flights (i.e., preclearance ports of entry) to ensure consistent application of CDC regulatory requirements for these travelers and any CDC-regulated items they may attempt to import. This work is performed remotely and primarily consists of periodic outreach and the provision of job aids.

Quarantine stations may also receive reports, typically from health departments, for travelers who were diagnosed with communicable diseases after travel. Quarantine station staff will work with quarantine medical officers to determine whether a contact investigation should be initiated.

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³ More information about the CDC’s protocol for reporting onboard deaths and illnesses is available from https://www.cdc.gov/quarantine/air/reporting-deaths-illness/guidance-reporting-onboard-deaths-illnesses.html (accessed February 22, 2022).

More information on the Electronic Passenger Reporting System used for contact investigations is reported in a separate section, which follows.⁴ In 2019, the Council of State and Territorial Epidemiologists (CSTE), with support from the CDC, evaluated reports to the DGMQ of infectious travelers in order to assess processes that state and local epidemiologists use to report ill travelers with diseases of public health concern to the QBHSB. The CSTE identified areas for improvement for both state and territorial epidemiologists and the CDC’s DGMQ (Council of State and Territorial Epidemiologists, 2020).

The DGMQ also supports efforts with partners to develop Communicable Disease Response Plans (CDRPs), which provide the basis for a multisector and multistate response to a public health disaster/emergency at ports of entry. This is accomplished through federal regulatory enforcement at ports of entry and by supporting local, state, and tribal public health agencies during domestic travel communicable disease responses, as requested, to prevent the introduction, transmission, or spread of communicable diseases.

Federal Public Health Travel Restrictions

Two public health tools for communicable disease control used by federal authorities are the DNB list and the Public Health Lookout.⁵ These tools—managed jointly by the U.S. Department of Homeland Security (DHS) and the CDC—were established in 2007. The DNB list prevents individuals known or suspected to have a communicable disease that poses a public health threat from being issued a boarding pass for any commercial airplane traveling into, within, or out of the United States. Additionally, to facilitate public health notification, these individuals are also issued a Public Health Lookout to allow them to be identified if they seek entry to the United States at an airport, land, or sea port of entry.⁶

In cases where an individual who poses a public health risk intends to travel, local and state public health authorities can request assistance from the CDC to ensure that the individual does not travel while still infectious.⁷ Individuals may be placed on the DNB list and issued a Lookout if they are

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⁴ See Protecting Travelers’ Health from Airport to Community: Investigating Contagious Diseases on Flights | Quarantine | CDC https://www.cdc.gov/quarantine/contact-investigation.html (accessed April 3, 2022).

⁵ More information about these travel restriction tools is available from https://www.cdc.gov/quarantine/travel-restrictions.html (accessed March 15, 2022).

⁶ See https://www.federalregister.gov/documents/2015/03/27/2015-07118/criteria-for-requesting-federal-travel-restrictions-for-public-health-purposes-including-for-viral (accessed May 21, 2022).

⁷ See https://www.cdc.gov/quarantine/travel-restrictions.html (accessed May 21, 2022).

“known or believed to be infectious with, or at risk for, a serious contagious disease that poses a public health threat to others during travel” and meet at least one of the following three criteria: (1) the individual is not aware of the diagnosis or not following public health recommendations, (2) the individual is likely to travel on a commercial flight involving the United States or travel internationally by any means, or (3) a travel restriction needs to be issued to respond to a public health outbreak or to help enforce a public health order (CDC, 2022f). The CDC reviews the records of all individuals subject to these restrictions every 2 weeks to assess their eligibility for removal of restrictions. After public health authorities determine that an individual is no longer infectious or at risk of becoming infectious, the person’s information is removed from both tools (CDC, 2022f).

During the COVID-19 pandemic, these federal public health tools have been used to restrict travel by individuals with COVID-19 and their close contacts who are recommended to quarantine. These authorities can also be utilized to restrict travel by individuals with other suspected or confirmed infectious diseases that could threaten public health during travel. Before the COVID-19 pandemic, most uses of federal public health travel restrictions were for people with infectious TB; however, the tools have also been used for measles, MERS, Ebola virus disease, and Lassa fever.⁸

When an individual on the Public Health Lookout enters the United States, the CDC is notified by CBP officers at the point of entry; a public health evaluation is then performed prior to the individual’s release (DeSisto et al., 2015). The CDC’s Quarantine Public Health Officers are responsible for (1) notifying the relevant local and state public health authorities that an individual on the Public Health Lookout has been identified and (2) working with local and state authorities to conduct the appropriate public health interventions, including isolation, coordinated treatment referral, and compliance with any established federal and state legal measures (CDC, 2022f; DeSisto et al., 2015).

The DNB and Lookout lists have been most commonly used for people with suspected or confirmed infectious TB, including MDR-TB. TB is a curable, preventable, but potentially serious infectious disease that is not highly transmissible. However, an individual with active (i.e., infectious) pulmonary TB can transmit the disease during periods of prolonged close contact, such as air travel (Martinez et al., 2010). Despite federally mandated overseas TB screening for immigrants and refugees, the CDC reports that there are about 125 active TB cases per year among arriving travelers including visitors, students, and temporary workers (Kim et al., 2012). The escalating rates of MDR-TB and XDR-TB warrant major concerns regard-

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⁸ See https://www.cdc.gov/quarantine/travel-restrictions.html (accessed May 21, 2022).

ing transmission into the United States at both air and land-border points of entry (Salzer et al., 2016).

Health screenings also occur at quarantine stations to assess passengers for illness who may not be on a DNB or Public Health Lookout. This form of surveillance can vary depending on context, such the event of a public health emergency. During the West Africa Ebola outbreak of 2014–2016, passengers from affected countries went through exit screening prior to leaving the country.⁹ This included temperature checks, answering health questions, and visual assessment for illness. Those who arrived in the United States were subject to entry screening. Passengers who had traveled through Guinea, Sierra Leone, or Liberia underwent screenings that included answering questions about potential risk, temperature checks, and observation for other Ebola symptoms. Staff at all U.S. international airports were trained to respond to any reports of ill travelers (CDC and DHS, 2014).¹⁰ During the COVID-19 pandemic, regulations surrounding screenings changed throughout the course of the pandemic. In February 2020, all incoming flights from China were directed to 11 U.S. airports. At these airports, “[i]ncoming passengers [were] screened for fever, cough, and shortness of breath. Any travelers with signs or symptoms of illness receive[d] a more comprehensive public health assessment” (Jernigan, 2020). As of December 6, 2021, prior to boarding a flight bound for the United States, international travelers must show either (1) documentation of a recent negative COVID-19 test or (2) documentation of recent recovery from COVID-19 infection with a physician’s note clearing the passenger for travel (U.S. Department of State, 2022).

The challenge of passenger screening and enacting public health measures is highlighted by the increase in the number of travelers to the United States over the past several years. The number of international arrivals in U.S. airports increased from about 80 million in 2006 to about 120 million in 2019. These numbers dropped to ~30 million in 2020 and 20 million in 2021 (Maskery, 2022). The volume of travelers arriving via land borders does not demonstrate as significant a change, but still represents a large population that requires screening. International land border arrivals have gone from a high of nearly 300 million in 2006 to approximately 210 million in 2011. Numbers of arrivals ranged from 210 to 250 million between 2011 and 2019. This number dropped to 115 million in 2020, and rose only slightly to 130 million in 2021 as a result of restricted travel due to the COVID-19 pandemic (Maskery, 2022). The COVID-19 pandemic also resulted in a drastic increase in the number of illnesses detected in airports that warranted

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⁹ This text was modified after release of the report to the study sponsor to clarify which departing passengers were screened.

¹⁰ This text was modified after release of the report to the study sponsor to specify which international airports had staff trained to respond to ill travelers.

responses. From 2016–2019, annual responses ranged from 1,300 to 1,500 responses before, during, or after travel. This number soared to over 35,000 in 2020, and to near 90,000 in 2021 (CDC, 2022f; Maskery, 2022).

Contact Investigations

Contact investigations are another tool used by the CDC and DGMQ to protect the health of individuals who have been exposed to an infectious disease during air travel and to prevent the forward spread of that disease in communities.¹¹ Historically, most flight contact investigations are conducted by the CDC in close coordination with state and local public health authorities for cases of infectious TB, measles, rubella, pertussis, meningococcal disease, and more recently for COVID-19. The CDC typically notifies state, tribal, local, and territorial (STLT) authorities about exposed persons in their jurisdictions and health departments then notify identified persons of their exposures and put in place appropriate disease control plans, including provision of post-exposure prophylaxis or vaccine when indicated.

A contact investigation is typically triggered after the CDC is notified by state or local public health authorities that an air traveler (i.e., the index patient) has sought treatment at a medical facility and has been diagnosed with a specific infectious disease, which can happen up to days or weeks after travel. In other situations, the CDC may be notified about an ill traveler who is currently on a plane, or has recently landed. The CDC is responsible for coordinating contact investigations on domestic flights, arriving international flights, land-border crossings, and cruises that were taken by the index patient.¹² Quarantine public health officers in consultation with the Quarantine Medical Officer evaluate whether the index patient was contagious during the flight and may have potentially exposed passengers seated nearby (i.e., contacts).¹³ The CDC then requests the flight manifest¹⁴ for those contacts and shares the passengers’ information with the relevant state, local, or international public health authorities, who in turn try to locate the passengers to inform them about their potential exposure and recommended actions.

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¹¹ More information about CDC contact investigations is available from https://www.cdc.gov/quarantine/contact-investigation.html (accessed March 15, 2022).

¹² This text was modified to correct the characterization of CDC’s responsibilities for contact investigations.

¹³ This text was modified after release of the report to the study sponsor to correctly describe who conducts the evaluations.

¹⁴ The CDC protects passenger privacy and does not release any information about the index patient or the contacts beyond public health staff working on the investigation. This information is protected and its access is strictly limited to public health use (https://www.cdc.gov/quarantine/contact-investigation.html, accessed May 21, 2022).

Isolation and Quarantine

In relatively rare instances, the federal government exercises its legal authorities¹⁵ to implement isolation and quarantine to help prevent the public’s exposure to an individual who has or may have specific infectious diseases of great public health risk (CDC, 2021c). Isolation and quarantine functions differ, in that isolation separates individuals who are sick with a designated infectious disease of consequence from individuals who are not sick. The quarantine function separates and restricts the movement of people who were exposed to an infectious disease, in order to observe (or monitor) them to see if they become sick and to prevent them from exposing others during the period of time that they are potentially infectious.

An executive order of the president authorizes federal isolation and quarantine for a specific set of infectious diseases; this list can also be revised by the president through executive order. Currently, isolation and quarantine are federally authorized for cholera, diphtheria, infectious tuberculosis, plague, smallpox, yellow fever, viral hemorrhagic fevers, severe acute respiratory syndromes, novel influenza strains with pandemic potential, and measles.

The U.S. Department of Health and Human Services (HHS) has delegated the federal authority¹⁶ to carry out isolation and quarantine functions to the CDC. If an individual has a suspected or confirmed case of one of the designated infectious diseases, the CDC can issue a federal isolation or quarantine order. An individual may be conditionally released from quarantine subject to compliance with medical monitoring and surveillance. Breaking a federal quarantine order is punishable by fines and imprisonment. In most scenarios, these orders are enforced with support from partners, such as federal, state, tribal, and/or local public health authorities; law enforcement officers; U.S. CBP officers; and U.S. Coast Guard officers.

Despite these authorities, individual federal isolation and quarantine powers are rarely used in practice and have been used even less frequently at large scale. There is generally heavy reliance on state and local health authorities to issue orders for isolation and quarantine. State and local officials usually have policies, procedures, staff, and structure in place to enforce these orders. Across the DGMQ’s network of quarantine stations, infectious TB was the most frequently occurring infectious disease for

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¹⁵ The authority for isolation and quarantine derives from the Commerce Clause of the U.S. Constitution. Under section 361 of the Public Health Service Act (42 U.S. Code §264), the U.S. secretary of Health and Human Services is authorized to take measures to prevent the entry and spread of communicable diseases from foreign countries into the United States and between states. Isolation and quarantine also are considered “police power” functions that are derived from the state’s right to take action affecting individuals for the benefit of society.

¹⁶ Under 42 Code of Federal Regulations parts 70 and 71, the CDC is authorized to detain, medically examine, and release persons arriving into the United States and traveling between states who are suspected of carrying these communicable diseases.

which federal individual isolation was authorized between 2007 and 2012 (Kim et al., 2012). Local health jurisdictions in most states also have the authority to enact disease control measures, including imposing isolation, in response to reports of TB (CDC, 2012).

Immigrant, Refugee, and Migrant Screening Responsibilities

In addition to supporting efforts to curb the spread of infectious disease at U.S. ports of entry, the DGMQ is also responsible for preventing the importation of infectious diseases into the United States by protecting the health of incoming U.S.-bound immigrants, refugees, and asylum seekers (CDC, 2021e).¹⁷ The DGMQ’s Immigrant, Refugee, and Migrant Health (IRMH) Branch¹⁸ works with a range of federal interagency partners, governments, and other organizations to promote the health of immigrants, U.S.-bound refugees, and migrants and to bolster health systems to prevent disease spread across international borders.

HHS has the regulatory authority to promulgate regulations that establish requirements for the medical examination of immigrants, refugees, and nonimmigrants required to have an examination prior to admission to the United States.¹⁹ Under this authority, the DGMQ administers regulations regarding health-related conditions that determine ineligibility for entry into the country. They have established systems for cohorts, such as overseas screening programs, treatment protocols, and vaccination requirements (Ortega et al., 2011). All immigrants and refugees entering the United States receive mandatory medical examinations, which includes TB screening conducted by panel physicians in over 150 countries. In addition, refugees are

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¹⁷ An immigrant is any individual legally admitted to the United States as a lawful permanent resident. A refugee is defined as “any person who is outside the country of such person’s nationality or, in the case of a person having no nationality, is outside any country in which such person last habitually resided. In addition, it is a person who is unable or unwilling to return to, and is unable or unwilling to avail himself or herself of the protection of, that country because of persecution, or a well-founded fear of persecution, on account of race, religion, nationality, membership in a particular social group, or political opinion.” A migrant is an individual who temporarily or permanently moves away from their place of usual residence, either within a country or across an international border. An asylum seeker is an individual who is seeking protection within the United States due to having suffered or having a well-founded fear of suffering persecution due to their race, religion, nationality, membership in a particular social group, or political opinion. (Source: https://www.uscis.gov/humanitarian/refugees-and-asylum/asylum, accessed April 29, 2022.)

¹⁸ More information about the work of the Immigrant, Refugee, and Migrant Health (IRMH) Branch is available from https://www.cdc.gov/ncezid/dgmq/focus-areas/irmh.html (accessed March 15, 2022).

¹⁹ Title 8: Aliens and Nationality and Title 42: The Public Health and Welfare of the U.S. Code and relevant supporting regulations at Title 42 Public Health in the Code of Federal Regulations (CFR). (Source: https://www.cdc.gov/immigrantrefugeehealth/laws-regulations.html, accessed March 15, 2022.)

provided with public health interventions such as vaccination and parasitic treatment programs. Health records from these activities are provided to U.S. state and local health departments and screening clinics along with notifications of the arrival of all refugees and the subset of immigrants with health conditions for which medical follow-up is recommended.²⁰

As of 2012, four quarantine stations at U.S. ports of entry were responsible for meeting and providing a TB-clinic referral to immigrants who had been diagnosed with admissible TB conditions during their pre-immigration medical examination. A study found that immigrants with noninfectious TB who received such referrals—the costs of which are typically covered by state and local health departments—were about four times more likely to engage in follow-up evaluation than those who did not (Kim et al., 2012). For newly arrived immigrants with prior TB infection or previously treated active disease, follow-up care is particularly critical, due to their heightened risk of developing or redeveloping active disease during the first years after they arrive. In 2018, the DGMQ, in collaboration with U.S. Department of State (DOS), launched the U.S. version of eMedical. This is a system for processing overseas medical examination data for immigrants. Panel physicians in the countries in which the examinations are performed enter data directly into the eMedical system, and the data are transferred to the DGMQ’s Electronic Disease Notification system within 2 days of the immigrant’s arrival in the United States. The substantial reduction in record-processing time increases the likelihood that health departments will be able to initiate timely follow-up with new-arrival immigrants relative to the earlier paper-based systems (Phares et al., 2022). As a result, the QBHSB staff are less involved with meeting immigrants and refugees since the notifications to health departments are automated.

In 2009, the CDC revised the vaccination criteria for U.S. immigration to align with the criteria for vaccines recommended by the Advisory Committee on Immunization Practices (ACIP) to determine which vaccines are required for immigrants to the United States. According to these vaccination criteria, the vaccine must (1) be age appropriate for the immigrant applicant, (2) protect against a disease that has the potential to cause an outbreak, and (3) protect against a disease that has been or is in the process of being eliminated in the United States.²¹ The responsibilities of the IRMH Branch are illustrated in Box 3-1.

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²⁰ More information about these activities is available from https://www.cdc.gov/immigrantrefugeehealth/about-irmh.html, https://www.cdc.gov/immigrantrefugeehealth/riise-project.html, and https://www.cdc.gov/immigrantrefugeehealth/Electronic-Disease-Notification-System.html (accessed March 15, 2022).

²¹ More information about CDC’s revised criteria for vaccination for immigration is available from https://www.cdc.gov/immigrantrefugeehealth/laws-regs/vaccination-immigration/revised-vaccination-criteria-immigration.html (accessed March 15, 2022).

Land-Border Crossing Responsibilities: U.S.–Mexico Border

The DGMQ’s United States–Mexico Unit (U.S. MU) plays a major role in preventing the transmission of infectious diseases across the nation’s land-border crossings at the U.S.–Mexico border. To execute these responsibilities, the CDC and DGMQ collaborate with U.S. and Mexico health officials at the local, state, and federal levels to support efforts to (1) limit the cross-border spread of infectious diseases, (2) protect the health of people living in the U.S.–Mexico border region, and (3) promote the health of travelers,

migrants, and other mobile populations.²² Housed within U.S. M.U. is the CureTB program that works with states and local jurisdictions across the United States to assist in continuity of care for mobile patients with tuberculosis who intend to travel outside the United States prior to treatment completion, by linking them to TB services in destination countries. The program also accepts referrals from international sources requesting continuity of care linkages for TB patients planning travel to the United States.²³ CureTB also uses their international connections to assist quarantine stations and the Travel Restriction and Interventions Activity to determine when people can be removed from the DNB list and Public Health Lookout prior to U.S. reentry.

The QBHSB is responsible for preventing the transmission of communicable diseases across the nation’s northern border crossings along the U.S.–Canadian border. Although the QBHSB does not have staff physically present along the northern border, these activities are executed remotely by the airport-based quarantine stations located in Boston, MA (BOS), New York, NY (JFK), Detroit, MI (DTW), Minneapolis, MN (MSP), and Seattle, WA (SEA). These specific quarantine stations partner with the CBP and STLT health jurisdictions to ensure plans are in place and understood to provide for consequence management should ill travelers or CDC-regulated goods be detected at the U.S.–Canadian border.

In the United States, people of international origin have a higher rate of TB than the U.S.-born population, with those born in Mexico representing the majority of new TB cases between 1993 and 2015 (DeSisto et al., 2015). In 2015, about two-thirds of TB cases among internationally born individuals occurred in the border states of California, Texas, Arizona, and New Mexico (DeSisto et al., 2015). Given that more than 159 million individuals entered the United States at the land-border crossing with Mexico in 2012, for example, the U.S.–Mexico interface creates prime conditions for the transmission of TB across the border, which requires coordinated cross-border follow-up and control strategies (DeSisto et al., 2015).

A study evaluated the use of DNB and Lookout lists to detect and refer back to treatment individuals with infectious or potentially infectious TB crossing the U.S.–Mexico land border between 2007 and 2013 (DeSisto et al., 2015). Most cases were Hispanic, male citizens of the United States or Mexico, more than 30 percent of whom were undocumented migrants and about 20 percent of whom had MDR-TB. Nearly two-thirds of the cases were located and treated due to their placement on the list, but about

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²² More information about the work of DGMQ’s U.S.–Mexico Unit is available at https://www.cdc.gov/ncezid/dgmq/focus-areas/usmh.html (accessed March 16, 2022).

²³ More information on the CureTB Program is available from https://www.cdc.gov/usmexicohealth/curetb.html (accessed May 10, 2022).

one-quarter—mainly undocumented migrants—were lost to follow-up. The authors suggested several strategies to improve the effectiveness of the Public Health Lookout tool at the U.S.–Mexico border, including (1) using the tool earlier for binational individuals who are at risk of progressing to infectious TB due to treatment nonadherence and are likely to travel across the border, (2) training U.S. CBP officers to contact the CDC if they locate undocumented migrants who are on the Public Health Lookout, and (3) collaborating with Immigration and Customs Enforcement (ICE) on TB referral projects and resources (DeSisto et al., 2015).

Maritime Responsibilities

The maritime industry presents unique public health challenges due to the thousands of ships that make calls at U.S. ports each year, the number of passengers on cruise ships, and crew members often arriving from countries with suboptimal vaccination coverage (CDC, 2011). The CDC is responsible for addressing disease outbreaks on both cruise ships and noncruise ships. Federal regulations authorize the CDC to conduct public health prevention measures at U.S. ports of entry to prevent the introduction and spread of communicable diseases. The agency issues guidance and orders for ships to follow in reducing the risk of disease transmission and in responding to illnesses suggestive of communicable diseases (CDC, 2020, 2022c). International conveyances traveling to the United States are required to report all onboard deaths and illnesses meeting the CDC’s regulatory definition to the CDC (CDC, 2021b). Between 2010 and 2014, the DGMQ’s quarantine stations received almost 3,000 individual maritime case reports of illnesses (77 percent of reports) and deaths (23 percent) (Stamatakis et al., 2017). The most frequent illness reported was varicella (36 percent) and the most common causes of death were cardiovascular or pulmonary-related conditions (80 percent).

In September and October of 2019 the CDC’s Vessel Sanitation Program was notified of three outbreaks of acute gastroenteritis that proved to be norovirus on cruise ships (Rispens et al., 2020). The CDC surveyed passengers, collected and tested specimens to confirm norovirus, partnered with the Food and Drug Administration (FDA) to test food samples for the virus, and determined the source of contamination from a berry supplier in China. Cruises continued to operate as normal during the outbreak, and no known land transmission was reported to be linked. The CDC coordinates CaliciNet, a national network of federal, state, and local public health laboratories that conduct norovirus surveillance activities (CDC, 2019b).

As discussed in Chapter 5, the CDC coordinated a number of mitigation efforts during the COVID-19 pandemic. On March 14, 2020, a No Sail Order issued by the CDC went into effect (CDC, 2022g) that ceased

operations of cruise ships in waters under U.S. jurisdiction. The order also required cruise ship operators to develop comprehensive plans for preventing, monitoring, and responding to COVID-19. On October 30, 2020, the CDC lifted the No Sail Order and instituted the Framework for Conditional Sailing Order that was in place from November 1, 2020, to January 15, 2022. This framework involved a phased approach of testing, screening, and simulation measures required to obtain a COVID-19 Conditional Sailing Certificate. The certificate would enable a cruise ship operator to resume passenger operations. On January 29, 2021, the CDC issued an order requiring that all people—including both passengers and employees—on public transportation conveyances or on the premises of transportation hubs wear face masks (Federal Register, 2021). In February 2022 all cruise lines were required to either participate or formally opt out of the CDC COVID-19 Program for Cruise Ships (CDC, 2022b). This program provides travelers with color-coded status for cruise ships to inform travel choices. Travelers can review data such as the number of COVID-19 cases a ship has reported, the public health measures a ship is taking, and whether a ship warranted investigation or has opted out of the program.

Responsibilities for Animals

The DGMQ is responsible for regulating the entry of certain animals and products of animal origin into the United States and restricting animal products that could be harmful to humans (CDC, 2021f). Quarantine stations are charged with inspecting CDC-regulated animals and animal products that pose a potential threat to human health. For example, in 2021 the CDC suspended the importation of dogs from 113 countries classified as being at high risk for dog rabies after experiencing an increase in the number of canines arriving with incomplete vaccination documentation (CDC, 2022e; Cima, 2021). The CDC has estimated that approximately 1.06 million dogs are imported into the United States each year, with 700,000 arriving via air travel and 360,000 at land-border ports of entry. The CDC and U.S. Department of Agriculture (USDA) both regulate the entry of dogs, with the USDA and CBP being the only agencies that track the purpose of importation for a subset of dogs. The CDC requires all dogs arriving in the United States to be healthy upon arrival. Additionally, dogs from countries at high risk for canine rabies virus variant are denied entry if they arrive without proper documentation of rabies vaccination or without a CDC-issued permit. The USDA has additional regulations if the intent of importation is for resale purposes (USDA, 2019). Additionally, the DGMQ carries out federal quarantine regulations that prohibit the importation of nonhuman primates as pets due to their ability to transmit TB and other pathogens to humans (CDC, 2022a). All nonhuman primates that enter the United States are inspected by the DGMQ, with 33,818 nonhuman

primates imported in FY2019 (Galland, 2021). All nonhuman primates imported into the United States are held in a CDC-approved quarantine facility for at least 31 days and are tested for TB and monitored for symptoms of disease. If a nonhuman primate dies during the quarantine period, the cause of death will be determined through an animal autopsy and series of diagnostic tests (CDC, 2022d). The CDC prohibited the importation of rodents of African origin into the United States due to an importation-related outbreak of monkeypox in 2003 (CDC, 2015a). The CDC also regulates the importation of bats,²⁴ turtles,²⁵ and civets²⁶ due to the association these animals have with previous outbreaks of disease in human populations.

To this date, there is no evidence suggesting that animals play a significant role in the transmission of the SARS-CoV-2 virus to humans. However, studies show that many animals can be infected with the virus although reported transmission from animals to humans have been rare.²⁷ Future studies are needed to further investigate the transmission of the virus from animals to humans. Modeling studies could be utilized to better understand possible scenarios of transmission. There is the potential that canine and other exotic pet imports will increase due to the growing U.S. demand. Therefore, continued vigilance will be essential with the possibility of new zoonotic disease threats emerging beyond canine rabies.

Human Remains

The CDC regulates the importation of biologics and human remains, which are coregulated by the Division of Select Agents and Toxins (DSAT) and the DGMQ. The DGMQ will respond to inquiries at ports of entry for biologic shipments (any shipment containing human or CDC-regulated animal tissues, body fluids, blood, etc.) and human remains that do not meet U.S. importation requirements, such as those with inadequate documentation or packaging violations. In 2020, the DGMQ and the DSAT updated the human remains importation regulation to provide clarification regarding the definition of human remains and that hermetically sealed caskets were no longer required as long as the remains were packaged in a leak-proof container.²⁸

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²⁴https://www.cdc.gov/importation/bringing-an-animal-into-the-united-states/bats.html (accessed May 10, 2022).

²⁵https://www.cdc.gov/importation/bringing-an-animal-into-the-united-states/turtles.html (accessed May 10, 2022).

²⁶https://www.cdc.gov/importation/bringing-an-animal-into-the-united-states/civets.html (accessed May 10, 2022).

²⁷https://www.cdc.gov/coronavirus/2019-ncov/daily-life-coping/animals.html (accessed May 10, 2022).

²⁸ More information about CDC’s human remains importation requirements is available at https://www.cdc.gov/importation/human-remains.html (accessed May 10, 2022).

The DGMQ’s Emergency Response Activities

The DGMQ’s network of quarantine stations and existing partnerships with federal, STLT, and international agencies and public health authorities is envisioned to scale to support emergency responses to emerging and ongoing infectious disease threats within the United States and abroad.²⁹

In situations of a localized outbreak of concern in another country or region of the world, the DGMQ supports the CDC’s efforts to stop outbreaks where they begin and help prevent infectious diseases from spreading across borders. In response to the West Africa Ebola outbreak (2014–2016), the DGMQ deployed personnel to support border health measures to reduce the risk of exportation and translocation of disease.³⁰ Specifically, the DGMQ provided technical support to strengthen airport exit screening for outbound travelers in the Ebola-affected countries. These activities were conducted in coordination with those countries, the World Health Organization, and the International Organization for Migration. After two case importations into the United States, the DGMQ worked with the DHS to conduct public health risk assessments of incoming travelers from the Ebola-affected countries for travelers funneled to selected airports with CDC Quarantine Stations. At these stations (Atlanta, New York, Newark, Washington, DC-Dulles, and Chicago), CDC and DHS staff conducted reviews of traveler health declaration forms, symptom screening, temperature checks, and visual inspections, and collected contact information that was shared with health departments in destination locations to facilitate recommended post-arrival monitoring.

This is particularly critical for outbreaks that could have hugely deleterious consequences if cases were imported into the United States, such as during the Ebola epidemic in Western Africa in 2014–2015. Diseases with potential or definite pandemic potential, such as a novel influenza strain with early evidence of human–human transmission and COVID-19, represent an even more substantial threat to the health of all populations worldwide, thus supporting a rapid and effective emergency response soon after outbreak detection (CDC, 2021d).

Emergency Response and Active Monitoring for Ebola Epidemic in West Africa

As part of the CDC’s response to the Ebola epidemic in West Africa—a major global health emergency—the DGMQ and its quarantine station

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²⁹ More information about CDC’s emergency response activities is available from https://www.cdc.gov/ncezid/dgmq/emergency-response.html (accessed March 16, 2022).

³⁰ Travel and Border Health Measures to Prevent the International Spread of Ebola. MMWR Supplements, July 8, 2016, 65(3):57–67.

network supported a range of disease control efforts.³¹ These included (1) providing screening, monitoring, and outreach to travelers arriving from West Africa, (2) streamlining response efforts by working with federal authorities to divert passengers arriving from high-risk countries to just five U.S. airports, (3) training CBP staff at these five airports to screen travelers arriving from high-risk countries for signs and symptoms of Ebola or possible exposures, and (4) in very close collaboration with state and local public health agencies, developing a program to monitor all arriving travelers for 21 days after their departure (CDC, 2015b).

From 2014 to 2016, 36,059 travelers arriving into the United States from three West African countries—Sierra Leone, Guinea, and Liberia—underwent active monitoring for 21 days after a monitoring system was put in place by the CDC in partnership with state and local health departments (CDC, 2015b).³² This system was largely a response to the first case of Ebola in an arriving international passenger in Dallas, Texas (CDC, 2014). The diagnosis of Ebola in this individual was delayed for 2 days after initial presentation to the hospital, resulting in transmission to two health care workers (CDC, 2019a). There were no additional Ebola cases detected through this large-scale active monitoring effort during the 15-month period in which this system was in place.

Of the 11 Ebola cases treated in the United States, most were identified in countries in West Africa and flown back to the United States for care (CDC, 2019a). Of the two cases detected after reentry into the United States—which occurred before the active monitoring system was established—the first case in Dallas was not recognized as a potential case until late in the person’s illness, as their direct exposure risk to a person with Ebola in West Africa was not identified until that point. The second case, which occurred in New York City, self-identified prior to seeking medical care and at the onset of their symptoms, because the individual had potential exposure through working as a health care provider in an Ebola Treatment Unit in Guinea.³³

Although no additional cases were detected through this active monitoring program, it had several unintended consequences. Individuals under active monitoring who developed symptoms, such as fever, needed to be evaluated first to rule out Ebola—usually at a designated Ebola assessment or treatment hospital. This practice often delayed testing and care for other serious diseases, especially malaria, which is common among persons returning from Western Africa. An analysis of monitoring and movement

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³¹ More information about DGMQ’s emergency response to the Ebola epidemic is available at https://www.cdc.gov/ncezid/dgmq/emergency-response.html (accessed March 16, 2022).

³² This text was modified after release of the report to the study sponsor to correctly identify the agency with authority over the monitoring system.

³³ This text was modified after release of the report to the study sponsor to clarify the nature of the exposure experienced in the second case.

restriction policies implemented in the United States during the Ebola epidemic (2014–2016) found that movement restriction policies—including quarantine—required substantial resources to implement and varied from voluntary to mandatory programs. Additionally, there was a lack of clarity in some of the quarantine enforcement procedures (Sell et al., 2021) For example, a nurse who returned to the United States in 2014 after working in Sierra Leone was ordered to spend 4 days in isolation followed by 3 weeks of quarantine, despite a lack of any symptoms of illness. A lawsuit followed, resulting in a modification of the 3-week home confinement order. Medical groups opposed these regulations, stating that automatic 3-week quarantines for all travelers returning from Ebola-affected areas, with no regard for symptoms, would discourage health care workers from responding to the Ebola outbreak. Some state health departments, on the other hand, maintained that these regulations were necessary for public health (Price, 2016). This incident highlights the complexities of state interactions in issuing public health orders.

Emergency Response to the COVID-19 Pandemic

At the outset of the COVID-19 pandemic in January 2020, the DGMQ was called on to assist in the CDC’s emergency response. Through the response, the DGMQ has supported a wide range of activities, including “providing guidance, recommendations, and requirements; educating travelers and migrant populations; working with international, federal, STLT, and industry partners; and protecting the health of immigrants, migrants, refugees, and communities along U.S. borders” (CDC, 2021d). More information about the DGMQ’s emergency response activities during the COVID-19 pandemic is provided in Box 3-2. Simultaneously, the DGMQ also supported response activities for Ebola, resettlement of U.S. citizens and lawful permanent residents as well as vulnerable Afghans, and public health interventions for migrants at the Southwest border.

IMPROVING STRATEGIC PLANNING FOR POTENTIAL DISEASE OUTBREAKS

Experiences during recent emergency response efforts highlight the importance of scenario-based planning for the most likely and/or concerning potential disease outbreaks, with the active involvement of key partners. The committee identified multiple opportunities to improve strategic planning for potential disease outbreaks in the domains of (1) coordinated and collaborative advanced planning, (2) large-scale isolation and quarantine planning, and (3) ethics and equity considerations. The committee also developed a potential prioritization scheme for categorization of pathogens to help inform scenario planning illustrated in Table 3-1.

TABLE 3-1 Potential Prioritization Scheme for Categorization of Pathogens

Coordinated and Collaborative Advanced Planning

As will be discussed in Chapter 5, an evaluation of reporting ill travelers to the QBHSB established a set of recommendations for the CDC and QBHSB, many of which highlight the importance of collaborative planning in advance (Council of State and Territorial Epidemiologists, 2019):

• “Develop standardized protocols/algorithms for jurisdiction reporting to quarantine stations.
• Provide clarity and justification for each piece of data requested for reporting a case.
• Distribute the QBHSB annual report to jurisdictions.
• Hold annual meetings and drills between quarantine stations and jurisdictions in the region covered by each station.
• Develop a training webinar and downloadable reference document with information essential for jurisdiction reporting to DGMQ/QBHSB.
• Explore additional opportunities for communication with state, local, and territorial health departments.”

Planning for Large-Scale Isolation and Quarantine

Experiences during past outbreaks, epidemics, and pandemics of infectious diseases have underscored the critical need for large-scale isolation and quarantine planning, as well the consequences of the failure to plan. It is also critical to engage in collaborative advance planning to develop approaches to support continuity of care for individuals after arrival in the United States—particularly for at-risk or vulnerable populations.

For instance, the responses to the Ebola virus disease outbreaks in Western Africa (2014–2016), as well as the COVID-19 pandemic, were undermined by lack of planning to identify potential sites and operational needs to support the large-scale isolation and quarantine measures required for effective management of international passengers with illness and/or exposures. There were gaps in clarity of standards or predetermined roles and responsibilities around housing infrastructure and wraparound services, including issues related to transportation between facilities or jurisdictions. Across different jurisdictions, there was substantial variation in their respective capacities to offer resources (Allen, 2022). Moreover, there was a lack of clarity extending throughout the federal, state, local, tribal, and territorial levels regarding which entities had various authorities and when, as well as ambiguity about their respective roles and responsibilities. Additionally, there was wide variation in state and local implementation of quarantine and isolation measures (Allen, 2022).

The Association of State and Territorial Health Officials (ASTHO) has suggested strategies to strengthen isolation and quarantine preparedness planning: (1) define federal, state, and local roles and responsibilities; (2) evaluate plans through drills and exercises with stakeholders; and (3) develop tools to estimate resource costs for isolation and quarantine. They have also suggested evaluating the use of direct active monitoring to determine when it is appropriate (e.g., its effectiveness may be limited for respiratory illnesses), to understand resource requirements, and to explore opportunities to leverage virtual technologies if appropriate.

Ethics and Equity Considerations

As will be discussed in Chapter 4, the committee identified a set of key ethical principles for consideration in disease control measures and innovations. These foundational principles also apply to the implementation of large-scale quarantine and isolation and include (1) protecting privacy, (2) maintaining autonomy, (3) promoting equity, (4) minimizing the risk of error, and (5) ensuring accountability.

Disease control efforts by their nature need to include ethics, privacy, and equity considerations. The infringement on individual rights

to maximize public health benefits should only take place when deemed necessary, effective, and proportional to the threat, and within a context of supportive services to provide shelter, food, medicine, and other basic needs, and should be as limited and of as short a duration as necessary to maximally effect the desired outcome (Rothstein, 2015). The effects of quarantine on individuals can be substantial. Time spent in isolation can result in significant loss of income, which can be detrimental—and in some cases devastating—for individuals (Nuffield Council on Bioethics, 2020; WHO, 2016). A literature review found that the psychological impact of quarantine can be substantial, wide ranging, and long lasting (Brooks et al., 2020). Experiences and stressors related to quarantine included posttraumatic stress symptoms, confusion, anger, fear, financial loss, and stigma. Given that isolation and quarantine can cause or exacerbate mental health concerns, mental health supports need to be considered when these disease control measures are deemed necessary (Nakazawa et al., 2020). For example, when passengers were quarantined for 14 days after detection of COVID-19 cases aboard a cruise ship in March 2020, they were provided with smartphones that could be used to access free health consultations and place medication requests. Enabling quarantined individuals to communicate with loved ones via provision of internet access and devices can also reduce feelings of isolation, stress, and panic (Brooks et al., 2020). It is also important to address the special needs of certain quarantined populations (including children, older adults, and people with disabilities) to ensure that the services they receive are culturally and linguistically appropriate. This includes ensuring that personnel are available to assist individuals who may have difficulty navigating these technologies.

BORDER MEASURES AND ACTIVE MONITORING OF INTERNATIONAL TRAVELERS DURING COVID-19: EVALUATION

The committee evaluated research on the effectiveness of border measures and active monitoring of international travelers during COVID-19. Overall, the effectiveness of border measures, including pretravel testing, is unclear, and additional research is needed to determine the factors that contribute to successful screening measures. Overall, evidence suggests that border and screening measures may be more effective when used within the context of a national disease mitigation program and not relied on as the sole mechanism for reducing transmission.

Effectiveness of Border Screening

Border screening is the process by which incoming travelers are tested or otherwise assessed for signs of illness. In the United States, the DGMQ

partners with U.S. CBP to provide enhanced screening for incoming travelers, including symptom screening for COVID-19, both at airports and the southern border (Rasicot, 2021).³⁴ In many countries, much of the research on border screening involved polymerase chain reaction (PCR) or antigen testing before traveling and/or after arrival. Both modeling and empirical studies provide evidence of the potential effectiveness of border screening in reducing the transmission of COVID-19. Results from one modeling study suggest that, when used as a solitary measure, a single-test screening process before departure was not sufficient to prevent a local outbreak at the arrival destination, because it had not been found to significantly reduce the number of infected travelers entering a country (Bays et al., 2021). A study conducted in Iceland found that COVID-19 testing conducted twice post-arrival reduced the risk of false-negative results that can lead to the spread of infection (Baddal et al., 2021). While more research is needed, initial studies suggest that a single test may not be a strong-enough border screening measure to reduce the spread of COVID-19.

One study conducted an international meta-analysis of both modeling and observational studies and stated that both types have reported mixed results when assessing the effectiveness of COVID-19 screening measures (Burns et al., 2021). Modeling studies found that COVID-19 screening based on symptoms or potential exposure reduced imported or exported cases and delayed outbreaks; however, the authors expressed concerns with the quality of some models, noting inconsistencies in assumptions and parameters. (Burns et al., 2021). Modeling studies predicted that this form of screening would detect between 1 and 53 percent of infected travelers. Observational studies reported a wide range of positive cases detected—between 0 to 100 percent—with the majority of studies reporting fewer than 54 percent of cases detected. For screening based on testing rather than on symptoms or potential exposure, modeling studies reported that testing travelers reduced both imported or exported cases and cases detected. Observational studies reported that the proportion of cases detected varied from 58 to 90 percent, with variability potentially being attributable to timing of testing (Burns et al., 2021). An observational study concluded that COVID-19 border screening by testing can involve very low positive predictive values and high costs per positive case detected (Grunér et al., 2022). A Bayesian modeling approach to estimate the relative capacity for detection of imported cases of COVID-19 for 194 locations (excluding China) compared with that for Singapore estimated the ability to detect Wuhan-to-location imported cases of COVID-19 to be 38 percent (Niehus et al., 2020).

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³⁴ This text was modified after release of the report to the study sponsor to clarify the division’s role and responsibilities.

As part of California’s efforts to reduce introductions of COVID-19 into the state and country during the initial months of the COVID-19 pandemic, the state implemented a program to screen travelers from selected countries on entry and to obtain their contact information and share it with other states for monitoring purposes. Despite this very labor-intensive effort, this traveler screening system did not effectively prevent the introduction of COVID-19 into California. In California, barriers to effective COVID-19 monitoring and screening of travelers included incomplete traveler information transmitted to federal officials and states, the number of travelers requiring follow-up, and potential presymptomatic and asymptomatic transmission (Myers et al., 2020).³⁵ This suggests that during an outbreak, health departments have to be cautious about devoting their often-limited resources to these types of monitoring efforts, rather than channeling those resources into more effective mitigation strategies.

During the early phases of the COVID-19 pandemic, the CDC also implemented an entry screening program at certain airports for passengers arriving from designated countries (Dollard et al., 2020). This effort required substantial resources, yet the yield of laboratory-confirmed COVID-19 cases was low (1 case per 85,000 travelers screened) and—because it was conducted with manual data collection—contact information was missing for a substantial proportion of travelers who were screened. The low case-detection rate of this resource-intensive program highlighted the need for fundamental change in the U.S. border health strategy. For a disease such as COVID-19, with nonspecific clinical presentation and asymptomatic cases, symptom-based screening programs are not effective. More effective strategies for mitigating the importation of COVID-19 cases could include (1) enhanced communication with travelers regarding preventive measures, and (2) expanding predeparture and post-arrival testing (Dollard et al., 2020). COVID-19 also presents a unique situation in that early diagnostics were used under emergency use authorizations, and later assessment by the FDA revealed that different tests had different levels of sensitivity in detecting the SARS-CoV-2 virus (FDA, 2020). The effectiveness of a screening measure is dependent on multiple factors, including the characteristics of disease presentation and availability of accurate diagnostics.

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³⁵ Biodetection dogs may increase the ability to detect asymptomatic cases. A study found that utilizing biodetection dogs as a preliminary SARS-CoV-2 screening method resulted in an average sensitivity of 82.63 percent (Baddal et al., 2021). The authors noted that PCR testing would be used to confirm identification of infection.

Effectiveness of Strategies to Reduce Case Importation

Evidence suggests that mandatory testing, both before departure and upon arrival, increases accuracy in case detection compared to predeparture testing alone. Repeated testing for travelers quarantined on arrival can also enable shorter quarantine times without increasing the risk of disease spread (Dickens et al., 2021). Travel restrictions are useful in preventing infection spread in the early stages of an outbreak when it is confined to a particular area (Gwee et al., 2021; Kraemer et al., 2020). These restrictions may be less effective once an outbreak spreads to additional locations. Local mitigation strategies are effective in containing both local transmission and more widespread outbreaks.

Modeling studies indicated that testing travelers at entry and isolating those who test positive can achieve similar reductions in disease transmission compared to quarantining all travelers (Dickens et al., 2020). A modeling study found that relative to no screening on entry, testing all incoming travelers and isolating those who tested positive for COVID-19 reduced case importation across countries by 90.2 percent for a 7-day isolation period followed by a negative test and by 91.7 percent for a 14-day isolation followed by a negative test. Isolation for all travelers followed by entry permission without subsequent testing resulted in reductions of case importation of 55.4 percent for 7-day isolation and 91.2 percent for 14-day isolation. Testing all travelers and denying entry to those who tested positive reduced case importation by 77.6 percent.

Vaccine-related measures—such as requiring travelers to be fully or partially vaccinated—reduced the likelihood of importing cases (Ronksley et al., 2021). A study of international travelers arriving by air in Alberta, Canada, in January–February 2021 found that 0.02 percent of travelers who were fully or partially vaccinated against COVID-19 tested positive for the virus, in comparison with 1.42 percent of unvaccinated travelers, although both were relatively low.

Effectiveness of Travel Restrictions

Early detection and isolation of cases have the potential to prevent more infections than targeted travel restrictions and contact reductions, whereas a combination of the aforementioned nonpharmaceutical intervention (NPI) approaches can achieve the strongest and most rapid effect (Lai et al., 2020). Genomic epidemiology analyses of SARS-CoV-2 in China’s Guangdong province indicate that large-scale surveillance and NPI were effective in containing the epidemic and limiting dissemination to other provinces (Lu et al., 2020). Europe and the United States were reactive in issuing country-specific travel restrictions only after local transmission of

SARS-CoV-2 was confirmed (Davis et al., 2021). In January and February 2020, testing capacity was limited and restricted to people who had recently traveled to China. Broader testing can bolster local outbreak prevention efforts in providing opportunities for earlier detection and interventions.

Complete border closures only with specific target countries can modestly affect an epidemic’s trajectory. More significant containment is achieved when travel restrictions are combined with community mitigation strategies to prevent local transmission (Kwok et al., 2021). Complete border closures in Hong Kong reduced both the cumulative COVID-19 case number and mortality by approximately 14 percent. A modeling study of COVID-19 prevalence in Italy found spatial heterogeneity in the effect of travel restrictions, with regions farthest from the initial outbreak receiving greater benefit from these restrictions (Parino et al., 2021).

The inflow volume of passengers, local case incidence, and local epidemic growth need to be considered when implementing travel restrictions. A modeling study found that many countries can attain a negligible number of imported cases—less than 1 percent—with only selective travel restrictions imposed (Russell et al., 2021). In the early stages of a pandemic, travel restrictions can reduce approximately 80 percent of exportation events (Chinazzi et al., 2020; Wells et al., 2020). This can provide cities unaffected by an outbreak with time to coordinate an appropriate public health response. Research studies indicate benefits of travel restrictions on delaying the spread of outbreaks, but different studies indicated varying lengths of delay ranging from 1 day to 85 days (Burns et al., 2021). Studies found very low–certainty evidence that travel restrictions reduced COVID-19 cases within a community and cases imported or exported. Research indicates that travel restrictions may provide short-term benefits, but these restrictions are ineffective at completely eliminating disease (Aleta et al., 2020). Furthermore, international travel restrictions become ineffective after the early stages of a pandemic (Askitas et al., 2021).

Summary of Evaluation

To prevent or minimize disease transmission in the United States, the committee found questionable evidence for the effectiveness of travel restrictions and border closures for COVID-19 reactively targeting countries only after local transmission is confirmed. More evidence is needed on the potential benefits of these methods. In addition, monitoring of all international travelers arriving from outbreak-affected countries, regardless of symptoms or history of exposure, has been shown to be porous to asymptomatic cases. Similar lack of evidence has been documented for pandemic influenza (Bajardi et al., 2011; Cowling et al., 2010; Hollingsworth et al., 2006). Travel restrictions, border closures, and active monitoring of

international travelers work best for diseases that have low proportions of asymptomatic and presymptomatic transmission risk and longer incubation periods (Fraser et al., 2004; Hollingsworth et al., 2006). Furthermore, the key to the impact of travel restrictions is the rate of growth of the epidemic in the source country and early implementation of the policies. Travel restrictions and border closure, however, can delay the progression of the epidemic, allowing more time for health authorities to prepare mitigation and control policies. More severe and stringent strategies, such as closing travel to everyone regardless of the country that they are traveling from, may be effective in stopping or slowing the spread of disease, although the economic, social, and political trade-offs of these policies should be carefully evaluated.

For diseases like SARS and Ebola, these interventions are more effective when measures can be more directly targeted to those with known risk exposures, as opposed to targeting all travelers from a country or region. Quarantine with active monitoring of persons at risk and/or exposed works best when most secondary cases become symptomatic after they are separated from others; this helps to prevent ongoing transmission to others (i.e., tertiary cases). These tools were successfully used with SARS and during prior Ebola outbreaks within Africa to stop ongoing transmission—even before a vaccine became available—as well as historically, for diseases like smallpox (Bogoch et al., 2015; Hollingsworth et al., 2006). Both Ebola and smallpox have longer incubation periods and persons are most infectious after they have been symptomatic for several days. It should be noted that travel restrictions and border closures might be needed especially in the early phases of a pandemic when etiology, exact modes of transmission, incubation periods, and other characteristics of novel viruses are unknown.

Detailed analysis concerning the impact of the timing and extent of travel restrictions—that is, number of countries, citizenship, residential status—with respect to the pathogen of interest needs to inform future strategies. Such analysis, through formal evaluation, can help determine the parameters for when these tools should be considered in the future, especially for a highly transmissible respiratory virus with a short incubation period and a high proportion of asymptomatic infections and contagiousness prior to illness onset.

When COVID-19 first emerged in early 2020, its etiology was initially unknown. It took months to start to understand the epidemiologic (i.e., transmission) and clinical characteristics of the SARS-CoV-2 virus to help guide public health measures. However, it then became clear that SARSCoV-2 had a short incubation period of 2–14 days (with median of 5 days)—especially for more recent variants such as Omicron—as well as a relatively high proportion of asymptomatic persons among confirmed cases (40 percent), with transmission risk occurring among both presymptomatic

and asymptomatic cases (Ma et al., 2021). These findings call into question the role of quarantine and active monitoring in minimizing transmission, given the large degree of unrecognized chains of transmission.

Moreover, once COVID-19 transmission was established in the United States, the role of active monitoring of all international travelers from countries deemed at higher risk—many of whom were not symptomatic or likely infected—probably had questionable impact on transmission levels in the United States. However, diverting state and local health department resources to monitor international travelers impacted other local infection control priorities, including vaccination, testing, and outbreak response. Similarly, by the time a new variant of concern of a virus as transmissible as SARS-CoV-2 is recognized overseas, it is likely that it is already widely spreading in other settings. Therefore, the impact of targeted country-level travel restrictions in preventing or minimizing SARS-CoV-2 transmission in the United States was minimal. This was demonstrated in the failed effort against the Omicron variant, when travel bans for selected countries in Africa did not prevent a major pandemic wave from occurring in the United States or elsewhere. The initial travel bans enacted against South Africa and other African countries were decried as discriminatory, as countries in Europe also had reported cases. Travel bans can produce unintended effects, such as placing undue economic burdens on target countries and discouraging researchers from reporting new strains. It is important that travel restrictions are considered within the broader context of the national response, as these restrictions alone are unlikely to be effective in reducing disease spread (WHO, 2021). Lessons learned during recent outbreak and pandemic responses—such as for Ebola and COVID-19—can be keys to guiding policy decisions for when to consider travel restrictions/border closures and active monitoring of international passengers for future pandemics as a tool for minimizing or preventing transmission of diseases in the United States. It should be noted that the current science on the effectiveness on travel restrictions and border closures is not definitive. There is a need for more extensive analyses to better identify and evaluate the methods that were most effective during the COVID-19 pandemic. The DGMQ has a tool kit of options available, and each individual threat should be assessed to determine the best course of action for disease mitigation strategies.

The CDC could also leverage academic partners (see Chapter 5), or the new Center for Forecasting and Outbreak Analytics (see Box 3-3), to provide modeling expertise to help determine the transmission characteristics of microbial pathogens (e.g., median/range of incubation period, proportion of asymptomatic cases and degree of asymptomatic/presymptomatic transmission risk) as well as the outbreak scenarios (e.g., isolated to one country or region) where border restrictions/active monitoring may have the most impact for preventing or minimizing disease introduction into the United States during future pandemics or outbreaks of concern.

CONCLUSIONS AND RECOMMENDATIONS

Conclusions

Recommendations

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