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James D. Heffelfinger, MD, MPH, Pragna Patel, MD, MPH, John T. Brooks, MD, Helene Calvet, MD, Charles L. Daley, MD, Hazel D. Dean, ScD, MPH, Brian R. Edlin, MD, Kathleen F. Gensheimer, MD, MPH, John Jereb, MD, Charlotte K. Kent, PhD, Jeffrey L. Lennox, MD, Janice K. Louie, MD, MPH, Ruth Lynfield, MD, Philip J. Peters, MD, Lauretta Pinckney, PhD, Philip Spradling, MD, Andrew C. Voetsch, PhD and Anthony Fiore, MD, MPH

James D. Heffelfinger, Pragna Patel, John T. Brooks, Hazel D. Dean, John Jereb, Charlotte K. Kent, Philip J. Peters, Lauretta Pinckney, Philip Spradling, Andrew C. Voetsch, and Anthony Fiore are with the Centers for Disease Control and Prevention (CDC), Atlanta, GA. Helene Calvet is with the Long Beach Department of Health and Human Services, Long Beach, CA. Charles L. Daley is with the National Jewish Medical and Research Center, Denver, CO. Brian R. Edlin is with the State University of New York Downstate Medical Center, Brooklyn, NY. Kathleen F. Gensheimer is with the Maine Department of Health and Human Services, Augusta, ME. Jeffrey L. Lennox is with Emory University, Atlanta. Janice K. Louie is with the California Department of Public Health, Berkeley, CA. Ruth Lynfield is with the Minnesota Department of Health, St. Paul, MN.

Correspondence: Correspondence should be sent to James D. Heffelfinger, 1600 Clifton Road NE, Centers for Disease Control and Prevention, Mail Stop: E-46, Atlanta, GA 30333 (e-mail: izh7{at}cdc.gov). Reprints can be ordered at http://www.ajph.org by clicking on the "Eprints/Reprints" link.

	ABSTRACT

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Among vulnerable populations during an influenza pandemic are persons with or at risk for HIV infection, tuberculosis, or chronic viral hepatitis. HIV-infected persons have higher rates of hospitalization, prolonged illness, and increased mortality from influenza compared with the general population. Persons with tuberculosis and chronic viral hepatitis may also be at increased risk of morbidity and mortality from influenza because of altered immunity and chronic illness. These populations also face social and structural barriers that will be exacerbated by a pandemic. Existing infrastructure should be expanded and pandemic planning should include preparations to reduce the risks for these populations.

	INTRODUCTION

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DURING AN INFLUENZA PANdemic, persons with or at risk for HIV infection, tuberculosis, or chronic hepatitis B or C will be particularly vulnerable,¹ not only to influenza^2–7 but also to disruptions in treatment and prevention services. These groups share several vulnerabilities: (1) HIV, Mycobacterium tuberculosis, and hepatitis B and C viruses are transmissible, and disruption of prevention services during a pandemic could increase their transmission; (2) influenza and these illnesses may interact to increase morbidity and mortality; (3) interruptions in treatment of these infections may increase morbidity, mortality, and transmission; (4) these infections occur more frequently among persons challenged by substance abuse, homelessness, mental illness, incarceration, and reduced access to prevention and treatment services^8–12; and (5) specialty clinics, medical associations, community-based organizations (CBOs), and public health infrastructures that control these infections may be enlisted to address a pandemic, leaving each unable to fully serve their usual clients.

In this article, we discuss steps that can be taken by public health programs and health care systems to reduce the risk of influenza illness among persons with or at risk for these conditions and to maintain continuity of care and prevention services for these conditions during a pandemic. The emergence of widespread infection with a novel influenza A(H1N1) virus and the recent pandemic declaration by the World Health Organization¹³ dramatically increase the urgency of considering these issues. We summarize data from the literature and discussions of a panel of experts in influenza, HIV, tuberculosis, and viral hepatitis, convened on May 5, 2008, in Atlanta, Georgia.

	RISK OF COMPLICATIONS FROM INFLUENZA

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HIV
An estimated 1.1 million persons are currently living with HIV/AIDS in the US.¹⁴ HIV infection is associated with increased susceptibility to opportunistic and other infections, including viral and bacterial lower respiratory tract infections and recurrent pneumonia.^2,4,5,7,15 Although data are limited about the frequency and severity of influenza illness among HIV-infected persons,¹⁶ several studies have noted higher hospitalization rates,^17,18 prolonged illness,^19,20 and increased mortality.²¹ Highly active antiretroviral therapy (HAART) may reduce the rate of influenza complications in persons with HIV.¹⁸

Tuberculosis
In the US, an estimated 11 million persons have latent tuberculosis infection,²² and over 13 000 people were diagnosed with tuberculosis disease in 2007.²³ Active tuberculosis causes acute and sometimes permanent pulmonary damage^24–26 that can compound morbidity from other respiratory infections.^26–28 Both M. tuberculosis and influenza impair immune functions, including host T-cell immunologic responses,^3,6,29 and influenza may promote the emergence of active tuberculosis in persons with latent infection.³⁰ Additionally, increased mortality from tuberculosis has been observed during influenza pandemics.^30,31

Viral Hepatitis
In the US, an estimated 1.4 million persons have chronic hepatitis B,³² and 3.4 million persons have chronic HCV.³³ Chronic viral hepatitis can progress to cirrhosis, end-stage liver disease, and hepatocellular carcinoma, and may require liver transplantation.^34,35 Persons with cirrhosis and liver transplant recipients may be at particular risk for developing complications from influenza due to immune dysfunction.^36,37 Influenza can also cause systemic effects³⁸ that may exacerbate chronic hepatic disease, including direct injury to hepatocytes by influenza virus, injury from circulating cytokines, or worsening of comorbid respiratory conditions.^38–40

	PREVENTION, TREATMENT, AND CONTINUITY OF CARE

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Influenza Vaccination
Although vaccination is the most effective strategy to prevent influenza, in the early stages of a pandemic, the supply of influenza vaccine may be insufficient to meet demand. Once vaccine becomes available in a pandemic, vaccination of persons with these conditions as quickly as possible will be critical.

Influenza vaccination is recommended annually to prevent seasonal influenza for persons at increased risk for complications from influenza,¹⁶ including persons with HIV infection, pulmonary disease, and chronic liver disease. However, the percentage of persons older than 50 years with chronic medical conditions who receive annual influenza vaccine is less than 35%.¹ Efforts to increase seasonal influenza vaccine coverage in these groups will improve individual health and may strengthen infrastructure that is capable of quickly delivering influenza vaccine during a pandemic. In June 2009, the World Health Organization raised the level of pandemic alert to the highest level in response to novel influenza A(H1N1) because the virus is readily transmitted from person-to-person and from one country to another, and further spread was considered to be inevitable.⁴¹ Recent 2009 H1N1 vaccination recommendations from the Advisory Committee on Immunizations Practices indicate that persons with chronic medical conditions should be among the groups vaccinated as soon as vaccine is available.⁴²

Trivalent inactivated influenza vaccine is effective in preventing seasonal influenza among persons with HIV infection,^43,44 yet the benefit is reduced with advanced HIV disease.¹⁷ Anti-influenza antibody titers are typically adequate among vaccinated HIV-infected persons with normal or slightly reduced CD4 cell counts,⁴⁵ but may not protect persons with low CD4 cell counts.⁴ Several studies have shown that vaccination with the trivalent inactivated influenza vaccine is not associated with progression of HIV disease or long-term immunologic or HIV virologic effects.^43,46–48 Live attenuated influenza vaccine is not recommended for persons with HIV infection or other chronic medical conditions.

Data on the effectiveness of influenza vaccination in persons with tuberculosis and chronic viral hepatitis are limited. Small studies indicate that patients with tuberculosis have normal serological responses to influenza vaccination and infection.^49,50 Although inactivated influenza vaccination provides adequate antibody responses in adult liver transplant recipients, the applicability of these data to persons with chronic viral hepatitis is unclear.^51,52 Nevertheless, given the potential for influenza infection to exacerbate chronic pulmonary or hepatic disease and the safety of trivalent inactivated influenza vaccine, persons with tuberculosis and chronic viral hepatitis should be vaccinated.

Treatment of and Chemoprophylaxis Against Influenza
Four antiviral agents have been approved by the Food and Drug Administration for the treatment of influenza A virus (Table 1). Antiviral treatment is recommended for persons with chronic medical conditions such as chronic lung disease, chronic liver disease, and immunodeficiency.⁵⁸ Based on limited drug-interaction data, no absolute contraindications are known for coadministration of these medications with antiretroviral medications, antituberculosis medications, or antiviral medications used to treat viral hepatitis.^53,54 Antiviral chemoprophylaxis may be an important method for preventing and controlling influenza early during a pandemic or for persons who are exposed to pandemic virus and those who have high risk for influenza complications. Neuraminidase inhibitors are currently recommended for both treatment of and chemoprophylaxis against novel H1N1 virus infections,^55,60 and persons with HIV, tuberculosis, or chronic viral hepatitis who meet criteria should receive standard antiviral regimens (Table 1). Given the emergence of antiviral resistance among influenza viruses,^16,61–63 the ideal antiviral regimens during a pandemic will depend on the pandemic strain's sensitivity to available agents. To date, novel influenza A(H1N1) viruses have been susceptible to neuraminidase inhibitors.¹³

Similarly, ensuring completion of treatment courses for persons with tuberculosis should be a priority during a pandemic. Incomplete or sporadic treatment of tuberculosis can lead to relapse, drug resistance, and secondary transmission. During a pandemic, the standard practice of directly observed therapy for the duration of therapy (at least 6 months) should be maintained. To alleviate personnel shortages during a pandemic, health care providers should consider giving directly observed therapy intermittently (e.g., twice weekly instead of daily) to stable patients with drug-sensitive tuberculosis.

In general, interferon-–based therapies for chronic viral hepatitis should be continued during a pandemic. Interferon- may have activity against influenza,⁶⁹ and discontinuing treatment could lead to rebound viremia and increased transmission of HCV. The decision to initiate interferon- during an influenza pandemic should take into account the likelihood that side effects, which mimic influenza, may complicate its diagnosis. Treatment of hepatitis B with antivirals, such as lamivudine or telbivudine, should be continued during an influenza pandemic because interrupting treatment can lead to rebound viremia, severe exacerbations of chronic hepatitis,⁷⁰ and, possibly, increased transmission of hepatitis B virus.

Maintaining access to prevention services and continuity of care will be important challenges for persons with these illnesses during a pandemic. Such persons are disproportionately affected by social, structural, and behavioral conditions that are associated with reduced access to health care and prevention services and increased vulnerability to infectious diseases. These conditions include poverty, unemployment, homelessness, substance use, mental health conditions, incarceration or involvement with the criminal justice system or immigration authorities, cultural and language barriers, lack of health insurance or access to care, and reliance on fragmented, underfunded, or nonexistent health services.^71–77 Groups at highest risk for these infections are men who have sex with men, illicit drug users, and immigrants, because they are disadvantaged by stigma, discrimination, or illegal status. Transmission of tuberculosis and influenza may be amplified in crowded conditions such as homeless shelters, jails, and prisons.^78,79 Often, responsibility for prevention and care for HIV, tuberculosis, and viral hepatitis falls on an already fragile health infrastructure, including public and community clinics, CBOs, correctional health care systems, local emergency departments, and outreach programs. The confluence of these factors is likely to exacerbate racial, ethnic, and socioeconomic disparities in pandemic influenza-related morbidity and mortality.

	STRENGTHENING AND ADAPTING EXISTING PUBLIC HEALTH INFRASTRUCTURE

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During an influenza pandemic, the capacity to maintain health care services and prevention programs for persons with HIV infection, tuberculosis, and chronic viral hepatitis will be strained by the need to provide care for patients seeking prevention against and treatment of influenza. Treatment and prevention activities will also be compromised by loss or displacement of patients and personnel, disruptions in transportation systems, and interruptions of supplies of essential medications. Although literature describing the impact of a pandemic on persons with these illnesses in the United States is not available, the effect of Hurricane Katrina on care and prevention services for persons with HIV infection and tuberculosis provides some insight. Access to HIV care, supplies of antiretrovirals and other medications, and support services were limited in the immediate aftermath of the hurricane, and many patients treated by the largest HIV care provider in New Orleans experienced a 4–6 week disruption in treatment.⁸⁰ Normal operations of tuberculosis control efforts in New Orleans were also disrupted; approximately half of the Louisiana Tuberculosis Control Program staff were evacuated to other states and normal communication channels were interrupted.⁸¹

In a severe pandemic, public health programs should focus on the highest priorities, such as diagnosing, locating, and providing prevention services and care to persons at greatest risk of acquiring and transmitting these diseases.

Nonpharmaceutical Interventions
Currently, recommendations for use of nonpharmaceutical interventions for vulnerable populations do not differ from other populations, but the urgency is greater because of their susceptibility. Recommendations may include longer periods of home isolation. A full discussion of nonpharmaceutical interventions has been published by CDC in an interim prepandemic guidance.^82,83

Maintaining and Improving Delivery of Health Care
During a pandemic, alternate delivery methods may be needed for vaccination, antiviral prophylaxis, and treatment of preexisting illnesses caused by HIV infection, tuberculosis, and chronic viral hepatitis. Public health clinics and programs will be vital because their infrastructure for communicable disease investigation and control can be adapted to assist with influenza vaccination and prevention activities. For example, local disease intervention specialists, the public health personnel who provide outreach and prevention services to persons infected with these and other diseases, can find persons exposed to influenza infection and get them to prevention and treatment services. These personnel also can help maintain continuity of care by distributing medications and providing essential services to persons in their homes and in jails, homeless shelters, and long-term care facilities.

	NEXT STEPS

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To address the unique needs of persons with and at risk for HIV infection, tuberculosis, and chronic viral hepatitis, and of health care providers during a pandemic, we suggest the following steps in pandemic planning and response efforts.

Providers and public health personnel should improve rates of annual vaccination against seasonal influenza in these vulnerable populations, their caretakers, and their health care providers.

Federal, state, and local governments and health departments should be transparent, proactive, and ethical in their planning to prevent and control influenza and minimize disruptions in continuity of care for these vulnerable populations. Contingency plans should register and train personnel who could be deployed during a pandemic; identify and partner with CBOs, professional organizations, health facilities, and other agencies serving vulnerable populations to develop operational plans; and develop the capacity to deliver vital medications and other support to vulnerable populations.

States should modify laws and regulations to allow medications to be prescribed and dispensed and vaccines administered as expeditiously as possible during a pandemic. Statutory restrictions should be eased for dispensing, delivering, and refilling prescriptions; for extending the supply of medications that can be dispensed by pharmacies and by assistance programs; and for expanding the number and types of persons who can administer vaccines.

Patients with HIV, tuberculosis, or chronic viral hepatitis should be educated about their vulnerability to influenza, the importance of vaccination against seasonal and pandemic influenza, the availability of influenza antiviral medications, nonpharmaceutical measures, and methods for achieving continuity of care for underlying illnesses. Their providers should be trained to diagnose and treat influenza, understand vaccination and prophylaxis against influenza and isolation measures, and prevent influenza exposures in the community.

During pandemic planning, it is important to examine the current public health infrastructure to determine ways to expand the system for other services during a pandemic. Public health officials and health care providers should determine the priorities for continuity of services and disseminate this information.

Communication between patients, health care systems, public health agencies, and CBOs will be essential during a pandemic for providing access to services for influenza and continuity of care for underlying illnesses. Public health agencies and health care facilities should determine needs and develop informational materials that are concise, easy to understand, and available in a variety of languages before a pandemic occurs.

Evidence supporting the effectiveness of vaccination and treatment strategies for influenza in these populations is limited.⁸⁴ Additional research on influenza prevention and treatment in these populations would improve public health planning and interventions for a pandemic. A research agenda should be developed to close these gaps. Topics that should be considered in such a research agenda are listed in the box on page S336.

Topics That Should be Considered in a Research Agenda to Address Gaps in Knowledge Regarding Prevention and Treatment of Influenza Among Persons Infected With HIV, Tuberculosis, and Chronic Viral Hepatitis Topics to be addressed include investigation of: New strategies to achieve high seasonal influenza vaccination coverage levels among persons with HIV, tuberculosis, and chronic viral hepatitis, their close contacts, their health care providers, staff at organizations serving them, and those who may be more likely to come into contact with them, such as staff at correctional facilities and homeless shelters. The clinical effectiveness of current and newly developed influenza vaccines and antiviral agents among persons with these illnesses (including the optimal duration of treatment and prophylaxis). Methods to use data from surveillance systems to evaluate seasonal influenza vaccine effectiveness, safety, and coverage in these populations. The duration and extent of influenza virus shedding after infection among persons with these illnesses. Methods to make influenza vaccines more immunogenic (and effective) in persons with immunosuppression. Drug–drug interactions (e.g. oseltamivir and antiretroviral medications) and the effects of chronic medications on host–antibody response to influenza vaccination in persons with these illnesses. The effects of interferon-a on susceptibility to influenza, the clinical manifestations and course of the illness, and response to influenza vaccination. The acceptance of influenza vaccination by persons with and at risk for these chronic infections. Measures to reduce the risk of bacterial superinfections among persons with and at risk for these chronic infections during a pandemic. The feasibility and acceptance of nonpharmaceutical interventions by persons with and at risk for these illnesses. Trends in morbidity and mortality from tuberculosis during past influenza pandemics using existing data. We encourage investigators to accept the challenge to pursue these research opportunities so that improvements to the current recommendations can be made.

 

Conclusions
During an influenza pandemic, persons with HIV, tuberculosis, or chronic viral hepatitis are at greater risk of complications and are subject to interactions between influenza and their underlying illnesses. Preventing and treating influenza, reducing disruptions in care and prevention services for these conditions, adapting existing health infrastructure, and encouraging and preparing public health agencies, providers, and CBOs to work together to provide essential services will reduce morbidity and mortality and should be viewed as critical public health priorities. The recent declaration of an influenza pandemic caused by a novel H1N1 virus, and the finding that young persons with chronic medical conditions are at higher risk for complications, underscores the urgency in addressing these issues.

	Human Participant Protection

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No human participants were involved in this study.

	Footnotes

 
Peer Reviewed

Note. The findings and conclusions in this paper are those of the authors and do not necessarily represent the views of the Centers for Disease Control and Prevention.

Contributors

J. D. Heffelfinger coordinated the expert panel review, reviewed relevant literature, and wrote the article. P. Patel, J. T. Brooks, H. Calvet, C. L. Daley, H. D. Dean, B. R. Edlin, K. F. Gensheimer, J. Jereb, C. K. Kent, J. L. Lennox, J. K. Louie, R. Lynfield, P. J. Peters, L. Pinckney, P. Spradling, A. C. Voetsch, and A. Fiore helped determine the format and content of the article, assisted with literature searches, and provided critical review of all drafts.

Accepted for publication August 15, 2009.

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