Influenza in immunosuppressed populations: a review of infection frequency, morbidity, mortality, and vaccine responses

doi:10.1016/S1473-3099(09)70175-6

The Lancet Infectious Diseases

Volume 9, Issue 8, August 2009, Pages 493-504

https://doi.org/10.1016/S1473-3099(09)70175-6 Get rights and content

Summary

Patients that are immunosuppressed might be at risk of serious influenza-associated complications. As a result, multiple guidelines recommend influenza vaccination for patients infected with HIV, who have received solid-organ transplants, who have received haemopoietic stem-cell transplants, and patients on haemodialysis. However, immunosuppression might also limit vaccine responses. To better inform policy, we reviewed the published work relevant to incidence, outcomes, and prevention of influenza infection in these patients, and in patients being treated chemotherapy and with systemic corticosteroids. Available data suggest that most immunosuppressed populations are indeed at higher risk of influenza-associated complications, have a general trend toward impaired humoral vaccine responses (although these data are mixed), and can be safely vaccinated—although longitudinal data are largely lacking. Randomised clinical trial data were limited to one study of HIV-infected patients with high vaccine efficacy. Better trial data would inform vaccination recommendations on the basis of efficacy and cost in these at-risk populations.

Introduction

The influenza virus is among the most common human respiratory viruses. In the USA, for example, influenza can result in the admission of over 225 000 patients to hospital¹ and 36 000 deaths every year.² High rates of influenza infection and complication rates are suggested to occur among people with impaired immune defences. Immunosuppression can result from many different biological mechanisms, ranging from rare congenital immunodeficiencies to more common causes such as immunosuppressive drugs or HIV infection.

Despite prevailing concerns about the risk of influenza infection in patients with immunosuppression, the actual rate and effect of infection in this population are not well characterised. Whether people that are immunocompromised would be even more susceptible to new viruses, such as the recent swine-origin influenza A H1N1 strain,³ without the benefit of previous exposure, is an area for investigation. Moreover, although influenza vaccination is widely recommended for people that are immunosuppressed, the same immune dysfunction that can increase the risk and consequences of influenza infection might also compromise vaccine responses and effectiveness. These distinctions are particularly important in settings of vaccine shortages or in response to a new pandemic, where selective and prioritised allocation of vaccine is necessary. To better inform influenza vaccination policies for immunocompromised populations, we reviewed the published work relevant to influenza infection and vaccination in patients with HIV infection, recipients of solid-organ transplants (SOTs), recipients of haemopoietic stem-cell transplants (HSCTs), patients receiving chemotherapy, patients on chronic haemodialysis, and patients receiving corticosteroids. These conditions affect about 3 million people in the USA (about 1% of the total US population), and the worldwide HIV epidemic affects about 33 million people (table 1).

The primary purpose of this Review is to identify and summarise the incidence and mortality rates of influenza infection among adults who are immunocompromised, as well as the risks of vaccination, the ability of vaccine to elicit appropriate immune responses, and the clinical effectiveness of vaccination in these populations. We also summarise guidelines on influenza vaccination of these populations, limitations of the available data, and alternative approaches to influenza control.

Section snippets

HIV/AIDS

An estimated 1·3 million (480 000 to 1·9 million) people are living with HIV/AIDS in North America. Worldwide, the epidemic affects an estimated 33·2 million (30·6 million to 36·1 million) people.⁴ Influenza is a common cause of respiratory illness in adults with HIV.¹⁰ Because both antibodies and T cells play a crucial part in viral immune responses, patients infected with HIV might be expected have severe and prolonged influenza infections, as reported in several early case series and

Solid-organ transplantation

Patients receiving SOTs are treated with immunosuppressive drugs that alter multiple immune mechanisms.⁶¹ Therefore, those patients might have more severe influenza infections and compromised responses to vaccination. As of the end of 2004, 153 245 people in the USA were living with a functioning transplanted solid organ.⁵ Over 27 000 transplantations are done every year in the USA, nearly 90% of which are kidney, liver, and heart procedures.⁵

A retrospective review of patients that received

Bone-marrow transplantation

An estimated 35 000 people receive autologous (reimplanted from the same person) and 20 000 allogeneic (from a genetically similar donor) HSCTs every year worldwide.⁷ Preparation for stem-cell infusion generally requires high doses of chemotherapy, radiation, or both to prevent allograft rejection from residual host immune cells, destroy any residual malignant cells in patients receiving HSCTs for malignancies, and provide marrow space for donor stem-cell engraftment. These intensive

Malignancies and chemotherapy

Some 1·4 million patients will be diagnosed with new haematological and invasive solid-organ cancers in the USA in 2009,⁸ many of whom will require treatment with chemotherapy. Similar to preparation for HSCT, chemotherapy can produce acute and profound immunosuppression, although the degree differs depending on the chemotherapy drugs, doses, and total duration of therapy. An estimated number of patients receiving chemotherapy every year is not available.

Information about influenza frequency

Haemodialysis

By the end of 2006, 327 754 people were on chronic haemodialysis in the USA, with projected increases in prevalence.⁶ The complex and multifactorial causes of immune dysfunction in patients on haemodialysis include defects in complement activation, neutrophil function, and B-cell and T-cell function.126, 127, 128 Infections are the second leading cause of death in patients receiving dialysis.⁶ Compared with the general population, pulmonary infection kills more patients on dialysis¹²⁹ and

Systemic corticosteroids

Many patients use systemic corticosteroids to treat a wide variety of disorders, particularly inflammatory and autoimmune disorders such as asthma, rheumatoid arthritis, and inflammatory bowel disease. Some patients receive corticosteroids for short periods, whereas others remain on chronic therapy. The prevalence of corticosteroid use is not well known. Of the total British adult population, an estimated 0·9% (or about 409 000 adult Britons) are using oral corticosteroids at any given time,

Limitations and challenges

Among all immunosuppressive conditions discussed, very few data exist on the prevention of clinical influenza infection by vaccination. Most studies have focused on the surrogate outcome of humoral antibody responses. However, a positive humoral response can be defined in multiple ways, most commonly a haemagglutination inhibition titre of 1:40 or greater, or a four-fold or greater rise in titres after vaccination. The limitations of these definitions become apparent, for example, in a patient

Other options to control influenza infection

The priority for control of influenza is focused on generating effective antibody responses with vaccines.¹³ Progress is being made to increase the scale, duration, and breadth of vaccine responses to haemagglutinin and neuraminidase in healthy and immunocompromised populations.163, 164 Concerns that the cold-adapted live, attenuated vaccine would pose a risk to people that are immunocompromised have proven unfounded so far, but efficacy studies in adults that are immunocompromised have not

Conclusions

We encourage further clinical trials with relevant clinical outcome measures, as opposed to surrogate outcomes like vaccine-induced antibody titres. We would particularly welcome randomised trials comparing standard influenza vaccine with active comparators such as modified vaccines⁵⁵ or antiviral prophylaxis with or without vaccination. Such data would greatly enhance our ability to make more informed vaccination recommendations for this population, particularly in situations of vaccine

Search strategy and selection criteria

Relevant articles were identified by searches of Medline (1966–2009) with the medical subject heading terms “influenza, human”, “influenza A virus”, “influenza B virus”, or “influenza vaccines”, combined with the following associated disease terms: “HIV”, “HIV-1”, “dialysis”, “renal dialysis”, “organ transplantation”, “transplantation”, “bone marrow transplantation”, “neoplasms”, “glucocorticoids”, “adrenal cortex hormones”, “prednisone”, and “prednisolone”. Additional relevant articles

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ReviewInfluenza in immunosuppressed populations: a review of infection frequency, morbidity, mortality, and vaccine responses

Summary

Introduction

Section snippets

HIV/AIDS

Solid-organ transplantation

Bone-marrow transplantation

Malignancies and chemotherapy

Haemodialysis

Systemic corticosteroids

Limitations and challenges

Other options to control influenza infection

Conclusions

Search strategy and selection criteria

Am J Transplant

Chest

Chest

Lancet

Blood

Vaccine

Vaccine

Vaccine

Vaccine

Am J Kidney Dis

Vaccine

Am J Transplant

J Clin Virol

J Heart Lung Transplant

Chest

Am J Transplant

Transplant Proc

J Heart Lung Transplant

Transplant Proc

J Heart Lung Transplant

Antiviral Res

Liver Transpl

Vaccine

Am J Transplantation

Vaccine

Influenza-associated hospitalizations in the united states

JAMA

Mortality associated with influenza and respiratory syncytial virus in the United States

JAMA

Pandemic potential of a strain of influenza A (H1N1): early findings

Science

2007 AIDS epidemic update

USRDS 2008 Annual data report: atlas of chronic kidney disease and end-stage renal disease in the United States

Report on state of the art in blood and marrow transplantation

SEER cancer statistics review, 1975–2006

Use of oral corticosteroids in the United Kingdom

QJM

Influenza virus infection is a primary cause of febrile respiratory illness in HIV-infected adults, despite vaccination

Clin Infect Dis

Susceptibility to influenza A in HIV-positive patients

JAMA

Influenza in human immunodeficiency virus-infected patients during the 1997–1998 influenza season

Clin Infect Dis

Influenza-associated morbidity and mortality in young and middle-aged women

JAMA

Excess mortality due to pneumonia or influenza during influenza seasons among persons with acquired immunodeficiency syndrome

Arch Intern Med

Cardiopulmonary hospitalizations during influenza season in adults and adolescents with advanced HIV infection

J Acquir Immune Defic Syndr

Prevention and control of influenza: recommendations of the advisory committee on immunization practices (ACIP), 2007

MMWR Recomm Rep

Report on the global AIDS epidemic 2006: A UNAIDS 10th anniversary special edition. Geneva: Joint United Nations Programme on HIV/AIDS (UNAIDS)

Primary care guidelines for the management of persons infected with human immunodeficiency virus: recommendations of the HIV Medicine Association of the Infectious Diseases Society of America

Clin Infect Dis

An overview of the 1999 US public health service/infectious diseases society of America guidelines for preventing opportunistic infections in human immunodeficiency virus-infected persons

Clin Infect Dis

Activation of virus replication after vaccination of HIV-1-infected individuals

J Exp Med

Dynamics of HIV-1 replication following influenza vaccination of HIV+ individuals

Clin Exp Immunol

Effect of influenza vaccination on viral replication and immune response in persons infected with human immunodeficiency virus receiving potent antiretroviral therapy

J Infect Dis

Genotypic analysis of plasma HIV-1 RNA after influenza vaccination of patients with previously undetectable viral loads

AIDS

Influenza vaccination of human immunodeficiency virus (HIV)-infected adults: Impact on plasma levels of HIV type 1 RNA and determinants of antibody response

Clin Infect Dis

Review
Influenza in immunosuppressed populations: a review of infection frequency, morbidity, mortality, and vaccine responses