Keywords
Influenza
Vaccination
HIV/AIDS
Vaccination
HIV/AIDS
Abstract
Background: Despite the burden of disease and increased risk of influenza-associated morbidity and mortality among PLWHA, influenza vaccination has been understudied in this population.
Methods: We built an 11-year cohort of HIV-infected adults from medical records of PLWHA seeking care within the Louisiana State University medical system from June 2002-June 2013. Influenza vaccination uptake among PLWHA was calculated overall and for each medical facility for each influenza season. Linear regression was used to assess influenza vaccination uptake over time both overall and by facility. Data were restricted to the final influenza season (2012-13) to assess predictors of PLWHA vaccination. Individuals were nested within medical facilities in order to assess the amount of variability in influenza vaccination rates across medical facilities.
Results: Influenza vaccination uptake among PLWHA increased over the study period (p<0.01). The overall proportion of PLWHA vaccinated during the 2012-13 influenza season was 33.7%. 37.9% of the variability in the model occurred at the facility-level.
Conclusions: Although there was an increase in influenza vaccination within the PLWHA cohort over the course of the study, vaccination rates remained low overall. Special efforts must be made to increase vaccination uptake among PLWHA, with particular focus on those within the population who are likely to be at highest risk. The substantial variability at the facility-level indicates that there are unmeasured facility-level factors that contribute significantly to PLWHA vaccination.
References
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26. Durham MD, Buchacz K, Armon C, Patel P, Wood K, Brooks JT, et al. Seasonal Influenza Vaccination Rates in the HIV Outpatient Study—United States, 1999–2013. Clinical Infectious Diseases. 2014; 60:976-7.
27. Gallagher KM, Juhasz M, Harris NS, Teshale EH. Predictors of Influenza Vaccination in HIV-Infected Patients in the United States, 1990-2002. The Journal of Infectious Diseases. 2007; 196:339-46.
28. Valour F, Cotte L, Voirin N, Godinot M, Ader F, Ferry T, et al. Vaccination coverage against hepatitis A and B viruses, Streptococcus pneumoniae, seasonal flu, and A(H1N1)2009 pandemic influenza in HIV-infected patients. Vaccine. 2014; 32:4558-64.
29. Cataldi JR, O’Leary ST, Lindley MC, Hurley LP, Allison MA, Brtnikova M, et al. Survey of Adult Influenza Vaccination Practices and Perspectives Among US Primary Care Providers (2016–2017 Influenza Season). Journal of General Internal Medicine. 2019; 34:2167-75.
30. Changolkar S, Rareshide CAL, Snider CK, Patel MS. Patient, Physician, and Environmental Predictors of Influenza Vaccination During Primary Care Visits. Journal of General Internal Medicine. 2020; 35:611-3.
31. Dexter LJ, Teare MD, Dexter M, Siriwardena AN, Read RC. Strategies to increase influenza vaccination rates: outcomes of a nationwide cross-sectional survey of UK general practice. BMJ Open. 2012; 2:e000851.
32. Humiston SG, Bennett NM, Long C, Eberly S, Arvelo L, Stankaitis J, et al. Increasing Inner-City Adult Influenza Vaccination Rates: A Randomized Controlled Trial. Public Health Reports. 2011; 126:39-47.
33. Lu P-j, Srivastav A, Amaya A, Dever JA, Roycroft J, Kurtz MS, et al. Association of provider recommendation and offer and influenza vaccination among adults aged ≥18 years – United States. Vaccine. 2018; 36:890-8.
34. Murray K, Low C, O’Rourke A, Young F, Callanan I, Feeney E, et al. A quality improvement intervention failed to significantly increase pneumococcal and influenza vaccination rates in immunosuppressed inflammatory arthritis patients. Clinical Rheumatology. 2020; 39:747-54.
35. Nichol KL. Ten-year durability and success of an organized program to increase influenza and pneumococcal vaccination rates among high-risk adults. The American Journal of Medicine. 1998; 105:385-92.
36. Tan L. A review of the key factors to improve adult immunization coverage rates: What can the clinician do? Vaccine. 2018; 36:5373-8.
37. Tan LJ, VanOss R, Ofstead CL, Wetzler HP. Maximizing the impact of, and sustaining standing orders protocols for adult immunization in outpatient clinics. American Journal of Infection Control. 2020; 48:290-6.
38. Armstrong K, Berlin M, Schwartz JS, Propert K, Ubel PA. Barriers to influenza immunization in a low-income urban population. American Journal of Preventive Medicine. 2001; 20:21-5.
39. Chen JY, Fox, S. A., Cantrell, C. H., Stockdale, S. E., & Kagawa-Singer, M. . Health desparities and prevention: racial/ethnic barriers to flu vaccinations. J Community Health. 2007; 32:5-20.
40. Egede LE, Zheng D. Racial/Ethnic Differences in Influenza Vaccination Coverage in High-Risk Adults. American Journal of Public Health. 2003; 93:2074-8.
41. Frew PM, Painter JE, Hixson B, Kulb C, Moore K, del Rio C, et al. Factors mediating seasonal and influenza A (H1N1) vaccine acceptance among ethnically diverse populations in the urban south. Vaccine. 2012; 30:4200-8.
42. Zimmerman RK, Santibanez TA, Janosky JE, Fine MJ, Raymund M, Wilson SA, et al. What affects influenza vaccination rates among older patients? An analysis from inner-city, suburban, rural, and veterans affairs practices. The American Journal of Medicine. 2003; 114:31-8.
43. Louisiana State University Health Care Services Division. LSU Health Annual Report2011.
44. Vach W, Blettner M. Biased Estimation of the Odds Ratio in Case-Control Studies due to the Use of Ad Hoc Methods of Correcting for Missing Values for Confounding Variables. American Journal of Epidemiology. 1991; 134:895-907.
45. Department of Health and Human Services OoDPaHP. Healthy People 2020. Washington, D.C. [cited 2020 February 29th]; Available from: https://www.healthypeople.gov/2020/topics-objectives/topic/immunization-and-infectious-diseases/objectives.
46. Fine AD, Bridges CB, De Guzman AM, Glover L, Zeller B, Wong SJ, et al. Influenza A among Patients with Human Immunodeficiency Virus: An Outbreak of Infection at a Residential Facility in New York City. Clinical Infectious Diseases. 2001; 32:1784-91.
47. Radwan HM, Cheeseman SH, Lai KK, Ellison RT, III. Influenza in Human Immunodeficiency Virus-Infected Patients during the 1997–1998 Influenza Season. Clinical Infectious Diseases. 2000; 31:604-6.
48. Bennett KJ, Bellinger JD, Probst JC. Receipt of Influenza and Pneumonia Vaccinations: The Dual Disparity of Rural Minorities. Journal of the American Geriatrics Society. 2010; 58:1896-902.
49. Fiscella K, Franks P, Doescher MP, Saver BG. Disparities in health care by race, ethnicity, and language among the insured: findings from a national sample. Medical care. 2002; 40:52-9.
50. Johnson DR, Nichol KL, Lipczynski K. Barriers to Adult Immunization. The American Journal of Medicine. 2008; 121:S28-S35.
51. Winston CA, Wortley PM, Lees KA. Factors Associated with Vaccination of Medicare Beneficiaries in Five U.S. Communities: Results from the Racial and Ethnic Adult Disparities in Immunization Initiative Survey, 2003. Journal of the American Geriatrics Society. 2006; 54:303-10.
52. Yousey-Hindes KM, Hadler JL. Neighborhood Socioeconomic Status and Influenza Hospitalizations Among Children: New Haven County, Connecticut, 2003–2010. American Journal of Public Health. 2011; 101:1785-9.
53. Hebert PL, Frick KD, Kane RL, McBean AM. The Causes of Racial and Ethnic Differences in Influenza Vaccination Rates among Elderly Medicare Beneficiaries. Health Services Research. 2005; 40:517-38.
54. Wooten KG, Wortley PM, Singleton JA, Euler GL. Perceptions matter: Beliefs about influenza vaccine and vaccination behavior among elderly white, black and Hispanic Americans. Vaccine. 2012; 30:6927-34.
2. Centers for Disease Control and Prevention. Estimated Influenza Illnesses and Hospitalizations Averted by Vaccination — United States. [cited 2017 February 2]; Available from: https://www.cdc.gov/flu/about/disease/2015-16.htm.
3. Thompson WW, Shay DK, Weintraub E, et al. Influenza-associated hospitalizations in the united states. JAMA. 2004; 292:1333-40.
4. Centers for Disease Control and Prevention. Diagnoses of HIV infection in the United States and dependent areas, 2017. HIV Surveillance Report. 2018; 29.
5. Cohen C, Simonsen L, Sample J, Kang J-W, Miller M, Madhi SA, et al. Influenza-Related Mortality Among Adults Aged 25–54 Years With AIDS in South Africa and the United States of America. Clinical Infectious Diseases. 2012; 55:996-1003.
6. Kunisaki KM, Janoff EN. Influenza in Immunosuppressed Populations: A Review of Infection Frequency, Morbidity, Mortality, and Vaccine Responses. The Lancet infectious diseases. 2009; 9:493-504.
7. Lin JC, Nichol KL. Excess Mortality Due to Pneumonia or Influenza During Influenza Seasons Among Persons With Acquired Immunodeficiency Syndrome. Archives of Internal Medicine. 2001; 161:441-6.
8. Sheth AN, Patel P, Peters PJ. Influenza and HIV: Lessons from the 2009 H1N1 Influenza Pandemic. Current HIV/AIDS Reports. 2011; 8:181-91.
9. Cheryl C, Sibongile W, Cecile V, Adam LC, Shabir AM, Marietjie V, et al. Deaths Associated with Respiratory Syncytial and Influenza Viruses among Persons ≥5 Years of Age in HIV-Prevalent Area, South Africa, 1998–2009. Emerging Infectious Disease journal. 2015; 21:600.
10. Cohen C, Moyes J, Tempia S, Groom M, Walaza S, Pretorius M, et al. Severe influenza-associated respiratory infection in high HIV prevalence setting, South Africa, 2009-2011. Emerging Infectious Diseases. 2013; 19:1766-74.
11. Mor SM, Aminawung JA, Demaria Jr A, Naumova EN. Pneumonia and influenza hospitalization in HIV-positive seniors. Epidemiology and Infection. 2011; 139:1317-25.
12. Tasker SA, Treanor JJ, Paxton WB, Wallace MR. Efficacy of influenza vaccination in hiv-infected persons: A randomized, double-blind, placebo-controlled trial. Annals of Internal Medicine. 1999; 131:430-3.
13. Remschmidt C, Wichmann O, Harder T. Influenza vaccination in HIV-infected individuals: Systematic review and assessment of quality of evidence related to vaccine efficacy, effectiveness and safety. Vaccine. 2014; 32:5585-92.
14. Atashili J, Kalilani L, Adimora AA. Efficacy and clinical effectiveness of influenza vaccines in HIV-infected individuals: a meta-analysis. BMC Infectious Diseases. 2006; 6:138.
15. Ceravolo A, Orsi A, Parodi V, Ansaldi F. Influenza vaccination in HIV-positive subjects: latest evidence and future perspective. J Prev Med Hyg. 2013; 54:1-10.
16. Beck CR, McKenzie BC, Hashim AB, Harris RC, Zanuzdana A, Agboado G, et al. Influenza vaccination for immunocompromised patients: summary of a systematic review and meta-analysis. Influenza and Other Respiratory Viruses. 2013; 7:72-5.
17. Beck CR, McKenzie BC, Hashim AB, Harris RC, Influenza UoN, the ImmunoCompromised Study Group a, et al. Influenza Vaccination for Immunocompromised Patients: Systematic Review and Meta-analysis by Etiology. The Journal of Infectious Diseases. 2012; 206:1250-9.
18. El Chaer F, El Sahly HM. Vaccination in the Adult Patient Infected with HIV: A Review of Vaccine Efficacy and Immunogenicity. The American Journal of Medicine. 2019; 132:437-46.
19. Centers for Disease Control and Prevention. Prevention and Control of Influenza; Recommendations of the Immunization Practices Advisory Comittee (ACIP). MMWR. 1991; 40:1-15.
20. Centers for Disease Control and Prevention. USPHS/IDSA Guidelines for the Prevention of Opportunistic Infections in Persons Infected with Human Immunodeficiency Virus: A Summary. MMWR. 1995; 44:1-34.
21. Centers for Disease Control and Prevention. Prevention and Control of Seasonal Influenza with Vaccines: Recommendations of the Advisory Committee on Immunization Practices — United States, 2019–20 Influenza Season. MMWR. 2019; 68:1-21.
22. Sorvillo FJ, Nahlen BL. Influenza immunization for HIV-infected persons in Los Angeles. Vaccine. 1995; 13:377-80.
23. Wortley PM, Farizo KM. Pneumococcal and influenza vaccination levels among HIV-infected adolescents and adults receiving medical care in the United States. Adult and Adolescent Spectrum of HIV Disease Project Group. AIDS (London, England). 1994; 8:941-4.
24. Althoff KN, Anastos K, Nelson KE, Celentano DD, Sharp GB, Greenblatt RM, et al. Predictors of reported influenza vaccination in HIV-infected women in the United States, 2006–2007 and 2007–2008 seasons. Preventive Medicine. 2010; 50:223-9.
25. Durham MD, Buchacz K, Armon C, Patel P, Wood K, Brooks JT. Rates and correlates of influenza vaccination among HIV-infected adults in the HIV Outpatient Study (HOPS), USA, 1999–2008. Preventive Medicine. 2011; 53:89-94.
26. Durham MD, Buchacz K, Armon C, Patel P, Wood K, Brooks JT, et al. Seasonal Influenza Vaccination Rates in the HIV Outpatient Study—United States, 1999–2013. Clinical Infectious Diseases. 2014; 60:976-7.
27. Gallagher KM, Juhasz M, Harris NS, Teshale EH. Predictors of Influenza Vaccination in HIV-Infected Patients in the United States, 1990-2002. The Journal of Infectious Diseases. 2007; 196:339-46.
28. Valour F, Cotte L, Voirin N, Godinot M, Ader F, Ferry T, et al. Vaccination coverage against hepatitis A and B viruses, Streptococcus pneumoniae, seasonal flu, and A(H1N1)2009 pandemic influenza in HIV-infected patients. Vaccine. 2014; 32:4558-64.
29. Cataldi JR, O’Leary ST, Lindley MC, Hurley LP, Allison MA, Brtnikova M, et al. Survey of Adult Influenza Vaccination Practices and Perspectives Among US Primary Care Providers (2016–2017 Influenza Season). Journal of General Internal Medicine. 2019; 34:2167-75.
30. Changolkar S, Rareshide CAL, Snider CK, Patel MS. Patient, Physician, and Environmental Predictors of Influenza Vaccination During Primary Care Visits. Journal of General Internal Medicine. 2020; 35:611-3.
31. Dexter LJ, Teare MD, Dexter M, Siriwardena AN, Read RC. Strategies to increase influenza vaccination rates: outcomes of a nationwide cross-sectional survey of UK general practice. BMJ Open. 2012; 2:e000851.
32. Humiston SG, Bennett NM, Long C, Eberly S, Arvelo L, Stankaitis J, et al. Increasing Inner-City Adult Influenza Vaccination Rates: A Randomized Controlled Trial. Public Health Reports. 2011; 126:39-47.
33. Lu P-j, Srivastav A, Amaya A, Dever JA, Roycroft J, Kurtz MS, et al. Association of provider recommendation and offer and influenza vaccination among adults aged ≥18 years – United States. Vaccine. 2018; 36:890-8.
34. Murray K, Low C, O’Rourke A, Young F, Callanan I, Feeney E, et al. A quality improvement intervention failed to significantly increase pneumococcal and influenza vaccination rates in immunosuppressed inflammatory arthritis patients. Clinical Rheumatology. 2020; 39:747-54.
35. Nichol KL. Ten-year durability and success of an organized program to increase influenza and pneumococcal vaccination rates among high-risk adults. The American Journal of Medicine. 1998; 105:385-92.
36. Tan L. A review of the key factors to improve adult immunization coverage rates: What can the clinician do? Vaccine. 2018; 36:5373-8.
37. Tan LJ, VanOss R, Ofstead CL, Wetzler HP. Maximizing the impact of, and sustaining standing orders protocols for adult immunization in outpatient clinics. American Journal of Infection Control. 2020; 48:290-6.
38. Armstrong K, Berlin M, Schwartz JS, Propert K, Ubel PA. Barriers to influenza immunization in a low-income urban population. American Journal of Preventive Medicine. 2001; 20:21-5.
39. Chen JY, Fox, S. A., Cantrell, C. H., Stockdale, S. E., & Kagawa-Singer, M. . Health desparities and prevention: racial/ethnic barriers to flu vaccinations. J Community Health. 2007; 32:5-20.
40. Egede LE, Zheng D. Racial/Ethnic Differences in Influenza Vaccination Coverage in High-Risk Adults. American Journal of Public Health. 2003; 93:2074-8.
41. Frew PM, Painter JE, Hixson B, Kulb C, Moore K, del Rio C, et al. Factors mediating seasonal and influenza A (H1N1) vaccine acceptance among ethnically diverse populations in the urban south. Vaccine. 2012; 30:4200-8.
42. Zimmerman RK, Santibanez TA, Janosky JE, Fine MJ, Raymund M, Wilson SA, et al. What affects influenza vaccination rates among older patients? An analysis from inner-city, suburban, rural, and veterans affairs practices. The American Journal of Medicine. 2003; 114:31-8.
43. Louisiana State University Health Care Services Division. LSU Health Annual Report2011.
44. Vach W, Blettner M. Biased Estimation of the Odds Ratio in Case-Control Studies due to the Use of Ad Hoc Methods of Correcting for Missing Values for Confounding Variables. American Journal of Epidemiology. 1991; 134:895-907.
45. Department of Health and Human Services OoDPaHP. Healthy People 2020. Washington, D.C. [cited 2020 February 29th]; Available from: https://www.healthypeople.gov/2020/topics-objectives/topic/immunization-and-infectious-diseases/objectives.
46. Fine AD, Bridges CB, De Guzman AM, Glover L, Zeller B, Wong SJ, et al. Influenza A among Patients with Human Immunodeficiency Virus: An Outbreak of Infection at a Residential Facility in New York City. Clinical Infectious Diseases. 2001; 32:1784-91.
47. Radwan HM, Cheeseman SH, Lai KK, Ellison RT, III. Influenza in Human Immunodeficiency Virus-Infected Patients during the 1997–1998 Influenza Season. Clinical Infectious Diseases. 2000; 31:604-6.
48. Bennett KJ, Bellinger JD, Probst JC. Receipt of Influenza and Pneumonia Vaccinations: The Dual Disparity of Rural Minorities. Journal of the American Geriatrics Society. 2010; 58:1896-902.
49. Fiscella K, Franks P, Doescher MP, Saver BG. Disparities in health care by race, ethnicity, and language among the insured: findings from a national sample. Medical care. 2002; 40:52-9.
50. Johnson DR, Nichol KL, Lipczynski K. Barriers to Adult Immunization. The American Journal of Medicine. 2008; 121:S28-S35.
51. Winston CA, Wortley PM, Lees KA. Factors Associated with Vaccination of Medicare Beneficiaries in Five U.S. Communities: Results from the Racial and Ethnic Adult Disparities in Immunization Initiative Survey, 2003. Journal of the American Geriatrics Society. 2006; 54:303-10.
52. Yousey-Hindes KM, Hadler JL. Neighborhood Socioeconomic Status and Influenza Hospitalizations Among Children: New Haven County, Connecticut, 2003–2010. American Journal of Public Health. 2011; 101:1785-9.
53. Hebert PL, Frick KD, Kane RL, McBean AM. The Causes of Racial and Ethnic Differences in Influenza Vaccination Rates among Elderly Medicare Beneficiaries. Health Services Research. 2005; 40:517-38.
54. Wooten KG, Wortley PM, Singleton JA, Euler GL. Perceptions matter: Beliefs about influenza vaccine and vaccination behavior among elderly white, black and Hispanic Americans. Vaccine. 2012; 30:6927-34.