Get 20M+ Full-Text Papers For Less Than $1.50/day. Start a 14-Day Trial for You or Your Team.

Learn More →

Homelessness and Hepatitis A—San Diego County, 2016–2018

Homelessness and Hepatitis A—San Diego County, 2016–2018 Downloaded from https://academic.oup.com/cid/article/71/1/14/5550168 by DeepDyve user on 13 July 2022 Clinical Infectious Diseases MAJOR ARTICLE Homelessness and Hepatitis A—San Diego County, 2016–2018 1,2,3, 2 4 5 5 5 5 2 Corey M. Peak, Sarah S. Stous, Jessica M. Healy, Megan G. Hofmeister, Yulin Lin, Sumathi Ramachandran, Monique A. Foster, Annie Kao, and Eric C. McDonald 1 2 3 Epidemic Intelligence Service, Centers for Disease Control and Prevention, Atlanta, Georgia; County of San Diego Health and Human Services Agency, and Division of Global Migration and 4 5 Quarantine, Centers for Disease Control and Prevention, San Diego, California; and Divisions of Foodborne, Waterborne, and Environmental Diseases, and Viral Hepatitis, Centers for Disease Control and Prevention, Atlanta, Georgia Background. Hepatitis A  is a vaccine-preventable viral disease transmitted by the fecal-oral route. During 2016–2018, the County of San Diego investigated an outbreak of hepatitis A infections primarily among people experiencing homelessness (PEH) to identify risk factors and support control measures. At the time of the outbreak, homelessness was not recognized as an independent risk factor for the disease. Methods. We tested the association between homelessness and infection with hepatitis A  virus (HAV) using a test-negative study design comparing patients with laboratory-confirmed hepatitis A with control subjects who tested negative for HAV infection. We assessed risk factors for severe hepatitis A disease outcomes, including hospitalization and death, using multivariable logistic re- gression. We measured the frequency of indications for hepatitis A vaccination according to Advisory Committee on Immunization Practices (ACIP) guidelines. Results. Among 589 outbreak-associated cases reported, 291 (49%) occurred among PEH. Compared with those who were not homeless, PEH had 3.3 (95% confidence interval [CI], 1.5–7.9) times higher odds of HAV infection, 2.5 (95% CI, 1.7–3.9) times higher odds of hospitalization, and 3.9 (95% CI, 1.1–16.9) times higher odds of death associated with hepatitis A. Among PEH, 212 (73%) patients recorded other ACIP indications for hepatitis A vaccination. Conclusions. PEH were at higher risk of infection with HAV and of severe hepatitis A disease outcomes compared with those not experiencing homelessness. Approximately one-fourth of PEH had no other ACIP indication for hepatitis A vaccination. These findings support the recent ACIP recommendation to add homelessness as an indication for hepatitis A vaccination. Keywords. hepatitis A; homelessness; hepatitis A vaccine. Infection with hepatitis A  virus (HAV) is characterized by During November 2016–May 2018, San Diego County ex- acute onset of jaundice, fatigue, diarrhea, and other signs and perienced an outbreak of hepatitis A notable for a high propor- symptoms of acute liver infection. Transmission of HAV fol- tion of cases among people experiencing homelessness (PEH) lows the fecal-oral route through person-to-person contact or people who used illicit drugs (injection or noninjection) or ingestion of contaminated water or food, but can be inter- during their exposure period [3]. At the time of the outbreak, rupted through improvements in drinking water, sanitation, the Advisory Committee on Immunization Practices (ACIP) hygiene, and vaccination [1]. During 1994–1998, the County recommended hepatitis A vaccination for certain people rec- of San Diego Health and Human Services Agency (COSD) re- ognized to be at increased risk of HAV infection or severe ported approximately 500 hepatitis A cases per year [2]. After outcomes attributable to illness, including children, men the introduction of routine childhood hepatitis A vaccination who have sex with men (MSM), people who travel to coun- in California in 1999 and nationwide in 2006, the number of tries with high or intermediate rates of HAV, people who cases decreased to 40 or fewer cases each year, most of which use illicit drugs, and people who have chronic liver diseases were travel associated [2]. [4]. Although homelessness was not recognized as an inde- pendent risk factor for HAV infection at the time [4, 5], out- breaks of hepatitis A  in 2016–2018 in California, Michigan, Utah, Kentucky, and other states among similar risk groups Received 8 February 2019; editorial decision 7 August 2019; accepted 13 August 2019; pub- prompted consideration of homelessness as an independent lished online August 15, 2019. risk factor for HAV infection [6, 7]. On 24 October 2018, the Correspondence: C. M. Peak, Epidemic Intelligence Service, Centers for Disease Control and Prevention, 1600 Clifton Road, Atlanta, GA 30329, USA (coreypeak@gmail.com). ACIP voted to recommend adding homelessness to the list of Clinical Infectious Diseases 2020;71(1):14–21 hepatitis A vaccine indications [8]. Published by Oxford University Press for the Infectious Diseases Society of America 2019. This We investigated to assess whether homelessness was an inde- work is written by (a) US Government employee(s) and is in the public domain in the US. DOI: 10.1093/cid/ciz788 pendent risk factor for HAV infection and increased severity of 14 • cid 2020:71 (1 July) • Peak et al Downloaded from https://academic.oup.com/cid/article/71/1/14/5550168 by DeepDyve user on 13 July 2022 Case Assessment hepatitis A  disease during the outbreak in San Diego County. We defined a confirmed case as isolation of HAV genotype IB Additionally, we determined whether patients had 1 or more in a resident of San Diego County with acute onset of hepatitis known ACIP indications other than homelessness for hepatitis A symptoms during 1 November 2016–23 May 2018 (Table 1). A vaccination. In the absence of serum available for RT-PCR testing, we de- fined a probable case as signs or symptoms consistent with METHODS acute viral hepatitis, evidence of either jaundice or elevated Case Reporting and Investigation aminotransferase levels, and either positive IgM antibody to The COSD received reports of hepatitis A through routine clin- HAV or an epidemiologic link to a laboratory-confirmed case ical and laboratory surveillance and contacted patients while [12]. We defined a control subject as a patient reported by rou- hospitalized or by personal phone for interview. Upon de- tine surveillance to COSD for suspicion of hepatitis A but who tection of an increase in hepatitis A  reports in March 2017, a tested negative for HAV by RT-PCR. supplemental hypothesis-generating questionnaire was devel- oped with targeted questions on homelessness and illicit drug Risk Factor Analysis: Hepatitis A Virus Infection use to complement routine surveillance questions on clinical To test for an association between homelessness and infection symptoms, contact history, and other exposure information. with HAV, we used a test-negative study design comparing con- Homelessness was defined as self-reported lack of reliable firmed case-patients with control subjects. Because of the strict housing during the 2–7 weeks before illness onset. Vaccination use of RT-PCR criteria, probable cases were excluded from the indications according to ACIP at the time were assessed using test-negative study. We calculated crude and adjusted infec- information on history of international travel, illicit drug use, tion odds ratios (ORs) for homelessness using univariate and sexual exposures, and coinfection with either hepatitis B virus multivariable logistic regression models built by backwards (HBV) or hepatitis C virus (HCV) documented by hepatitis B stepwise selection (retention P < .10) of known risk factors for surface antigen positivity, HCV antibody positivity, or HCV HAV infection (ie, international travel, MSM, or illicit drug use) RNA detection. and age and sex. This time- and resource-efficient study design Serum specimens positive for immunoglobulin M (IgM) an- has been used to study risk factors for dengue [13] and more tibody to HAV were requested from the hospital or diagnostic broadly for estimating vaccine efficacy against influenza [14– laboratory to test for the presence of HAV RNA using reverse 16], rotavirus [17], cholera [18, 19], and pneumococcus [20]. transcriptase–polymerase chain reaction (RT-PCR), the most The method reduces misclassification bias through use of strict sensitive and widely used method for assessing HAV viremia laboratory criteria and reduces bias attributable to differential [9]. Serum specimens collected within 4 weeks aer sy ft mptom health-seeking behavior by including only those patients who onset were considered for testing. Next-generation sequencing sought care. was used to amplify a 315–base-pair fragment of the VP1-P2B region to differentiate the IB genotype attributed to the out- Risk Factor Analysis: Hepatitis A Disease Severity break from the genotypes common in North America, such To test for an association between homelessness and clinical se- as IA [10, 11]. Molecular characterization and genotype as- verity of hepatitis A, we assessed 2 outcomes as follows: hospi- sessment were conducted by the Centers for Disease Control talization and death from causes associated with hepatitis A. We and Prevention (CDC) Division of Viral Hepatitis Branch determined if death was associated with hepatitis A through ex- Laboratory, the California Department of Public Health Viral pert review of cause of death and contributing conditions listed and Rickettsial Disease Laboratory, and the San Diego Public on death certificates. Among confirmed and probable cases, we Health Laboratory. calculated crude and adjusted ORs between homelessness and Table 1. Assessment Criteria for Case Status and Inclusion in Risk Factor Analyses Risk Factor Analysis Positive for IgM RT-PCR Testing a b Clinical Presentation Antibody to HAV or Epi-link for HAV RNA HAV Infection Disease Severity Control subject Either Tested, negative Included … Confirmed case Positive Positive Tested, positive Included Included Probable case Positive Positive Not tested … Included Abbreviations: HAV, hepatitis A virus; IgM, immunoglobulin M; RT-PCR, reverse transcriptase–polymerase chain reaction. Acute illness with a discrete onset of any sign or symptom consistent with acute viral hepatitis (eg, fever, headache, malaise, anorexia, nausea, vomiting, diarrhea, and abdominal pain) and either (1) jaundice or (2) elevated serum alanine aminotransferase or aspartate aminotransferase. Epidemiologic link with a person who has laboratory-confirmed hepatitis A (ie, household or sexual contact with an infected person during the 15–50 days before the onset of symptoms). HAV RNA genotype IB only. Homelessness and Hepatitis A • cid 2020:71 (1 July) • 15 Downloaded from https://academic.oup.com/cid/article/71/1/14/5550168 by DeepDyve user on 13 July 2022 each outcome using univariate and multivariable logistic regres- to match 1 of the genotype IB strains (Table 2). Median patient sion models built by backwards selection (P < .10) of age, sex, age was 43 years (range, 5–87 years), 400 (68%) were male, and illicit drug use, MSM, and coinfection with either HBV or HCV. 404 (69%) were hospitalized. Among 20 (3%) patients who e Th CDC reviewed this study for human subjects protec- died of causes associated with hepatitis A, 19 (95%) had under- tion and deemed it to be nonresearch. Patient data were col- lying factors (eg, cirrhosis, diabetes, or cardiomyopathy) that lected confidentially by epidemiology program staff for public may have contributed to increased risk of severe outcomes, 14 health response activities and stored in a secure Confidential (70%) reported homelessness, and 2 (10%) had relapsing HAV Morbidity Report system by COSD. infection, defined as recurrent disease within 6 months of last recovery [21]. No patients reported having received the full, RESULTS 2-dose vaccination series before becoming infected. Among During 1 November 2016–23 May 2018, a total of 589 hepatitis the 589 confirmed and probable cases, outbreak risk factor data A cases were reported; 502 (85%) were confirmed by RT-PCR were available for 535 (91%), 200 (37%) of whom reported both Table 2. Patient Characteristics and Risk Factors Among Confirmed and Probable Cases—San Diego County, 2016–2018 All Confirmed and Patients Reporting Patients Not Reporting Probable Case-patients Homelessness Homelessness (N = 589) (N = 291) (N = 253) No. % No. % No. % Sex (male) 400 67.9 210 72.2 159 62.8 Case classification Confirmed 502 85.2 251 86.3 218 86.2 Probable 87 14.8 40 13.7 35 13.8 Clinical outcome Hospitalized 404 68.6 237 81.4 149 58.9 Died 20 3.4 14 4.8 5 2.0 Risk group Homeless and illicit drug use 200 34.0 200 68.7 … … Homeless only 91 15.4 91 31.3 … … Illicit drug use only 77 13.1 … … 66 26.1 Neither 167 28.4 … … 167 66.0 Unknown 54 9.2 … … 20 7.9 Signs and symptoms Dark urine 410 69.6 196 67.4 197 77.9 Jaundice 391 66.4 182 62.5 181 71.5 Vomiting 318 54.0 155 53.3 142 56.1 Fever 293 49.7 128 44.0 147 58.1 Diarrhea 223 37.9 134 46.0 81 32.0 Hepatitis coinfection HBV 25 5.1 16 6.5 6 2.9 HCV 83 17.5 61 25.0 14 7.2 ACIP vaccine indication Any 324 54.6 212 72.9 95 37.5 Illicit drug use 277 47.0 200 68.7 66 26.1 Coinfection with HBV or HCV 101 20.1 72 28.6 19 9.0 International travel 23 5.3 4 1.9 18 8.0 MSM 14 3.5 6 2.1 8 5.0 Aged <18 years 2 0.3 0 0.0 2 0.8 Median IQR Median IQR Median IQR Age, years 43 34–52 44 35–52 42 33–55 Laboratory results ALT, IU/L 1735 905–2801 1613 804–2635 1974 1090–3044 AST, IU/L 1226 417–2357 1328 412–2424 1234 435–2213 Total bilirubin, mg/dL 6.0 3.4–9.0 5.8 3.1–8.9 6.4 3.9–9.2 Abbreviations: ACIP, Advisory Committee on Immunization Practices; ALT, alanine aminotransferase; AST, aspartate aminotransferase; IQR, interquartile range; HBV, hepatitis B virus; HCV, hepatitis C virus; MSM, men who have sex with men. Data on homelessness was not available for 45 (7.6%) patients. Percentage of males. 16 • cid 2020:71 (1 July) • Peak et al Downloaded from https://academic.oup.com/cid/article/71/1/14/5550168 by DeepDyve user on 13 July 2022 Risk Factor Analysis: Hepatitis A Disease Severity homelessness and illicit drug use, 91 (17%) reported homeless- Among the 589 confirmed and probable cases, 404 (68%) pa- ness only, and 77 (14%) reported illicit drug use only. tients were hospitalized and 20 (3%) died. The OR for hospital- Among the 291 patients who reported experiencing home- ization was 3.1 (95% CI, 2.1–4.5) comparing patients reporting lessness, 79 (27%) did not report any other ACIP indications homelessness with those not reporting homelessness (Table 4). for vaccination (Table 2). Of the 212 (73%) PEH with at least 1 The adjusted OR for hospitalization was 2.5 (95% CI, 1.7–3.9) known indication, 200 (94%) reported illicit drug use, 72 (34%) after adjustment for illicit drug use and age. Hospitalization and were coinfected with HBV or HCV, 6 (2.8%) were MSM, and 4 death were more common as patient age increased (Figure 1). (1.9%) reported recent international travel to Mexico, which is The OR for death associated with hepatitis A  was not statis- a country with intermediate or high rates of HAV. tically significantly elevated at 2.5 (95% CI, .9–7.8), but after adjusting for age and coinfection with HBV or HCV, the odds Risk Factor Analysis: Hepatitis A Virus Infection of death were 3.9 (95% CI, 1.1–16.9) times higher for patients In total, 502 RT-PCR–confirmed case-patients and 96 control reporting homelessness than for those not reporting homeless- subjects with negative RT-PCR results were included for test- ness (Table 5). negative case-control analysis. Homelessness was reported by 251 (50%) case-patients and 23 (24%) control subjects; the DISCUSSION crude OR for infection was 2.4 (95% confidence interval [CI], 1.4–4.1) (Table 3). This association increased to 3.3 (95% CI, During a hepatitis A outbreak in San Diego County with ap- 1.5–7.9) after adjustment for age, sex, and international travel proximately 600 reported cases, we identified homelessness in the multiple logistic regression model. as an independent risk factor for HAV transmission and Table 3. Crude and Adjusted Logistic Regression Results from Risk Factor Analysis for Hepatitis A Virus Infection Confirmed Case-patients (N = 502) Control Subjects (N = 96) Adjusted Odds No. % No. % Odds Ratio (95% CI) Ratio (95% CI) Homelessness b b Yes 251 50.0 23 24.0 2.40 (1.43–4.14) 3.28 (1.52–7.90) No 218 43.4 48 50.0 Ref Ref Missing 33 6.6 25 26.0 … … Age, years b b Median 43 49 0.97 (.95–.98) per year 0.97 (.95–.99) per year Sex b b Male 334 66.5 46 47.9 2.17 (2.46–3.39) 2.31 (1.20–4.53) Female 167 32.3 50 52.1 Ref Ref Other 1 0.2 0 0.0 … … International travel b b Yes 36 7.2 9 9.4 0.23 (.10–0.57) 0.29 (.12–.75) No 360 71.7 36 37.5 Ref Ref Missing 106 21.1 51 53.1 … … Illicit drug use Yes 232 46.2 24 25.0 2.58 (1.59–4.30) … No 197 39.2 35 36.5 Ref … Missing 73 14.5 37 38.5 … … MSM Yes 11 2.2 1 1.0 2.46 (.47–45.5) … No 259 51.6 58 60.4 Ref … Missing 232 46.2 37 38.5 … … HBV or HCV coinfection Yes 81 16.1 11 11.5 1.08 (.68–1.82) … No 350 69.7 53 55.2 Ref … Missing 71 14.1 32 33.3 … … Abbreviations: CI, confidence interval; HBV, hepatitis B virus; HCV, hepatitis C virus; MSM, men who have sex with men; Ref, reference. Multivariable model including homelessness, age, sex, and history of international travel. Association significant at P < .05. Homelessness and Hepatitis A • cid 2020:71 (1 July) • 17 Downloaded from https://academic.oup.com/cid/article/71/1/14/5550168 by DeepDyve user on 13 July 2022 Table 4. Crude and Adjusted Logistic Regression Results From Risk Factor Analysis for Hospitalization Associated With Hepatitis A Among Confirmed and Probable Cases Hospitalized (N = 404) Not Hospitalized (N = 185) No. % No. % Odds Ratio (95% CI) Adjusted Odds Ratio (95% CI) Homelessness b b Yes 237 58.7 54 29.2 3.06 (2.09–4.54) 2.53 (1.66–3.88) No 149 36.9 104 25.8 Ref Ref Missing 18 6.7 27 6.7 … … Age, years Median 44 40 1.01 (1.00–1.03) per year 1.02 (1.00–1.03) per year Illicit drug use b b Yes 215 53.2 62 33.5 2.26 (1.58–3.26) 1.66 (1.07–2.57) No 142 35.1 78 42.2 Ref Ref Missing 47 11.6 45 24.3 … … HBV or HCV coinfection Yes 83 20.5 18 9.7 1.70 (1.17–2.55) … No 275 68.1 126 68.1 Ref … Missing 46 11.4 41 22.2 … … Sex Male 277 68.6 123 66.5 1.12 (.77–1.62) … Female 125 30.9 62 33.5 Ref … Other 2 0.5 0 0.0 … … MSM Yes 6 1.5 6 3.2 0.62 (.21–1.92) … No 199 49.3 92 49.7 Ref … Missing 199 49.3 87 47.0 … … Abbreviations: CI, confidence interval; HBV, hepatitis B virus; HCV, hepatitis C virus; MSM, men who have sex with men; Ref, reference. Multivariable model including homelessness, age, and illicit drug use. Association significant at P < .05. severe hepatitis A disease. Homelessness is a recognized risk high burden of homelessness may have contributed to the factor for a range of health conditions and diseases [22] and size and severity of this outbreak. Therefore, COSD targeted has been associated with outbreaks of hepatitis A in the past interventions toward PEH beginning with the recommenda- [23–25], but homelessness was not recognized by the ACIP tion to vaccinate PEH in the first health alert sent by the as an independent risk factor for hepatitis A infection at the county on 10 March 2017 [3]. To reach this population, ap- time of the outbreak [4, 5]. proximately 2500 HAV vaccination events occurred through PEH, especially those who are unsheltered, may be at in- stationary points of dispensary, mobile vans, and vaccina- creased risk of HAV infection because of high population den- tion foot teams consisting of a nurse and law enforcement sity and inadequate facilities for sanitation and hygiene and at officer [31]. Hepatitis A virus vaccinations were also admin- increased risk of severe outcomes because of a high prevalence istered by other community partners at homeless shelters, of associated comorbidities, malnutrition, and alcohol-related jails, emergency departments, and during influenza vacci- liver disease [26]. Studies have reported that homelessness may nation drives. Beyond vaccination, other interventions for be an independent risk factor for HAV antibody positivity [27], this risk group included transitional housing in tent cities, and targeted vaccination of PEH is feasible [28] and helped 24-hour public bathrooms and handwashing stations, en- control previous outbreaks among PEH [25]. Using the frame- hanced street sanitation, targeted health messaging, personal work of a recent consensus report from the National Academy hygiene kits, and temporary convalescent housing after hos- of Sciences [29], further research should assess whether hep- pital discharge [31]. atitis A  is a “housing-sensitive condition” from a public Case-fatality ratios from recent outbreaks, including San health perspective because of risks for PEH acquiring and Diego County, are higher than historical outbreaks and may transmitting HAV. result in part from a shifting case demographic toward older San Diego City and County, with an estimated 9116 people patients [11]. e Th increasing risk of hospitalization and death who were homeless in 2017, ranks fourth highest among US among older patients in this outbreak is consistent with pre- city areas and second only to Los Angeles in the number of vious studies that reported that case fatality increased with age people who are homeless and unsheltered [30]. The relatively from 0.1% among children aged less than 15 years, 0.3% among 18 • cid 2020:71 (1 July) • Peak et al Downloaded from https://academic.oup.com/cid/article/71/1/14/5550168 by DeepDyve user on 13 July 2022 Figure 1. Risk of hospitalization (A, B) and death (C, D) among confirmed and probable cases by homelessness and age quintile (ie, 0 to <33, 33 to <39, 39 to <55, and ≥55 years). people aged 15–39 years, and 2.1% among adults aged 40 years In this investigation, we suspect that the measured associa- or older [5, 32]. tion between homelessness and HAV infection is likely under- e Th median age of 43  years among confirmed and prob- estimated, because associations between homelessness and able cases is similar among patients reporting homelessness other causes of symptoms consistent with viral hepatitis in- (median, 44  years) and not reporting homelessness (median, fection may inflate the prevalence of homelessness among the 42 years) and is consistent with contemporaneous outbreaks in test-negative control subjects. Additionally, PEH may be pref- other states [11]. While the occurrence of hepatitis A  has de- erentially hospitalized for reasons beyond those measured [34, creased nationally in all age groups since 2000, incidence of the 35], but we expect that the outcome of case fatality is robust to disease is lowest among persons aged 0–9 years and 10–19 years this potential bias. compared with older age groups as of 2016 [33]. These findings strongly support the ACIP recommendation Our study limitations include possible misclassification of to add homelessness as an indication for hepatitis A vaccina- sensitive topics including homelessness status and history of il- tion [8], as well as the need to improve adult hepatitis A vac- licit drug use, although we expect such misclassification to be cination rates among groups who are at risk and to address independent of case-control status because of the delayed re- the underlying causes of homelessness [26]. Approximately ceipt of confirmatory RT-PCR test results. Self-reported vacci- half of all patients in this outbreak, and three-quarters of nation history was cross-referenced and supplemented using PEH, had at least 1 previously known ACIP indication for the San Diego Immunization Registry, although vaccinations vaccination (Table 2), yet none received the 2-dose HAV vac- received outside San Diego County are more likely to be missed. cination series before infection. Outbreak response vaccina- e p Th revalence of comorbidities may be underestimated by tion with 1 dose of HAV vaccine was found to be feasible in using coinfection status with HBV or HCV as an incomplete San Diego County and elsewhere [31, 36, 37], and previous surrogate for chronic liver disease caused by risk factors such as studies have shown that the single vaccine can confer protec- chronic alcoholism. tion for 4–11 years [38, 39]. Homelessness and Hepatitis A • cid 2020:71 (1 July) • 19 Downloaded from https://academic.oup.com/cid/article/71/1/14/5550168 by DeepDyve user on 13 July 2022 Table 5. Crude and Adjusted Logistic Regression Results From Risk Factor Analysis for Death Associated With Hepatitis A Among Confirmed and Probable Cases Died (N = 20) Survived (N = 569) No. % No. % Odds Ratio (95% CI) Adjusted Odds Ratio (95% CI) Homelessness Yes 14 70.0 277 48.7 2.51 (.94–7.85) 3.91 (1.14–16.9) No 5 25.0 248 43.4 Ref Ref Missing 1 5.0 44 7.7 … … Age, years b b Median 58 42 1.07 (1.04–1.11) per year 1.11 (1.07–1.17) per year HBV or HCV coinfection Yes 7 35.0 94 16.5 1.99 (.96–3.91) 2.52 (1.11–5.75) No 11 55.0 390 68.7 Ref Ref Missing 2 10.0 85 15.0 … … Illicit drug use Yes 4 20.0 273 48.0 0.34 (.09–1.07) … No 9 45.0 211 37.1 Ref … Missing 7 35.0 85 14.9 … … Sex Male 17 85.0 383 67.3 2.72 (.90–11.8) … Female 3 15.0 184 32.3 Ref … Other 0 0.0 2 0.4 … … Abbreviations: CI, confidence interval; HBV, hepatitis B virus; HCV, hepatitis C virus; Ref, reference. Multivariable model including homelessness, age, and HBV or HCV coinfection. Association significant at P < .05. Notes 7. Centers for Disease Control and Prevention. Outbreak of hepatitis A virus (HAV) infections among persons who use drugs and persons experiencing homelessness. Author contributions. C.  M. P.  and S.  S. S.  analyzed the information. 2018. CDC Health Alert Network. Available at: https://emergency.cdc.gov/han/ Y. L. and S. R. performed molecular testing and analysis. C. M. P., S. S. S., han00412.asp. Accessed 21 August 2019. and E. C. M. wrote the initial draft. All authors contributed to the writing, 8. Doshani M, Weng M, Moore KL, Romero JR, Nelson NP. Recommendations revision, and finalization of the manuscript. of the Advisory Committee on Immunization Practices for use of hepatitis Acknowledgments. e a Th uthors acknowledge helpful feedback from A  vaccine for persons experiencing homelessness. Morb Mortal Wkly Rep. Mark Sawyer on conceptualizing this paper and from Wences Arvelo on 2019; 68:153–6. revising versions of the paper. 9. Nainan OV, Xia G, Vaughan G, Margolis HS. Diagnosis of hepatitis a virus infec- tion: a molecular approach. Clin Microbiol Rev 2006; 19:63–79. Disclaimer. e fin Th dings and conclusions in this report are those of the 10. Association of Public Health Laboratories. Hepatitis A  virus testing and re- authors and do not necessarily represent the official position of the Centers sources. 2018;1–3. Available at: https://www.aphl.org/programs/infectious_di- for Disease Control and Prevention. sease/Documents/2018_HAV_DiagnosticUpdate.pdf. Accessed 21 August 2019. Potential coni fl cts of interest. e a Th uthors report no potential conflicts 11. Foster  M, Ramachandran  S, Myatt  K, et  al. Hepatitis A  virus outbreaks associ- of interest. All authors have submitted the ICMJE Form for Disclosure of ated with drug use and homelessness—California, Kentucky, Michigan, and Utah, Potential Conflicts of Interest. Conflicts that the editors consider relevant to 2017. Morb Mortal Wkly Rep 2018; 67:2017–9. the content of the manuscript have been disclosed. 12. Council of State and Territorial Epidemiologists. Public health reporting and national notification for hepatitis A. 2011. Available at: www.cste.org/resource/ resmgr/PS/11-ID-02.pdf. Accessed 21 August 2019. References 13. Yung CF, Chan SP, Thein TL, Chai SC, Leo YS. Epidemiological risk factors for 1. Centers for Disease Control and Prevention. Hepatitis A. In: Hamborsky J, Kroger adult dengue in Singapore: an 8-year nested test negative case control study. BMC A, Wolfe S, eds. Epidemiology and prevention of vaccine-preventable diseases. Infect Dis 2016; 16:323. 13th ed. Washington, DC: Public Health Foundation, 2015. 14. Fukushima W, Hirota Y. Basic principles of test-negative design in evaluating in- 2. County of San Diego Health and Human Services Agency. San Diego County fluenza vaccine effectiveness. Vaccine 2017; 35:4796–800. Annual Communicable Disease Report. 2016. 15. Sullivan  SG, Tchetgen  Tchetgen  EJ, Cowling  BJ. Theoretical basis of the test- 3. County of San Diego Health and Human Services Agency. Hepatitis A  virus negative study design for assessment of influenza vaccine effectiveness. Am J outbreak associated with homelessness, drug use in San Diego County. Epidemiol 2016; 184:345–53. 2017; Available at: https://www.sandiegocounty.gov/content/dam/sdc/hhsa/ 16. Belongia EA, Simpson MD, King JP, et al. Variable influenza vaccine effectiveness programs/phs/cahan/communications_documents/03-10-17.pdf. Accessed 21 by subtype: a systematic review and meta-analysis of test-negative design studies. August 2019. Lancet Infect Dis 2016; 16:942–51. 4. Centers for Disease Control and Prevention. Prevention of hepatitis A  through 17. Bar-Zeev  N, Kapanda  L, Tate  JE, et  al. Effectiveness of a monovalent rotavirus active or passive immunization: recommendations of the Advisory Committee on vaccine in infants in Malawi after programmatic roll-out: an observational and Immunization Practices (ACIP). Morb Mortal Wkly Rep 2006; 55:1–23. case-control study. Lancet Infect Dis 2015 15(4):422–8. 5. World Health Organization. WHO position paper on hepatitis A vaccines—June 18. Azman AS, Parker LA, Rumunu J, et al. Effectiveness of one dose of oral cholera 2012. Wkly Epidemiol Rec 2012; 87:261–76. Available at: https://www.who.int/ vaccine in response to an outbreak: a case-cohort study. Lancet Glob Health 2016; wer/2012/wer8728_29/en/. Accessed 21 August 2019. 4:e856–63. 6. Centers for Disease Control and Prevention. Advisory Committee on 19. Franke MF, Jerome JG, Matias WR, et al. Comparison of two control groups for Immunization Practices (ACIP) summary report. 2017. Available at: https:// estimation of oral cholera vaccine effectiveness using a case-control study design. stacks.cdc.gov/view/cdc/58894. Accessed 21 August 2019. Vaccine 2017; 35:5819–27. 20 • cid 2020:71 (1 July) • Peak et al Downloaded from https://academic.oup.com/cid/article/71/1/14/5550168 by DeepDyve user on 13 July 2022 20. Broome CV, Facklam RR, Fraser DW. Pneumococcal disease after pneumococcal catalog/25133/permanent-supportive-housing-evaluating-the-evidence-for- vaccination: an alternative method to estimate the efficacy of pneumococcal vac- improving-health-outcomes. Accessed 21 August 2019. cine. N Engl J Med 1980; 303:549–52. 30. Regional Task Force on the Homeless. WeALLCount annual comprehensive 21. Glickson  M, Galun  E, Oren  R, Tur-Kaspa  R, Shouval  D. Relapsing Hepatitis A: report. San Diego, 2017. Available at: http://www.rtfhsd.org/wp-content/up- review of 14 cases and literature survey. Medicine 1992; 71: 14–23. loads/2017/07/comp-report-final.pdf. Accessed 21 August 2019. 22. Aldridge  RW, Story  A, Hwang  SW, et  al. Morbidity and mortality in homeless 31. County of San Diego. Hepatitis A  outbreak after action report. 2018. Available individuals, prisoners, sex workers, and individuals with substance use disorders at: https://www.sandiegocounty.gov/content/dam/sdc/cosd/SanDiegoHepatitis in high-income countries: a systematic review and meta-analysis. Lancet 2018; AOutbreak-2017-18-AfterActionReport.pdf. Accessed 21 August 2019. 391:241–50. 32. Hollinger F, Ticehurst J. Hepatitis A. In: Fields virology. Philadelphia: Lippincott- 23. Syed NA, Hearing SD, Shaw IS, et al. Outbreak of hepatitis A in the injecting drug Raven, 1996:735–82. user and homeless populations in Bristol: control by a targeted vaccination pro- 33. Centers for Disease Control and Prevention. Viral hepatitis surveillance— gramme and possible parenteral transmission. Eur J Gastroenterol Hepatol 2003; United States, 2016. Available at: https://www.cdc.gov/hepatitis/statistics/ 15:901–6. 2016surveillance/pdfs/2016HepSurveillanceRpt.pdf. Accessed 21 August 2019. 24. Tjon GMS, Götz H, Koek AG, et al. An outbreak of hepatitis A among homeless 34. Salit SA, Kuhn EM, Hartz AJ, Vu JM, Mosso AL. Hospitalization costs associated drug users in Rotterdam, The Netherlands. J Med Virol 2005; 77:360–6. with homelessness in New York City. N Engl J Med 1998; 338:1734–40. 25. James TL, Aschkenasy M, Eliseo LJ, Olshaker J, Mehta SD. Response to hepatitis 35. Feigal J, Park B, Bramante C, Nordgaard C, Menk J, Song J. Homelessness and dis- A  epidemic: emergency department collaboration with public health commis- charge delays from an urban safety net hospital. Public Health 2014; 128:1033–5. sion. J Emerg Med 2009; 36:412–6. 36. McMahon BJ, Beller M, Williams J, Schloss M, Tanttila H, Bulkow L. A program 26. Kushel M. Hepatitis A outbreak in California—addressing the root cause. N Engl to control an outbreak of hepatitis A in Alaska by using an inactivated hepatitis J Med 2018; 378:211–3. A vaccine. Arch Pediatr Adolesc Med 1996; 150:733–9. 27. Hennessey  KA, Bangsberg  DR, Weinbaum  C, Hahn  JA. Hepatitis A  seropreva- 37. Zamir C, Rishpon S, Zamir D, Leventhal A, Rimon N, Ben-Porath E. Control of lence and risk factors among homeless adults in San Francisco: should homeless- a community-wide outbreak of hepatitis A by mass vaccination with inactivated ness be included in the risk-based strategy for vaccination? Public Health Rep hepatitis A vaccine. Eur J Clin Microbiol Infect Dis 2001; 20:185–7. 2009; 124:813–7. 38. Hatz  C, van  der  Ploeg  R, Beck  BR, Frösner  G, Hunt  M, Herzog  C. Successful 28. Poulos  RG, Ferson  MJ, Orr  KJ, et  al. Vaccination against hepatitis A  and B in memory response following a booster dose with a virosome-formulated hepatitis persons subject to homelessness in inner Sydney: vaccine acceptance, completion A vaccine delayed up to 11 years. Clin Vaccine Immunol 2011; 18:885–7. rates and immunogenicity. Aust N Z J Public Health 2010; 34:130–5. 39. Iwarson  S, Lindh  M, Widerström  L. Excellent booster response 4-6 y after a 29. National Academy of Sciences. Permanent supportive housing. Washington, single primary dose of an inactivated hepatitis A vaccine. Scand J Infect Dis 2002; DC: National Academies Press, 2018. Available at: https://www.nap.edu/ 34:110–1. Homelessness and Hepatitis A • cid 2020:71 (1 July) • 21 Please excuse the presence of this and the following test pages, which have been added to a small number of article PDFs for a limited time as part of our process of continual development and improvement. academic.oup.com/cid 1 of 4 academic.oup.com/cid Lorem ipsum dolor sit amet, consectetur adipiscing elit, sed do eiusmod tempor incididunt ut labore et dolore magna aliqua. Ut enim ad minim veniam, quis nostrud exercitation ullamco laboris nisi ut aliquip ex ea commodo consequat. Duis aute irure dolor in reprehenderit in voluptate velit esse cillum dolore eu fugiat nulla pariatur. Excepteur sint occaecat cupidatat non proident, sunt in culpa qui officia deserunt mollit anim id est laborum. Lorem ipsum dolor sit amet, consectetur adipiscing elit, sed do eiusmod tempor incididunt ut labore et dolore magna aliqua. Ut enim ad minim veniam, quis nostrud exercitation ullamco laboris nisi ut aliquip ex ea commodo consequat. Duis aute irure dolor in reprehenderit in voluptate velit esse cillum dolore eu fugiat nulla pariatur. Excepteur sint occaecat cupidatat non proident, sunt in culpa qui officia deserunt mollit anim id est laborum. Lorem ipsum dolor sit amet, consectetur adipiscing elit, sed do eiusmod tempor incididunt ut labore et dolore magna aliqua. Ut enim ad minim veniam, quis nostrud exercitation ullamco laboris nisi ut aliquip ex ea commodo consequat. Duis aute irure dolor in reprehenderit in voluptate velit esse cillum dolore eu fugiat nulla pariatur. Excepteur sint occaecat cupidatat non proident, sunt in culpa qui officia deserunt mollit anim id est laborum. Lorem ipsum dolor sit amet, consectetur adipiscing elit, sed do eiusmod tempor incididunt ut labore et dolore magna aliqua. Ut enim ad minim veniam, quis nostrud exercitation ullamco laboris nisi ut aliquip ex ea commodo consequat. Duis aute irure dolor in reprehenderit in voluptate velit esse cillum dolore eu fugiat nulla pariatur. Excepteur sint occaecat cupidatat non proident, sunt in culpa qui officia deserunt mollit anim id est laborum. Lorem ipsum dolor sit amet, consectetur adipiscing elit, sed do eiusmod tempor incididunt ut labore et dolore magna aliqua. Ut enim ad minim veniam, quis nostrud exercitation ullamco laboris nisi ut aliquip ex ea commodo consequat. Duis aute irure dolor in reprehenderit in voluptate velit esse cillum dolore eu fugiat nulla pariatur. Excepteur sint occaecat cupidatat non proident, sunt in culpa qui officia deserunt mollit anim id est laborum. Lorem ipsum dolor sit amet, consectetur adipiscing elit, sed do eiusmod tempor incididunt ut labore et dolore magna aliqua. Ut enim ad minim veniam, quis nostrud exercitation ullamco laboris nisi ut aliquip ex ea commodo consequat. Duis aute irure dolor in reprehenderit in voluptate velit esse cillum dolore eu fugiat nulla pariatur. Excepteur sint occaecat cupidatat non proident, sunt in culpa qui officia deserunt mollit anim id est laborum. Lorem ipsum dolor sit amet, consectetur adipiscing elit, sed do academic.oup.com/cid 2 of 4 eiusmod tempor incididunt ut labore et dolore magna aliqua. Ut enim ad minim veniam, quis nostrud exercitation ullamco laboris nisi ut aliquip ex ea commodo consequat. Duis aute irure dolor in reprehenderit in voluptate velit esse cillum dolore eu fugiat nulla pariatur. Excepteur sint occaecat cupidatat non proident, sunt in culpa qui officia deserunt mollit anim id est laborum. Lorem ipsum dolor sit amet, consectetur adipiscing elit, sed do eiusmod tempor incididunt ut labore et dolore magna aliqua. Ut enim ad minim veniam, quis nostrud exercitation ullamco laboris nisi ut aliquip ex ea commodo consequat. Duis aute irure dolor in reprehenderit in voluptate velit esse cillum dolore eu fugiat nulla pariatur. Excepteur sint occaecat cupidatat non proident, sunt in culpa qui officia deserunt mollit anim id est laborum. Lorem ipsum dolor sit amet, consectetur adipiscing elit, sed do eiusmod tempor incididunt ut labore et dolore magna aliqua. Ut enim ad minim veniam, quis nostrud exercitation ullamco laboris nisi ut aliquip ex ea commodo consequat. Duis aute irure dolor in reprehenderit in voluptate velit esse cillum dolore eu fugiat nulla pariatur. Excepteur sint occaecat cupidatat non proident, sunt in culpa qui officia deserunt mollit anim id est laborum. Lorem ipsum dolor sit amet, consectetur adipiscing elit, sed do eiusmod tempor incididunt ut labore et dolore magna aliqua. Ut enim ad minim veniam, quis nostrud exercitation ullamco laboris nisi ut aliquip ex ea commodo consequat. Duis aute irure dolor in reprehenderit in voluptate velit esse cillum dolore eu fugiat nulla pariatur. Excepteur sint occaecat cupidatat non proident, sunt in culpa qui officia deserunt mollit anim id est laborum. Lorem ipsum dolor sit amet, consectetur adipiscing elit, sed do eiusmod tempor incididunt ut labore et dolore magna aliqua. Ut enim ad minim veniam, quis nostrud exercitation ullamco laboris nisi ut aliquip ex ea commodo consequat. Duis aute irure dolor in reprehenderit in voluptate velit esse cillum dolore eu fugiat nulla pariatur. Excepteur sint occaecat cupidatat non proident, sunt in culpa qui officia deserunt mollit anim id est laborum. Lorem ipsum dolor sit amet, consectetur adipiscing elit, sed do eiusmod tempor incididunt ut labore et dolore magna aliqua. Ut enim ad minim veniam, quis nostrud exercitation ullamco laboris nisi ut aliquip ex ea commodo consequat. Duis aute irure dolor in reprehenderit in voluptate velit esse cillum dolore eu fugiat nulla pariatur. Excepteur sint occaecat cupidatat non proident, sunt in culpa qui officia deserunt mollit anim id est laborum. Lorem ipsum dolor sit amet, consectetur adipiscing elit, sed do eiusmod tempor incididunt ut labore et dolore magna aliqua. academic.oup.com/cid 3 of 4 Ut enim ad minim veniam, quis nostrud exercitation ullamco laboris nisi ut aliquip ex ea commodo consequat. Duis aute irure dolor in reprehenderit in voluptate velit esse cillum dolore eu fugiat nulla pariatur. Excepteur sint occaecat cupidatat non proident, sunt in culpa qui officia deserunt mollit anim id est laborum. Lorem ipsum dolor sit amet, consectetur adipiscing elit, sed do eiusmod tempor incididunt ut labore et dolore magna aliqua. Ut enim ad minim veniam, quis nostrud exercitation ullamco laboris nisi ut aliquip ex ea commodo consequat. Duis aute irure dolor in reprehenderit in voluptate velit esse cillum dolore eu fugiat nulla pariatur. Excepteur sint occaecat cupidatat non proident, sunt in culpa qui officia deserunt mollit anim id est laborum. Lorem ipsum dolor sit amet, consectetur adipiscing elit, sed do eiusmod tempor incididunt ut labore et dolore magna aliqua. Ut enim ad minim veniam, quis nostrud exercitation ullamco laboris nisi ut aliquip ex ea commodo consequat. Duis aute irure dolor in reprehenderit in voluptate velit esse cillum dolore eu fugiat nulla pariatur. Excepteur sint occaecat cupidatat non proident, sunt in culpa qui officia deserunt mollit anim id est laborum. Lorem ipsum dolor sit amet, consectetur adipiscing elit, sed do eiusmod tempor incididunt ut labore et dolore magna aliqua. Ut enim ad minim veniam, quis nostrud exercitation ullamco laboris nisi ut aliquip ex ea commodo consequat. Duis aute irure dolor in reprehenderit in voluptate velit esse cillum dolore eu fugiat nulla pariatur. Excepteur sint occaecat cupidatat non proident, sunt in culpa qui officia deserunt mollit anim id est laborum. Lorem ipsum dolor sit amet, consectetur adipiscing elit, sed do eiusmod tempor incididunt ut labore et dolore magna aliqua. Ut enim ad minim veniam, quis nostrud exercitation ullamco laboris nisi ut aliquip ex ea commodo consequat. Duis aute irure dolor in reprehenderit in voluptate velit esse cillum dolore eu fugiat nulla pariatur. Excepteur sint occaecat cupidatat non proident, sunt in culpa qui officia deserunt mollit anim id est laborum. Lorem ipsum dolor sit amet, consectetur adipiscing elit, sed do eiusmod tempor incididunt ut labore et dolore magna aliqua. Ut enim ad minim veniam, quis nostrud exercitation ullamco laboris nisi ut aliquip ex ea commodo consequat. Duis aute irure dolor in reprehenderit in voluptate velit esse cillum dolore eu fugiat nulla pariatur. Excepteur sint occaecat cupidatat non proident, sunt in culpa qui officia deserunt mollit anim id est laborum. academic.oup.com/cid 4 of 4 http://www.deepdyve.com/assets/images/DeepDyve-Logo-lg.png Clinical Infectious Diseases Oxford University Press

Loading next page...
 
/lp/oxford-university-press/homelessness-and-hepatitis-a-san-diego-county-2016-2018-lF6oIIB2FD

References (39)

Publisher
Oxford University Press
Copyright
Copyright © 2022 Infectious Diseases Society of America
ISSN
1058-4838
eISSN
1537-6591
DOI
10.1093/cid/ciz788
Publisher site
See Article on Publisher Site

Abstract

Downloaded from https://academic.oup.com/cid/article/71/1/14/5550168 by DeepDyve user on 13 July 2022 Clinical Infectious Diseases MAJOR ARTICLE Homelessness and Hepatitis A—San Diego County, 2016–2018 1,2,3, 2 4 5 5 5 5 2 Corey M. Peak, Sarah S. Stous, Jessica M. Healy, Megan G. Hofmeister, Yulin Lin, Sumathi Ramachandran, Monique A. Foster, Annie Kao, and Eric C. McDonald 1 2 3 Epidemic Intelligence Service, Centers for Disease Control and Prevention, Atlanta, Georgia; County of San Diego Health and Human Services Agency, and Division of Global Migration and 4 5 Quarantine, Centers for Disease Control and Prevention, San Diego, California; and Divisions of Foodborne, Waterborne, and Environmental Diseases, and Viral Hepatitis, Centers for Disease Control and Prevention, Atlanta, Georgia Background. Hepatitis A  is a vaccine-preventable viral disease transmitted by the fecal-oral route. During 2016–2018, the County of San Diego investigated an outbreak of hepatitis A infections primarily among people experiencing homelessness (PEH) to identify risk factors and support control measures. At the time of the outbreak, homelessness was not recognized as an independent risk factor for the disease. Methods. We tested the association between homelessness and infection with hepatitis A  virus (HAV) using a test-negative study design comparing patients with laboratory-confirmed hepatitis A with control subjects who tested negative for HAV infection. We assessed risk factors for severe hepatitis A disease outcomes, including hospitalization and death, using multivariable logistic re- gression. We measured the frequency of indications for hepatitis A vaccination according to Advisory Committee on Immunization Practices (ACIP) guidelines. Results. Among 589 outbreak-associated cases reported, 291 (49%) occurred among PEH. Compared with those who were not homeless, PEH had 3.3 (95% confidence interval [CI], 1.5–7.9) times higher odds of HAV infection, 2.5 (95% CI, 1.7–3.9) times higher odds of hospitalization, and 3.9 (95% CI, 1.1–16.9) times higher odds of death associated with hepatitis A. Among PEH, 212 (73%) patients recorded other ACIP indications for hepatitis A vaccination. Conclusions. PEH were at higher risk of infection with HAV and of severe hepatitis A disease outcomes compared with those not experiencing homelessness. Approximately one-fourth of PEH had no other ACIP indication for hepatitis A vaccination. These findings support the recent ACIP recommendation to add homelessness as an indication for hepatitis A vaccination. Keywords. hepatitis A; homelessness; hepatitis A vaccine. Infection with hepatitis A  virus (HAV) is characterized by During November 2016–May 2018, San Diego County ex- acute onset of jaundice, fatigue, diarrhea, and other signs and perienced an outbreak of hepatitis A notable for a high propor- symptoms of acute liver infection. Transmission of HAV fol- tion of cases among people experiencing homelessness (PEH) lows the fecal-oral route through person-to-person contact or people who used illicit drugs (injection or noninjection) or ingestion of contaminated water or food, but can be inter- during their exposure period [3]. At the time of the outbreak, rupted through improvements in drinking water, sanitation, the Advisory Committee on Immunization Practices (ACIP) hygiene, and vaccination [1]. During 1994–1998, the County recommended hepatitis A vaccination for certain people rec- of San Diego Health and Human Services Agency (COSD) re- ognized to be at increased risk of HAV infection or severe ported approximately 500 hepatitis A cases per year [2]. After outcomes attributable to illness, including children, men the introduction of routine childhood hepatitis A vaccination who have sex with men (MSM), people who travel to coun- in California in 1999 and nationwide in 2006, the number of tries with high or intermediate rates of HAV, people who cases decreased to 40 or fewer cases each year, most of which use illicit drugs, and people who have chronic liver diseases were travel associated [2]. [4]. Although homelessness was not recognized as an inde- pendent risk factor for HAV infection at the time [4, 5], out- breaks of hepatitis A  in 2016–2018 in California, Michigan, Utah, Kentucky, and other states among similar risk groups Received 8 February 2019; editorial decision 7 August 2019; accepted 13 August 2019; pub- prompted consideration of homelessness as an independent lished online August 15, 2019. risk factor for HAV infection [6, 7]. On 24 October 2018, the Correspondence: C. M. Peak, Epidemic Intelligence Service, Centers for Disease Control and Prevention, 1600 Clifton Road, Atlanta, GA 30329, USA (coreypeak@gmail.com). ACIP voted to recommend adding homelessness to the list of Clinical Infectious Diseases 2020;71(1):14–21 hepatitis A vaccine indications [8]. Published by Oxford University Press for the Infectious Diseases Society of America 2019. This We investigated to assess whether homelessness was an inde- work is written by (a) US Government employee(s) and is in the public domain in the US. DOI: 10.1093/cid/ciz788 pendent risk factor for HAV infection and increased severity of 14 • cid 2020:71 (1 July) • Peak et al Downloaded from https://academic.oup.com/cid/article/71/1/14/5550168 by DeepDyve user on 13 July 2022 Case Assessment hepatitis A  disease during the outbreak in San Diego County. We defined a confirmed case as isolation of HAV genotype IB Additionally, we determined whether patients had 1 or more in a resident of San Diego County with acute onset of hepatitis known ACIP indications other than homelessness for hepatitis A symptoms during 1 November 2016–23 May 2018 (Table 1). A vaccination. In the absence of serum available for RT-PCR testing, we de- fined a probable case as signs or symptoms consistent with METHODS acute viral hepatitis, evidence of either jaundice or elevated Case Reporting and Investigation aminotransferase levels, and either positive IgM antibody to The COSD received reports of hepatitis A through routine clin- HAV or an epidemiologic link to a laboratory-confirmed case ical and laboratory surveillance and contacted patients while [12]. We defined a control subject as a patient reported by rou- hospitalized or by personal phone for interview. Upon de- tine surveillance to COSD for suspicion of hepatitis A but who tection of an increase in hepatitis A  reports in March 2017, a tested negative for HAV by RT-PCR. supplemental hypothesis-generating questionnaire was devel- oped with targeted questions on homelessness and illicit drug Risk Factor Analysis: Hepatitis A Virus Infection use to complement routine surveillance questions on clinical To test for an association between homelessness and infection symptoms, contact history, and other exposure information. with HAV, we used a test-negative study design comparing con- Homelessness was defined as self-reported lack of reliable firmed case-patients with control subjects. Because of the strict housing during the 2–7 weeks before illness onset. Vaccination use of RT-PCR criteria, probable cases were excluded from the indications according to ACIP at the time were assessed using test-negative study. We calculated crude and adjusted infec- information on history of international travel, illicit drug use, tion odds ratios (ORs) for homelessness using univariate and sexual exposures, and coinfection with either hepatitis B virus multivariable logistic regression models built by backwards (HBV) or hepatitis C virus (HCV) documented by hepatitis B stepwise selection (retention P < .10) of known risk factors for surface antigen positivity, HCV antibody positivity, or HCV HAV infection (ie, international travel, MSM, or illicit drug use) RNA detection. and age and sex. This time- and resource-efficient study design Serum specimens positive for immunoglobulin M (IgM) an- has been used to study risk factors for dengue [13] and more tibody to HAV were requested from the hospital or diagnostic broadly for estimating vaccine efficacy against influenza [14– laboratory to test for the presence of HAV RNA using reverse 16], rotavirus [17], cholera [18, 19], and pneumococcus [20]. transcriptase–polymerase chain reaction (RT-PCR), the most The method reduces misclassification bias through use of strict sensitive and widely used method for assessing HAV viremia laboratory criteria and reduces bias attributable to differential [9]. Serum specimens collected within 4 weeks aer sy ft mptom health-seeking behavior by including only those patients who onset were considered for testing. Next-generation sequencing sought care. was used to amplify a 315–base-pair fragment of the VP1-P2B region to differentiate the IB genotype attributed to the out- Risk Factor Analysis: Hepatitis A Disease Severity break from the genotypes common in North America, such To test for an association between homelessness and clinical se- as IA [10, 11]. Molecular characterization and genotype as- verity of hepatitis A, we assessed 2 outcomes as follows: hospi- sessment were conducted by the Centers for Disease Control talization and death from causes associated with hepatitis A. We and Prevention (CDC) Division of Viral Hepatitis Branch determined if death was associated with hepatitis A through ex- Laboratory, the California Department of Public Health Viral pert review of cause of death and contributing conditions listed and Rickettsial Disease Laboratory, and the San Diego Public on death certificates. Among confirmed and probable cases, we Health Laboratory. calculated crude and adjusted ORs between homelessness and Table 1. Assessment Criteria for Case Status and Inclusion in Risk Factor Analyses Risk Factor Analysis Positive for IgM RT-PCR Testing a b Clinical Presentation Antibody to HAV or Epi-link for HAV RNA HAV Infection Disease Severity Control subject Either Tested, negative Included … Confirmed case Positive Positive Tested, positive Included Included Probable case Positive Positive Not tested … Included Abbreviations: HAV, hepatitis A virus; IgM, immunoglobulin M; RT-PCR, reverse transcriptase–polymerase chain reaction. Acute illness with a discrete onset of any sign or symptom consistent with acute viral hepatitis (eg, fever, headache, malaise, anorexia, nausea, vomiting, diarrhea, and abdominal pain) and either (1) jaundice or (2) elevated serum alanine aminotransferase or aspartate aminotransferase. Epidemiologic link with a person who has laboratory-confirmed hepatitis A (ie, household or sexual contact with an infected person during the 15–50 days before the onset of symptoms). HAV RNA genotype IB only. Homelessness and Hepatitis A • cid 2020:71 (1 July) • 15 Downloaded from https://academic.oup.com/cid/article/71/1/14/5550168 by DeepDyve user on 13 July 2022 each outcome using univariate and multivariable logistic regres- to match 1 of the genotype IB strains (Table 2). Median patient sion models built by backwards selection (P < .10) of age, sex, age was 43 years (range, 5–87 years), 400 (68%) were male, and illicit drug use, MSM, and coinfection with either HBV or HCV. 404 (69%) were hospitalized. Among 20 (3%) patients who e Th CDC reviewed this study for human subjects protec- died of causes associated with hepatitis A, 19 (95%) had under- tion and deemed it to be nonresearch. Patient data were col- lying factors (eg, cirrhosis, diabetes, or cardiomyopathy) that lected confidentially by epidemiology program staff for public may have contributed to increased risk of severe outcomes, 14 health response activities and stored in a secure Confidential (70%) reported homelessness, and 2 (10%) had relapsing HAV Morbidity Report system by COSD. infection, defined as recurrent disease within 6 months of last recovery [21]. No patients reported having received the full, RESULTS 2-dose vaccination series before becoming infected. Among During 1 November 2016–23 May 2018, a total of 589 hepatitis the 589 confirmed and probable cases, outbreak risk factor data A cases were reported; 502 (85%) were confirmed by RT-PCR were available for 535 (91%), 200 (37%) of whom reported both Table 2. Patient Characteristics and Risk Factors Among Confirmed and Probable Cases—San Diego County, 2016–2018 All Confirmed and Patients Reporting Patients Not Reporting Probable Case-patients Homelessness Homelessness (N = 589) (N = 291) (N = 253) No. % No. % No. % Sex (male) 400 67.9 210 72.2 159 62.8 Case classification Confirmed 502 85.2 251 86.3 218 86.2 Probable 87 14.8 40 13.7 35 13.8 Clinical outcome Hospitalized 404 68.6 237 81.4 149 58.9 Died 20 3.4 14 4.8 5 2.0 Risk group Homeless and illicit drug use 200 34.0 200 68.7 … … Homeless only 91 15.4 91 31.3 … … Illicit drug use only 77 13.1 … … 66 26.1 Neither 167 28.4 … … 167 66.0 Unknown 54 9.2 … … 20 7.9 Signs and symptoms Dark urine 410 69.6 196 67.4 197 77.9 Jaundice 391 66.4 182 62.5 181 71.5 Vomiting 318 54.0 155 53.3 142 56.1 Fever 293 49.7 128 44.0 147 58.1 Diarrhea 223 37.9 134 46.0 81 32.0 Hepatitis coinfection HBV 25 5.1 16 6.5 6 2.9 HCV 83 17.5 61 25.0 14 7.2 ACIP vaccine indication Any 324 54.6 212 72.9 95 37.5 Illicit drug use 277 47.0 200 68.7 66 26.1 Coinfection with HBV or HCV 101 20.1 72 28.6 19 9.0 International travel 23 5.3 4 1.9 18 8.0 MSM 14 3.5 6 2.1 8 5.0 Aged <18 years 2 0.3 0 0.0 2 0.8 Median IQR Median IQR Median IQR Age, years 43 34–52 44 35–52 42 33–55 Laboratory results ALT, IU/L 1735 905–2801 1613 804–2635 1974 1090–3044 AST, IU/L 1226 417–2357 1328 412–2424 1234 435–2213 Total bilirubin, mg/dL 6.0 3.4–9.0 5.8 3.1–8.9 6.4 3.9–9.2 Abbreviations: ACIP, Advisory Committee on Immunization Practices; ALT, alanine aminotransferase; AST, aspartate aminotransferase; IQR, interquartile range; HBV, hepatitis B virus; HCV, hepatitis C virus; MSM, men who have sex with men. Data on homelessness was not available for 45 (7.6%) patients. Percentage of males. 16 • cid 2020:71 (1 July) • Peak et al Downloaded from https://academic.oup.com/cid/article/71/1/14/5550168 by DeepDyve user on 13 July 2022 Risk Factor Analysis: Hepatitis A Disease Severity homelessness and illicit drug use, 91 (17%) reported homeless- Among the 589 confirmed and probable cases, 404 (68%) pa- ness only, and 77 (14%) reported illicit drug use only. tients were hospitalized and 20 (3%) died. The OR for hospital- Among the 291 patients who reported experiencing home- ization was 3.1 (95% CI, 2.1–4.5) comparing patients reporting lessness, 79 (27%) did not report any other ACIP indications homelessness with those not reporting homelessness (Table 4). for vaccination (Table 2). Of the 212 (73%) PEH with at least 1 The adjusted OR for hospitalization was 2.5 (95% CI, 1.7–3.9) known indication, 200 (94%) reported illicit drug use, 72 (34%) after adjustment for illicit drug use and age. Hospitalization and were coinfected with HBV or HCV, 6 (2.8%) were MSM, and 4 death were more common as patient age increased (Figure 1). (1.9%) reported recent international travel to Mexico, which is The OR for death associated with hepatitis A  was not statis- a country with intermediate or high rates of HAV. tically significantly elevated at 2.5 (95% CI, .9–7.8), but after adjusting for age and coinfection with HBV or HCV, the odds Risk Factor Analysis: Hepatitis A Virus Infection of death were 3.9 (95% CI, 1.1–16.9) times higher for patients In total, 502 RT-PCR–confirmed case-patients and 96 control reporting homelessness than for those not reporting homeless- subjects with negative RT-PCR results were included for test- ness (Table 5). negative case-control analysis. Homelessness was reported by 251 (50%) case-patients and 23 (24%) control subjects; the DISCUSSION crude OR for infection was 2.4 (95% confidence interval [CI], 1.4–4.1) (Table 3). This association increased to 3.3 (95% CI, During a hepatitis A outbreak in San Diego County with ap- 1.5–7.9) after adjustment for age, sex, and international travel proximately 600 reported cases, we identified homelessness in the multiple logistic regression model. as an independent risk factor for HAV transmission and Table 3. Crude and Adjusted Logistic Regression Results from Risk Factor Analysis for Hepatitis A Virus Infection Confirmed Case-patients (N = 502) Control Subjects (N = 96) Adjusted Odds No. % No. % Odds Ratio (95% CI) Ratio (95% CI) Homelessness b b Yes 251 50.0 23 24.0 2.40 (1.43–4.14) 3.28 (1.52–7.90) No 218 43.4 48 50.0 Ref Ref Missing 33 6.6 25 26.0 … … Age, years b b Median 43 49 0.97 (.95–.98) per year 0.97 (.95–.99) per year Sex b b Male 334 66.5 46 47.9 2.17 (2.46–3.39) 2.31 (1.20–4.53) Female 167 32.3 50 52.1 Ref Ref Other 1 0.2 0 0.0 … … International travel b b Yes 36 7.2 9 9.4 0.23 (.10–0.57) 0.29 (.12–.75) No 360 71.7 36 37.5 Ref Ref Missing 106 21.1 51 53.1 … … Illicit drug use Yes 232 46.2 24 25.0 2.58 (1.59–4.30) … No 197 39.2 35 36.5 Ref … Missing 73 14.5 37 38.5 … … MSM Yes 11 2.2 1 1.0 2.46 (.47–45.5) … No 259 51.6 58 60.4 Ref … Missing 232 46.2 37 38.5 … … HBV or HCV coinfection Yes 81 16.1 11 11.5 1.08 (.68–1.82) … No 350 69.7 53 55.2 Ref … Missing 71 14.1 32 33.3 … … Abbreviations: CI, confidence interval; HBV, hepatitis B virus; HCV, hepatitis C virus; MSM, men who have sex with men; Ref, reference. Multivariable model including homelessness, age, sex, and history of international travel. Association significant at P < .05. Homelessness and Hepatitis A • cid 2020:71 (1 July) • 17 Downloaded from https://academic.oup.com/cid/article/71/1/14/5550168 by DeepDyve user on 13 July 2022 Table 4. Crude and Adjusted Logistic Regression Results From Risk Factor Analysis for Hospitalization Associated With Hepatitis A Among Confirmed and Probable Cases Hospitalized (N = 404) Not Hospitalized (N = 185) No. % No. % Odds Ratio (95% CI) Adjusted Odds Ratio (95% CI) Homelessness b b Yes 237 58.7 54 29.2 3.06 (2.09–4.54) 2.53 (1.66–3.88) No 149 36.9 104 25.8 Ref Ref Missing 18 6.7 27 6.7 … … Age, years Median 44 40 1.01 (1.00–1.03) per year 1.02 (1.00–1.03) per year Illicit drug use b b Yes 215 53.2 62 33.5 2.26 (1.58–3.26) 1.66 (1.07–2.57) No 142 35.1 78 42.2 Ref Ref Missing 47 11.6 45 24.3 … … HBV or HCV coinfection Yes 83 20.5 18 9.7 1.70 (1.17–2.55) … No 275 68.1 126 68.1 Ref … Missing 46 11.4 41 22.2 … … Sex Male 277 68.6 123 66.5 1.12 (.77–1.62) … Female 125 30.9 62 33.5 Ref … Other 2 0.5 0 0.0 … … MSM Yes 6 1.5 6 3.2 0.62 (.21–1.92) … No 199 49.3 92 49.7 Ref … Missing 199 49.3 87 47.0 … … Abbreviations: CI, confidence interval; HBV, hepatitis B virus; HCV, hepatitis C virus; MSM, men who have sex with men; Ref, reference. Multivariable model including homelessness, age, and illicit drug use. Association significant at P < .05. severe hepatitis A disease. Homelessness is a recognized risk high burden of homelessness may have contributed to the factor for a range of health conditions and diseases [22] and size and severity of this outbreak. Therefore, COSD targeted has been associated with outbreaks of hepatitis A in the past interventions toward PEH beginning with the recommenda- [23–25], but homelessness was not recognized by the ACIP tion to vaccinate PEH in the first health alert sent by the as an independent risk factor for hepatitis A infection at the county on 10 March 2017 [3]. To reach this population, ap- time of the outbreak [4, 5]. proximately 2500 HAV vaccination events occurred through PEH, especially those who are unsheltered, may be at in- stationary points of dispensary, mobile vans, and vaccina- creased risk of HAV infection because of high population den- tion foot teams consisting of a nurse and law enforcement sity and inadequate facilities for sanitation and hygiene and at officer [31]. Hepatitis A virus vaccinations were also admin- increased risk of severe outcomes because of a high prevalence istered by other community partners at homeless shelters, of associated comorbidities, malnutrition, and alcohol-related jails, emergency departments, and during influenza vacci- liver disease [26]. Studies have reported that homelessness may nation drives. Beyond vaccination, other interventions for be an independent risk factor for HAV antibody positivity [27], this risk group included transitional housing in tent cities, and targeted vaccination of PEH is feasible [28] and helped 24-hour public bathrooms and handwashing stations, en- control previous outbreaks among PEH [25]. Using the frame- hanced street sanitation, targeted health messaging, personal work of a recent consensus report from the National Academy hygiene kits, and temporary convalescent housing after hos- of Sciences [29], further research should assess whether hep- pital discharge [31]. atitis A  is a “housing-sensitive condition” from a public Case-fatality ratios from recent outbreaks, including San health perspective because of risks for PEH acquiring and Diego County, are higher than historical outbreaks and may transmitting HAV. result in part from a shifting case demographic toward older San Diego City and County, with an estimated 9116 people patients [11]. e Th increasing risk of hospitalization and death who were homeless in 2017, ranks fourth highest among US among older patients in this outbreak is consistent with pre- city areas and second only to Los Angeles in the number of vious studies that reported that case fatality increased with age people who are homeless and unsheltered [30]. The relatively from 0.1% among children aged less than 15 years, 0.3% among 18 • cid 2020:71 (1 July) • Peak et al Downloaded from https://academic.oup.com/cid/article/71/1/14/5550168 by DeepDyve user on 13 July 2022 Figure 1. Risk of hospitalization (A, B) and death (C, D) among confirmed and probable cases by homelessness and age quintile (ie, 0 to <33, 33 to <39, 39 to <55, and ≥55 years). people aged 15–39 years, and 2.1% among adults aged 40 years In this investigation, we suspect that the measured associa- or older [5, 32]. tion between homelessness and HAV infection is likely under- e Th median age of 43  years among confirmed and prob- estimated, because associations between homelessness and able cases is similar among patients reporting homelessness other causes of symptoms consistent with viral hepatitis in- (median, 44  years) and not reporting homelessness (median, fection may inflate the prevalence of homelessness among the 42 years) and is consistent with contemporaneous outbreaks in test-negative control subjects. Additionally, PEH may be pref- other states [11]. While the occurrence of hepatitis A  has de- erentially hospitalized for reasons beyond those measured [34, creased nationally in all age groups since 2000, incidence of the 35], but we expect that the outcome of case fatality is robust to disease is lowest among persons aged 0–9 years and 10–19 years this potential bias. compared with older age groups as of 2016 [33]. These findings strongly support the ACIP recommendation Our study limitations include possible misclassification of to add homelessness as an indication for hepatitis A vaccina- sensitive topics including homelessness status and history of il- tion [8], as well as the need to improve adult hepatitis A vac- licit drug use, although we expect such misclassification to be cination rates among groups who are at risk and to address independent of case-control status because of the delayed re- the underlying causes of homelessness [26]. Approximately ceipt of confirmatory RT-PCR test results. Self-reported vacci- half of all patients in this outbreak, and three-quarters of nation history was cross-referenced and supplemented using PEH, had at least 1 previously known ACIP indication for the San Diego Immunization Registry, although vaccinations vaccination (Table 2), yet none received the 2-dose HAV vac- received outside San Diego County are more likely to be missed. cination series before infection. Outbreak response vaccina- e p Th revalence of comorbidities may be underestimated by tion with 1 dose of HAV vaccine was found to be feasible in using coinfection status with HBV or HCV as an incomplete San Diego County and elsewhere [31, 36, 37], and previous surrogate for chronic liver disease caused by risk factors such as studies have shown that the single vaccine can confer protec- chronic alcoholism. tion for 4–11 years [38, 39]. Homelessness and Hepatitis A • cid 2020:71 (1 July) • 19 Downloaded from https://academic.oup.com/cid/article/71/1/14/5550168 by DeepDyve user on 13 July 2022 Table 5. Crude and Adjusted Logistic Regression Results From Risk Factor Analysis for Death Associated With Hepatitis A Among Confirmed and Probable Cases Died (N = 20) Survived (N = 569) No. % No. % Odds Ratio (95% CI) Adjusted Odds Ratio (95% CI) Homelessness Yes 14 70.0 277 48.7 2.51 (.94–7.85) 3.91 (1.14–16.9) No 5 25.0 248 43.4 Ref Ref Missing 1 5.0 44 7.7 … … Age, years b b Median 58 42 1.07 (1.04–1.11) per year 1.11 (1.07–1.17) per year HBV or HCV coinfection Yes 7 35.0 94 16.5 1.99 (.96–3.91) 2.52 (1.11–5.75) No 11 55.0 390 68.7 Ref Ref Missing 2 10.0 85 15.0 … … Illicit drug use Yes 4 20.0 273 48.0 0.34 (.09–1.07) … No 9 45.0 211 37.1 Ref … Missing 7 35.0 85 14.9 … … Sex Male 17 85.0 383 67.3 2.72 (.90–11.8) … Female 3 15.0 184 32.3 Ref … Other 0 0.0 2 0.4 … … Abbreviations: CI, confidence interval; HBV, hepatitis B virus; HCV, hepatitis C virus; Ref, reference. Multivariable model including homelessness, age, and HBV or HCV coinfection. Association significant at P < .05. Notes 7. Centers for Disease Control and Prevention. Outbreak of hepatitis A virus (HAV) infections among persons who use drugs and persons experiencing homelessness. Author contributions. C.  M. P.  and S.  S. S.  analyzed the information. 2018. CDC Health Alert Network. Available at: https://emergency.cdc.gov/han/ Y. L. and S. R. performed molecular testing and analysis. C. M. P., S. S. S., han00412.asp. Accessed 21 August 2019. and E. C. M. wrote the initial draft. All authors contributed to the writing, 8. Doshani M, Weng M, Moore KL, Romero JR, Nelson NP. Recommendations revision, and finalization of the manuscript. of the Advisory Committee on Immunization Practices for use of hepatitis Acknowledgments. e a Th uthors acknowledge helpful feedback from A  vaccine for persons experiencing homelessness. Morb Mortal Wkly Rep. Mark Sawyer on conceptualizing this paper and from Wences Arvelo on 2019; 68:153–6. revising versions of the paper. 9. Nainan OV, Xia G, Vaughan G, Margolis HS. Diagnosis of hepatitis a virus infec- tion: a molecular approach. Clin Microbiol Rev 2006; 19:63–79. Disclaimer. e fin Th dings and conclusions in this report are those of the 10. Association of Public Health Laboratories. Hepatitis A  virus testing and re- authors and do not necessarily represent the official position of the Centers sources. 2018;1–3. Available at: https://www.aphl.org/programs/infectious_di- for Disease Control and Prevention. sease/Documents/2018_HAV_DiagnosticUpdate.pdf. Accessed 21 August 2019. Potential coni fl cts of interest. e a Th uthors report no potential conflicts 11. Foster  M, Ramachandran  S, Myatt  K, et  al. Hepatitis A  virus outbreaks associ- of interest. All authors have submitted the ICMJE Form for Disclosure of ated with drug use and homelessness—California, Kentucky, Michigan, and Utah, Potential Conflicts of Interest. Conflicts that the editors consider relevant to 2017. Morb Mortal Wkly Rep 2018; 67:2017–9. the content of the manuscript have been disclosed. 12. Council of State and Territorial Epidemiologists. Public health reporting and national notification for hepatitis A. 2011. Available at: www.cste.org/resource/ resmgr/PS/11-ID-02.pdf. Accessed 21 August 2019. References 13. Yung CF, Chan SP, Thein TL, Chai SC, Leo YS. Epidemiological risk factors for 1. Centers for Disease Control and Prevention. Hepatitis A. In: Hamborsky J, Kroger adult dengue in Singapore: an 8-year nested test negative case control study. BMC A, Wolfe S, eds. Epidemiology and prevention of vaccine-preventable diseases. Infect Dis 2016; 16:323. 13th ed. Washington, DC: Public Health Foundation, 2015. 14. Fukushima W, Hirota Y. Basic principles of test-negative design in evaluating in- 2. County of San Diego Health and Human Services Agency. San Diego County fluenza vaccine effectiveness. Vaccine 2017; 35:4796–800. Annual Communicable Disease Report. 2016. 15. Sullivan  SG, Tchetgen  Tchetgen  EJ, Cowling  BJ. Theoretical basis of the test- 3. County of San Diego Health and Human Services Agency. Hepatitis A  virus negative study design for assessment of influenza vaccine effectiveness. Am J outbreak associated with homelessness, drug use in San Diego County. Epidemiol 2016; 184:345–53. 2017; Available at: https://www.sandiegocounty.gov/content/dam/sdc/hhsa/ 16. Belongia EA, Simpson MD, King JP, et al. Variable influenza vaccine effectiveness programs/phs/cahan/communications_documents/03-10-17.pdf. Accessed 21 by subtype: a systematic review and meta-analysis of test-negative design studies. August 2019. Lancet Infect Dis 2016; 16:942–51. 4. Centers for Disease Control and Prevention. Prevention of hepatitis A  through 17. Bar-Zeev  N, Kapanda  L, Tate  JE, et  al. Effectiveness of a monovalent rotavirus active or passive immunization: recommendations of the Advisory Committee on vaccine in infants in Malawi after programmatic roll-out: an observational and Immunization Practices (ACIP). Morb Mortal Wkly Rep 2006; 55:1–23. case-control study. Lancet Infect Dis 2015 15(4):422–8. 5. World Health Organization. WHO position paper on hepatitis A vaccines—June 18. Azman AS, Parker LA, Rumunu J, et al. Effectiveness of one dose of oral cholera 2012. Wkly Epidemiol Rec 2012; 87:261–76. Available at: https://www.who.int/ vaccine in response to an outbreak: a case-cohort study. Lancet Glob Health 2016; wer/2012/wer8728_29/en/. Accessed 21 August 2019. 4:e856–63. 6. Centers for Disease Control and Prevention. Advisory Committee on 19. Franke MF, Jerome JG, Matias WR, et al. Comparison of two control groups for Immunization Practices (ACIP) summary report. 2017. Available at: https:// estimation of oral cholera vaccine effectiveness using a case-control study design. stacks.cdc.gov/view/cdc/58894. Accessed 21 August 2019. Vaccine 2017; 35:5819–27. 20 • cid 2020:71 (1 July) • Peak et al Downloaded from https://academic.oup.com/cid/article/71/1/14/5550168 by DeepDyve user on 13 July 2022 20. Broome CV, Facklam RR, Fraser DW. Pneumococcal disease after pneumococcal catalog/25133/permanent-supportive-housing-evaluating-the-evidence-for- vaccination: an alternative method to estimate the efficacy of pneumococcal vac- improving-health-outcomes. Accessed 21 August 2019. cine. N Engl J Med 1980; 303:549–52. 30. Regional Task Force on the Homeless. WeALLCount annual comprehensive 21. Glickson  M, Galun  E, Oren  R, Tur-Kaspa  R, Shouval  D. Relapsing Hepatitis A: report. San Diego, 2017. Available at: http://www.rtfhsd.org/wp-content/up- review of 14 cases and literature survey. Medicine 1992; 71: 14–23. loads/2017/07/comp-report-final.pdf. Accessed 21 August 2019. 22. Aldridge  RW, Story  A, Hwang  SW, et  al. Morbidity and mortality in homeless 31. County of San Diego. Hepatitis A  outbreak after action report. 2018. Available individuals, prisoners, sex workers, and individuals with substance use disorders at: https://www.sandiegocounty.gov/content/dam/sdc/cosd/SanDiegoHepatitis in high-income countries: a systematic review and meta-analysis. Lancet 2018; AOutbreak-2017-18-AfterActionReport.pdf. Accessed 21 August 2019. 391:241–50. 32. Hollinger F, Ticehurst J. Hepatitis A. In: Fields virology. Philadelphia: Lippincott- 23. Syed NA, Hearing SD, Shaw IS, et al. Outbreak of hepatitis A in the injecting drug Raven, 1996:735–82. user and homeless populations in Bristol: control by a targeted vaccination pro- 33. Centers for Disease Control and Prevention. Viral hepatitis surveillance— gramme and possible parenteral transmission. Eur J Gastroenterol Hepatol 2003; United States, 2016. Available at: https://www.cdc.gov/hepatitis/statistics/ 15:901–6. 2016surveillance/pdfs/2016HepSurveillanceRpt.pdf. Accessed 21 August 2019. 24. Tjon GMS, Götz H, Koek AG, et al. An outbreak of hepatitis A among homeless 34. Salit SA, Kuhn EM, Hartz AJ, Vu JM, Mosso AL. Hospitalization costs associated drug users in Rotterdam, The Netherlands. J Med Virol 2005; 77:360–6. with homelessness in New York City. N Engl J Med 1998; 338:1734–40. 25. James TL, Aschkenasy M, Eliseo LJ, Olshaker J, Mehta SD. Response to hepatitis 35. Feigal J, Park B, Bramante C, Nordgaard C, Menk J, Song J. Homelessness and dis- A  epidemic: emergency department collaboration with public health commis- charge delays from an urban safety net hospital. Public Health 2014; 128:1033–5. sion. J Emerg Med 2009; 36:412–6. 36. McMahon BJ, Beller M, Williams J, Schloss M, Tanttila H, Bulkow L. A program 26. Kushel M. Hepatitis A outbreak in California—addressing the root cause. N Engl to control an outbreak of hepatitis A in Alaska by using an inactivated hepatitis J Med 2018; 378:211–3. A vaccine. Arch Pediatr Adolesc Med 1996; 150:733–9. 27. Hennessey  KA, Bangsberg  DR, Weinbaum  C, Hahn  JA. Hepatitis A  seropreva- 37. Zamir C, Rishpon S, Zamir D, Leventhal A, Rimon N, Ben-Porath E. Control of lence and risk factors among homeless adults in San Francisco: should homeless- a community-wide outbreak of hepatitis A by mass vaccination with inactivated ness be included in the risk-based strategy for vaccination? Public Health Rep hepatitis A vaccine. Eur J Clin Microbiol Infect Dis 2001; 20:185–7. 2009; 124:813–7. 38. Hatz  C, van  der  Ploeg  R, Beck  BR, Frösner  G, Hunt  M, Herzog  C. Successful 28. Poulos  RG, Ferson  MJ, Orr  KJ, et  al. Vaccination against hepatitis A  and B in memory response following a booster dose with a virosome-formulated hepatitis persons subject to homelessness in inner Sydney: vaccine acceptance, completion A vaccine delayed up to 11 years. Clin Vaccine Immunol 2011; 18:885–7. rates and immunogenicity. Aust N Z J Public Health 2010; 34:130–5. 39. Iwarson  S, Lindh  M, Widerström  L. Excellent booster response 4-6 y after a 29. National Academy of Sciences. Permanent supportive housing. Washington, single primary dose of an inactivated hepatitis A vaccine. Scand J Infect Dis 2002; DC: National Academies Press, 2018. Available at: https://www.nap.edu/ 34:110–1. Homelessness and Hepatitis A • cid 2020:71 (1 July) • 21 Please excuse the presence of this and the following test pages, which have been added to a small number of article PDFs for a limited time as part of our process of continual development and improvement. academic.oup.com/cid 1 of 4 academic.oup.com/cid Lorem ipsum dolor sit amet, consectetur adipiscing elit, sed do eiusmod tempor incididunt ut labore et dolore magna aliqua. Ut enim ad minim veniam, quis nostrud exercitation ullamco laboris nisi ut aliquip ex ea commodo consequat. Duis aute irure dolor in reprehenderit in voluptate velit esse cillum dolore eu fugiat nulla pariatur. Excepteur sint occaecat cupidatat non proident, sunt in culpa qui officia deserunt mollit anim id est laborum. Lorem ipsum dolor sit amet, consectetur adipiscing elit, sed do eiusmod tempor incididunt ut labore et dolore magna aliqua. Ut enim ad minim veniam, quis nostrud exercitation ullamco laboris nisi ut aliquip ex ea commodo consequat. Duis aute irure dolor in reprehenderit in voluptate velit esse cillum dolore eu fugiat nulla pariatur. Excepteur sint occaecat cupidatat non proident, sunt in culpa qui officia deserunt mollit anim id est laborum. Lorem ipsum dolor sit amet, consectetur adipiscing elit, sed do eiusmod tempor incididunt ut labore et dolore magna aliqua. Ut enim ad minim veniam, quis nostrud exercitation ullamco laboris nisi ut aliquip ex ea commodo consequat. Duis aute irure dolor in reprehenderit in voluptate velit esse cillum dolore eu fugiat nulla pariatur. Excepteur sint occaecat cupidatat non proident, sunt in culpa qui officia deserunt mollit anim id est laborum. Lorem ipsum dolor sit amet, consectetur adipiscing elit, sed do eiusmod tempor incididunt ut labore et dolore magna aliqua. Ut enim ad minim veniam, quis nostrud exercitation ullamco laboris nisi ut aliquip ex ea commodo consequat. Duis aute irure dolor in reprehenderit in voluptate velit esse cillum dolore eu fugiat nulla pariatur. Excepteur sint occaecat cupidatat non proident, sunt in culpa qui officia deserunt mollit anim id est laborum. Lorem ipsum dolor sit amet, consectetur adipiscing elit, sed do eiusmod tempor incididunt ut labore et dolore magna aliqua. Ut enim ad minim veniam, quis nostrud exercitation ullamco laboris nisi ut aliquip ex ea commodo consequat. Duis aute irure dolor in reprehenderit in voluptate velit esse cillum dolore eu fugiat nulla pariatur. Excepteur sint occaecat cupidatat non proident, sunt in culpa qui officia deserunt mollit anim id est laborum. Lorem ipsum dolor sit amet, consectetur adipiscing elit, sed do eiusmod tempor incididunt ut labore et dolore magna aliqua. Ut enim ad minim veniam, quis nostrud exercitation ullamco laboris nisi ut aliquip ex ea commodo consequat. Duis aute irure dolor in reprehenderit in voluptate velit esse cillum dolore eu fugiat nulla pariatur. Excepteur sint occaecat cupidatat non proident, sunt in culpa qui officia deserunt mollit anim id est laborum. Lorem ipsum dolor sit amet, consectetur adipiscing elit, sed do academic.oup.com/cid 2 of 4 eiusmod tempor incididunt ut labore et dolore magna aliqua. Ut enim ad minim veniam, quis nostrud exercitation ullamco laboris nisi ut aliquip ex ea commodo consequat. Duis aute irure dolor in reprehenderit in voluptate velit esse cillum dolore eu fugiat nulla pariatur. Excepteur sint occaecat cupidatat non proident, sunt in culpa qui officia deserunt mollit anim id est laborum. Lorem ipsum dolor sit amet, consectetur adipiscing elit, sed do eiusmod tempor incididunt ut labore et dolore magna aliqua. Ut enim ad minim veniam, quis nostrud exercitation ullamco laboris nisi ut aliquip ex ea commodo consequat. Duis aute irure dolor in reprehenderit in voluptate velit esse cillum dolore eu fugiat nulla pariatur. Excepteur sint occaecat cupidatat non proident, sunt in culpa qui officia deserunt mollit anim id est laborum. Lorem ipsum dolor sit amet, consectetur adipiscing elit, sed do eiusmod tempor incididunt ut labore et dolore magna aliqua. Ut enim ad minim veniam, quis nostrud exercitation ullamco laboris nisi ut aliquip ex ea commodo consequat. Duis aute irure dolor in reprehenderit in voluptate velit esse cillum dolore eu fugiat nulla pariatur. Excepteur sint occaecat cupidatat non proident, sunt in culpa qui officia deserunt mollit anim id est laborum. Lorem ipsum dolor sit amet, consectetur adipiscing elit, sed do eiusmod tempor incididunt ut labore et dolore magna aliqua. Ut enim ad minim veniam, quis nostrud exercitation ullamco laboris nisi ut aliquip ex ea commodo consequat. Duis aute irure dolor in reprehenderit in voluptate velit esse cillum dolore eu fugiat nulla pariatur. Excepteur sint occaecat cupidatat non proident, sunt in culpa qui officia deserunt mollit anim id est laborum. Lorem ipsum dolor sit amet, consectetur adipiscing elit, sed do eiusmod tempor incididunt ut labore et dolore magna aliqua. Ut enim ad minim veniam, quis nostrud exercitation ullamco laboris nisi ut aliquip ex ea commodo consequat. Duis aute irure dolor in reprehenderit in voluptate velit esse cillum dolore eu fugiat nulla pariatur. Excepteur sint occaecat cupidatat non proident, sunt in culpa qui officia deserunt mollit anim id est laborum. Lorem ipsum dolor sit amet, consectetur adipiscing elit, sed do eiusmod tempor incididunt ut labore et dolore magna aliqua. Ut enim ad minim veniam, quis nostrud exercitation ullamco laboris nisi ut aliquip ex ea commodo consequat. Duis aute irure dolor in reprehenderit in voluptate velit esse cillum dolore eu fugiat nulla pariatur. Excepteur sint occaecat cupidatat non proident, sunt in culpa qui officia deserunt mollit anim id est laborum. Lorem ipsum dolor sit amet, consectetur adipiscing elit, sed do eiusmod tempor incididunt ut labore et dolore magna aliqua. academic.oup.com/cid 3 of 4 Ut enim ad minim veniam, quis nostrud exercitation ullamco laboris nisi ut aliquip ex ea commodo consequat. Duis aute irure dolor in reprehenderit in voluptate velit esse cillum dolore eu fugiat nulla pariatur. Excepteur sint occaecat cupidatat non proident, sunt in culpa qui officia deserunt mollit anim id est laborum. Lorem ipsum dolor sit amet, consectetur adipiscing elit, sed do eiusmod tempor incididunt ut labore et dolore magna aliqua. Ut enim ad minim veniam, quis nostrud exercitation ullamco laboris nisi ut aliquip ex ea commodo consequat. Duis aute irure dolor in reprehenderit in voluptate velit esse cillum dolore eu fugiat nulla pariatur. Excepteur sint occaecat cupidatat non proident, sunt in culpa qui officia deserunt mollit anim id est laborum. Lorem ipsum dolor sit amet, consectetur adipiscing elit, sed do eiusmod tempor incididunt ut labore et dolore magna aliqua. Ut enim ad minim veniam, quis nostrud exercitation ullamco laboris nisi ut aliquip ex ea commodo consequat. Duis aute irure dolor in reprehenderit in voluptate velit esse cillum dolore eu fugiat nulla pariatur. Excepteur sint occaecat cupidatat non proident, sunt in culpa qui officia deserunt mollit anim id est laborum. Lorem ipsum dolor sit amet, consectetur adipiscing elit, sed do eiusmod tempor incididunt ut labore et dolore magna aliqua. Ut enim ad minim veniam, quis nostrud exercitation ullamco laboris nisi ut aliquip ex ea commodo consequat. Duis aute irure dolor in reprehenderit in voluptate velit esse cillum dolore eu fugiat nulla pariatur. Excepteur sint occaecat cupidatat non proident, sunt in culpa qui officia deserunt mollit anim id est laborum. Lorem ipsum dolor sit amet, consectetur adipiscing elit, sed do eiusmod tempor incididunt ut labore et dolore magna aliqua. Ut enim ad minim veniam, quis nostrud exercitation ullamco laboris nisi ut aliquip ex ea commodo consequat. Duis aute irure dolor in reprehenderit in voluptate velit esse cillum dolore eu fugiat nulla pariatur. Excepteur sint occaecat cupidatat non proident, sunt in culpa qui officia deserunt mollit anim id est laborum. Lorem ipsum dolor sit amet, consectetur adipiscing elit, sed do eiusmod tempor incididunt ut labore et dolore magna aliqua. Ut enim ad minim veniam, quis nostrud exercitation ullamco laboris nisi ut aliquip ex ea commodo consequat. Duis aute irure dolor in reprehenderit in voluptate velit esse cillum dolore eu fugiat nulla pariatur. Excepteur sint occaecat cupidatat non proident, sunt in culpa qui officia deserunt mollit anim id est laborum. academic.oup.com/cid 4 of 4

Journal

Clinical Infectious DiseasesOxford University Press

Published: Jun 24, 2020

Keywords: hepatitis a; infections; homelessness; hepatitis a vaccines; disease outbreaks; hepatitis a virus

There are no references for this article.