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<article xmlns:mml="http://www.w3.org/1998/Math/MathML" xmlns:xlink="http://www.w3.org/1999/xlink" dtd-version="1.3" xml:lang="en" article-type="research-article"><?properties manuscript?><processing-meta base-tagset="archiving" mathml-version="3.0" table-model="xhtml" tagset-family="jats"><restricted-by>pmc</restricted-by></processing-meta><front><journal-meta><journal-id journal-id-type="nlm-journal-id">8406899</journal-id><journal-id journal-id-type="pubmed-jr-id">7945</journal-id><journal-id journal-id-type="nlm-ta">Vaccine</journal-id><journal-id journal-id-type="iso-abbrev">Vaccine</journal-id><journal-title-group><journal-title>Vaccine</journal-title></journal-title-group><issn pub-type="ppub">0264-410X</issn><issn pub-type="epub">1873-2518</issn></journal-meta><article-meta><article-id pub-id-type="pmid">28668569</article-id><article-id pub-id-type="pmc">8995106</article-id><article-id pub-id-type="doi">10.1016/j.vaccine.2017.06.054</article-id><article-id pub-id-type="manuscript">HHSPA1793515</article-id><article-categories><subj-group subj-group-type="heading"><subject>Article</subject></subj-group></article-categories><title-group><article-title>Increasing seasonal influenza vaccination among high risk groups in China: Do community healthcare workers have a role to play?</article-title></title-group><contrib-group><contrib contrib-type="author"><name><surname>Song</surname><given-names>Ying</given-names></name><xref rid="A1" ref-type="aff">a</xref><xref rid="CR1" ref-type="corresp">*</xref><xref rid="FN1" ref-type="author-notes">1</xref></contrib><contrib contrib-type="author"><name><surname>Zhang</surname><given-names>Tao</given-names></name><xref rid="A2" ref-type="aff">b</xref></contrib><contrib contrib-type="author"><name><surname>Chen</surname><given-names>Liling</given-names></name><xref rid="A3" ref-type="aff">c</xref></contrib><contrib contrib-type="author"><name><surname>Yi</surname><given-names>Bo</given-names></name><xref rid="A4" ref-type="aff">d</xref></contrib><contrib contrib-type="author"><name><surname>Hao</surname><given-names>Xiaoning</given-names></name><xref rid="A5" ref-type="aff">e</xref></contrib><contrib contrib-type="author"><name><surname>Zhou</surname><given-names>Suizan</given-names></name><xref rid="A1" ref-type="aff">a</xref></contrib><contrib contrib-type="author"><name><surname>Zhang</surname><given-names>Ran</given-names></name><xref rid="A1" ref-type="aff">a</xref></contrib><contrib contrib-type="author"><name><surname>Greene</surname><given-names>Carolyn</given-names></name><xref rid="A1" ref-type="aff">a</xref><xref rid="FN1" ref-type="author-notes">1</xref></contrib></contrib-group><aff id="A1"><label>a</label>Centers for Disease Control and Prevention, Atlanta, GA, USA</aff><aff id="A2"><label>b</label>School of Public Health, Fudan University, Shanghai, China</aff><aff id="A3"><label>c</label>Suzhou Center for Disease Prevention and Control, Suzhou, Jiangsu Province, China</aff><aff id="A4"><label>d</label>Ningbo Center for Disease Prevention and Control, Ningbo, Zhejiang Province, China</aff><aff id="A5"><label>e</label>Health Development Research Center of the National Health and Family Planning Commission, Beijing, China</aff><author-notes><fn fn-type="equal" id="FN1"><label>1</label><p id="P1"> These authors contributed equally to this work.</p></fn><fn fn-type="con" id="FN2"><p id="P2">Authors&#x02019; contribution</p><p id="P3">Ying SONG, Suizan ZHOU, Tao ZHANG, Liling CHEN, Bo Yi, and Xiaoning HAO conceived of and designed the studies; Tao ZHANG, Liling CHEN, Bo Yi, and Xiaoning HAO coordinated the studies, assisted in data collection, and analyzed the data; Ying SONG and Carolyn Greene wrote the draft of the manuscript; Suizhan ZHOU and Ran Zhan helped revise drafts of the manuscript. All authors have seen and approved the final manuscript, and have contributed significantly to the work.</p></fn><corresp id="CR1"><label>*</label>Corresponding author at: United States Centers for Disease Control and Prevention Influenza Program China, Suite 601, Dongwai Diplomatic Office, 23 Dongzhimenwai Dajie, Beijing 100600, China. <email>kei2@cdc.gov</email>, <email>songying@cn.cdc.gov</email> (Y. Song).</corresp></author-notes><pub-date pub-type="nihms-submitted"><day>1</day><month>4</month><year>2022</year></pub-date><pub-date pub-type="ppub"><day>24</day><month>7</month><year>2017</year></pub-date><pub-date pub-type="epub"><day>28</day><month>6</month><year>2017</year></pub-date><pub-date pub-type="pmc-release"><day>10</day><month>4</month><year>2022</year></pub-date><volume>35</volume><issue>33</issue><fpage>4060</fpage><lpage>4063</lpage><abstract id="ABS1"><sec id="S1"><title>Background:</title><p id="P4">Seasonal influenza vaccine uptake in China is low. This study aims to assess the role of community healthcare workers (HCWs) in increasing vaccination among high risk groups in China.</p></sec><sec id="S2"><title>Methods:</title><p id="P5">We analyzed data from four knowledge, attitude and practice (KAP) studies on seasonal influenza vaccination in China targeting guardians of young children, pregnant women, adults aged &#x02265;60 years, and HCWs from 2012 to 2014.</p></sec><sec id="S3"><title>Results:</title><p id="P6">Thirty-one percent of pregnant women and 78% adults aged &#x02265;60 years reported willingness to follow HCWs&#x02019; recommendations for influenza vaccination. Guardians were more likely to vaccinate their children if they received HCWs&#x02019; recommendations (35% vs. 17%, p &#x0003c; 0.001). Community HCWs were more likely to recommend seasonal influenza vaccination than hospital HCWs (58% vs. 28%, p &#x0003c; 0.001).</p></sec><sec id="S4"><title>Conclusion:</title><p id="P7">Study results suggest the value of incorporating community HCWs&#x02019; recommendation for seasonal influenza vaccination into existing primary public health programs to increase vaccination coverage among high risk groups in China.</p></sec></abstract><kwd-group><kwd>Seasonal influenza vaccine</kwd><kwd>Vaccination</kwd><kwd>Healthcare worker</kwd><kwd>Community</kwd><kwd>KAP</kwd></kwd-group></article-meta></front><body><sec id="S5"><label>1.</label><title>Introduction</title><p id="P8">The World Health Organization and the Chinese Center for Disease Prevention and Control recommend seasonal influenza vaccine for groups at high risk for severe illness and complications from influenza infection, including pregnant women, young children, older adults and adults with chronic diseases [<xref rid="R1" ref-type="bibr">1</xref>,<xref rid="R2" ref-type="bibr">2</xref>]. In China, vaccine uptake within these groups remains low [<xref rid="R3" ref-type="bibr">3</xref>&#x02013;<xref rid="R5" ref-type="bibr">5</xref>]. Numerous factors contribute to low coverage. First, the seasonal influenza vaccine is not included in the national Expanded Program on Immunization (EPI) [<xref rid="R6" ref-type="bibr">6</xref>], but is available upon request, most often at cost (10&#x02013;15 USD). Second, misconceptions about influenza risk and vaccine safety and efficacy are common [<xref rid="R7" ref-type="bibr">7</xref>&#x02013;<xref rid="R9" ref-type="bibr">9</xref>]. While inadequate supply may contribute to low vaccine uptake in other countries, in China, from 2004 to 2009, an average of 25% of influenza vaccine was returned to manufacturers unused [<xref rid="R10" ref-type="bibr">10</xref>].</p><p id="P9">While studies in developed countries have shown that HCWs&#x02019; recommendations promote seasonal influenza vaccination [<xref rid="R11" ref-type="bibr">11</xref>&#x02013;<xref rid="R13" ref-type="bibr">13</xref>], few studies have addressed the HCW&#x02019;s role with respect to vaccination in China [<xref rid="R14" ref-type="bibr">14</xref>]. HCWs&#x02019; willingness to recommend vaccination in China may be influenced by reports of patient mistrust, and patient-on-doctor violence [<xref rid="R15" ref-type="bibr">15</xref>,<xref rid="R16" ref-type="bibr">16</xref>]. Within this context, our study assessed whether community HCWs, who provide primary public health services [<xref rid="R17" ref-type="bibr">17</xref>], have a role in increasing influenza vaccine coverage among high risk groups in China.</p></sec><sec id="S6"><label>2.</label><title>Methods</title><p id="P10">From 2012 to 2014, the United States (US) Centers for Disease Control and Prevention supported four knowledge, attitude and practice (KAP) studies on influenza infection and vaccination in China. We analyzed vaccination coverage, factors influencing influenza vaccination, preferred sources for information, whether HCWs recommended vaccination, and willingness to follow HCWs&#x02019; recommendations.</p><p id="P11">From October 2012 to January 2013, we conducted two cross-sectional surveys in Suzhou among guardians of children aged 6 months to 3 years at three vaccination clinics, and pregnant women at four prenatal clinics. Trained staff conducted face-to-face interviews using structured questionnaires.</p><p id="P12">In December 2014, we conducted a cross-sectional survey among adults aged &#x02265;60 years at three senior centers in Ningbo. Participants completed self-administered questionnaires, with support from trained study staff.</p><p id="P13">In November 2013 and May 2014, we conducted two cross-sectional surveys among HCWs in Qingdao, recruiting all HCWs providing direct patient care on investigation days at 10 healthcare institutions. We defined two groups: community HCWs were those who worked at community health centers providing primary health services. Hospital HCWs were those who worked at secondary and tertiary hospitals and focused on curative medicine. Enrolled HCWs completed self-administered questionnaires.</p></sec><sec id="S7"><label>3.</label><title>Ethics statement</title><p id="P14">Fudan University, Suzhou CDC, Ningbo CDC and the Health Development Research Center received local IRB approval for their site&#x02019;s survey. All survey participants provided verbal consent.</p></sec><sec id="S8"><label>4.</label><title>Results</title><sec id="S9"><label>4.1.</label><title>KAP among guardians of children aged 6 months to 3 years</title><p id="P15">Among responding guardians, 86/323 (27%) reported receiving a HCW&#x02019;s recommendation for influenza vaccination and 70/317 (22%) reported that their child was vaccinated in the prior year. Guardians who reported receiving a HCW recommendation were more likely to vaccinate their child than those who did not (35% vs. 17%, p &#x0003c; 0.001). The main reported reasons for not vaccinating their child were concerns for vaccine safety (62%), not receiving a HCW&#x02019;s recommendation (37%); believing vaccination was unnecessary (25%), and limited vaccine effectiveness (23%). Reported preferences for information about vaccines included television (64%), internet (57%) and educational leaflets (51%).</p></sec><sec id="S10"><label>4.2.</label><title>KAP among pregnant women</title><p id="P16">Among 1673 pregnant women interviewed, 4% reported receiving a HCW recommendation for influenza vaccination in the prior year. None reported receiving the vaccine during pregnancy, and none planned to get vaccinated in the current year. The most common reasons reported for not getting vaccinated included fear of harm to the fetus (83%), vaccine safety for the pregnant woman herself (28%), and believing vaccination was unnecessary (22%). Preferred sources for vaccine information included television (56%), internet (39%), and doctors (34%). Nearly one third (31%) stated they would get vaccinated if they received a HCW&#x02019;s recommendation.</p></sec><sec id="S11"><label>4.3.</label><title>KAP among adults aged &#x0003e;60 years</title><p id="P17">Among 379 adults aged &#x02265;60 years interviewed, 0.8% reported receiving the influenza vaccine in the prior year. The most common reasons for not getting vaccinated among those who responded (n = 268) were vaccination was unnecessary (33%), medical insurance did not pay for influenza vaccination (24%), and HCWs had not recommended vaccination (23%). Among all interviewed, 78% (296/379) reported willingness to get vaccinated if they received a HCW&#x02019;s recommendation. Most (280/379, 74%) reported a preference for receiving health information from HCWs.</p></sec><sec id="S12"><label>4.4.</label><title>KAP among HCWs</title><p id="P18">Among 1852 HCWs approached, 1301 (70%) completed both surveys; among these, 17% were community HCWs.</p><p id="P19">Post-influenza season, 5% HCWs reported receiving influenza vaccination during the prior season. Main reasons for not getting vaccinated included concerns about vaccine safety (43%), perceiving vaccination as unnecessary (27%), having insufficient time for vaccination (24%), and believing the vaccine was ineffective (20%).</p><p id="P20">HCWs wanted to learn more about influenza disease severity (68%), populations most susceptible to influenza illness (52%), vaccine contraindications (72%), safety (72%) and effectiveness (71%). Preferred sources of information on vaccines included internet (76%), television/radio (75%), newspapers/books (55%), and colleagues (50%).</p><p id="P21">Among all 1301 HCWs, 8% reported always recommending influenza vaccination to patients during the prior influenza season. Community HCWs were more likely to be vaccinated than hospital HCWs (P &#x0003c; 0.01) (<xref rid="F1" ref-type="fig">Fig. 1</xref>), and were also more likely to recommend vaccination to patients at least once in the prior season (58% vs. 28%, P &#x0003c; 0.001).</p><p id="P22">Seasonal influenza vaccination coverage and factors influencing vaccination among high risk groups and healthcare workers are summarized in <xref rid="T1" ref-type="table">Table 1</xref>.</p></sec></sec><sec id="S13"><label>5.</label><title>Discussion</title><sec id="S14"><label>5.1.</label><title>High risk groups in China cited similar reasons for not getting vaccinated for seasonal influenza, and all had suboptimal influenza vaccination coverage</title><p id="P23">A common barrier to vaccination was concern about vaccine safety. Another common barrier was perceiving vaccination as unnecessary (22&#x02013;33%); 23% guardians also cited low vaccine effectiveness as a barrier. These findings, in addition to the low seasonal influenza vaccine coverage among children less than 3 years of age and adults aged &#x02265;60 years, are consistent with prior studies conducted in China [<xref rid="R4" ref-type="bibr">4</xref>,<xref rid="R5" ref-type="bibr">5</xref>,<xref rid="R7" ref-type="bibr">7</xref>&#x02013;<xref rid="R9" ref-type="bibr">9</xref>]. We also found minimal coverage among HCWs (5%) and none among pregnant women.</p></sec><sec id="S15"><label>5.2.</label><title>High risk groups reported willingness to follow HCWs' advice for vaccination, and HCWs' recommendations were associated with increased coverage</title><p id="P24">More than a third of pregnant women and three quarters of adults aged &#x02265;60 years reported wanting to receive information from HCWs regarding vaccination. Further, 31% pregnant women and 78% adults aged &#x02265;60 years stated they would get vaccinated if a HCW recommended vaccination. Similarly, 37% guardians listed not receiving a HCW&#x02019;s recommendation as a main barrier to vaccination, and guardians who received a HCW recommendation were more likely to vaccinate their child. These findings are consistent with studies in the US and China [<xref rid="R11" ref-type="bibr">11</xref>&#x02013;<xref rid="R14" ref-type="bibr">14</xref>,<xref rid="R18" ref-type="bibr">18</xref>], in which high risk groups expressed trust in their physician, whose recommendation was a strong determinant of influenza immunization uptake.</p></sec><sec id="S16"><label>5.3.</label><title>Community HCWs may offer a practical way to increase seasonal influenza vaccine uptake among high risk groups in China</title><p id="P25">Only 8% HCWs in Qingdao reported always recommending influenza vaccination, and only 4% pregnant women and 27% guardians of young children reported receiving a HCW&#x02019;s recommendation for influenza vaccination in the prior year.</p><p id="P26">Several factors may prevent HCWs in China from routinely recommending influenza vaccination. First, in our study, HCWs themselves were not vaccinated due to concerns about vaccine safety, effectiveness, and perceiving vaccination as unnecessary. HCWs may also avoid recommending optional vaccines not included in EPI, such as influenza vaccine, to decrease risk of being held liable for adverse events.</p><p id="P27">Most HCWs, however, expressed interest in learning about vaccine contraindications, safety and effectiveness. As one Australian study found, improving HCWs&#x02019; knowledge in influenza infection and vaccination may increase the likelihood of their recommending influenza vaccine [<xref rid="R19" ref-type="bibr">19</xref>].</p><p id="P28">China&#x02019;s health system may impact which HCWs are more likely to incorporate vaccine recommendations into their routine work. Community HCWs provide primary healthcare, disease prevention and health education, which target pregnant women, young children, older adults and adults with chronic diseases residing in the community [<xref rid="R17" ref-type="bibr">17</xref>]. Influenza vaccination services are usually offered at EPI clinics, which, in China, are most often located in community health centers. Therefore, when high risk groups receive recommendations from community HCWs, they have immediate access to on-site immunization. Although most HCWs in China do not routinely recommend seasonal influenza vaccination, we found that community HCWs were more likely than hospital HCWs to recommend vaccination and to get vaccinated themselves. These findings are consistent with studies conducted in the US and Australia [<xref rid="R19" ref-type="bibr">19</xref>,<xref rid="R20" ref-type="bibr">20</xref>].</p></sec></sec><sec id="S17"><label>6.</label><title>Limitations</title><p id="P29">Our studies have several limitations. First, the convenient samples of high risk groups surveyed may not adequately represent these populations in the community. Second, vaccination status was self-reported and not verified through records. Finally, this study discusses just one component of what should become a multi-pronged strategy to increase seasonal influenza vaccination.</p></sec><sec id="S18"><label>7.</label><title>Recommendations</title><p id="P30">Our results suggest the utility of the following steps: (1) providing community HCWs with accurate information about influenza infection and seasonal influenza vaccination to ensure the knowledge required to make effective recommendations; (2) promoting annual influenza vaccination among community HCWs themselves; and (3) incorporating community HCWs&#x02019; recommendation for seasonal influenza vaccination into existing immunization, maternal healthcare, and chronic disease management programs in China.</p></sec></body><back><ack id="S20"><title>Acknowledgements</title><p id="P31">We thank all counterparts who participated in the implementation of the four KAP studies. We also thank those who contributed to study design, including Luzhao Feng, Jiandong Zheng, Jeffrey McFarland, Mei Shang, Danielle Iuliano, and Mark Thompson. In addition, we acknowledge Lance Rodewald for his review of this manuscript.</p><p id="P32">Funding</p><p id="P33">This work was supported by the Cooperative Agreement Number 1U2GGH000961, funded by the Centers for Disease Control and Prevention. The findings and conclusions in this report are those of the authors and do not necessarily represent the official position of the Centers for Disease Control and Prevention.</p></ack><fn-group><fn fn-type="COI-statement" id="FN3"><p id="P34">Conflict of interest</p><p id="P35">None.</p></fn></fn-group><ref-list><title>References</title><ref id="R1"><label>[1]</label><mixed-citation publication-type="book"><collab>World Health Organization</collab>. <part-title>Vaccines against influenza</part-title>. <source>WHO position paper November 2012</source> (WHO, <month>November</month>
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<hr/>
</th></tr></thead><tbody><tr><td align="left" valign="top" rowspan="1" colspan="1">Received seasonal influenza vaccine in past year</td><td align="left" valign="top" rowspan="1" colspan="1">22% (children vaccinated) (95% CI: 18&#x02013;27%)</td><td align="left" valign="top" rowspan="1" colspan="1">0 (95% CI: &#x0003c; 0.2%)</td><td align="left" valign="top" rowspan="1" colspan="1">0.8% (95% CI: 0.3&#x02013;2.3%)</td><td align="left" valign="top" rowspan="1" colspan="1">5% (95% CI: 4&#x02013;6%)</td></tr><tr><td align="left" valign="top" rowspan="1" colspan="1">Received HCW<sup><xref rid="TFN1" ref-type="table-fn">a</xref></sup> recommendation for seasonal influenza vaccination in past year</td><td align="left" valign="top" rowspan="1" colspan="1">27% (95% CI: 23&#x02013;32%)</td><td align="left" valign="top" rowspan="1" colspan="1">4% (95% CI: 2.8&#x02013;4.6%)</td><td align="left" valign="top" rowspan="1" colspan="1">Not asked</td><td align="left" valign="top" rowspan="1" colspan="1">Not asked</td></tr><tr><td align="left" valign="top" rowspan="1" colspan="1">Reported willingness to get vaccinated if HCW recommended vaccine</td><td align="left" valign="top" rowspan="1" colspan="1">Not asked</td><td align="left" valign="top" rowspan="1" colspan="1">31% (95% CI: 29&#x02013;33%)</td><td align="left" valign="top" rowspan="1" colspan="1">78% (95% CI: 74&#x02013;82%)</td><td align="left" valign="top" rowspan="1" colspan="1">N/A</td></tr><tr><td align="left" valign="top" rowspan="1" colspan="1">Main barriers to vaccination reported<sup><xref rid="TFN2" ref-type="table-fn">b</xref></sup></td><td align="left" valign="top" rowspan="1" colspan="1">&#x02003;(1) Vaccine safety (62%)<break/>&#x02003;(2) No HCW recommendation (37%)<break/>&#x02003;(3) Vaccination not necessary (25%)<break/>&#x02003;(4) Limited vaccine effectiveness (23%)</td><td align="left" valign="top" rowspan="1" colspan="1">&#x02003;(1) Harm to fetus (83%)<break/>&#x02003;(2) Vaccine safety for pregnant women (28%)<break/>&#x02003;(3) Vaccination not necessary (22%)</td><td align="left" valign="top" rowspan="1" colspan="1">&#x02003;(1) Vaccination not necessary (33%)<break/>&#x02003;(2) Medical insurance does not cover influenza vaccine (24%)<break/>&#x02003;(3) No HCW recommendation (23%)<break/>&#x02003;(4) Vaccine safety (22%)</td><td align="left" valign="top" rowspan="1" colspan="1">&#x02003;(1) Vaccine safety (43%)<break/>&#x02003;(2) Vaccination not necessary (27%)<break/>&#x02003;(3) No time for vaccination (24%)<break/>&#x02003;(4) Limited vaccine effectiveness (20%)</td></tr><tr><td align="left" valign="top" rowspan="1" colspan="1">Preferred resources for receiving vaccine information</td><td align="left" valign="top" rowspan="1" colspan="1">&#x02003;(1) TV (64%)<break/>&#x02003;(2) Internet (57%)<break/>&#x02003;(3) Educational leaflets (51%)</td><td align="left" valign="top" rowspan="1" colspan="1">&#x02003;(1) TV (56%)<break/>&#x02003;(2) Internet (39%)<break/>&#x02003;(3) HCWs (34%)</td><td align="left" valign="top" rowspan="1" colspan="1">&#x02003;(1) HCWs (74%)<break/>&#x02003;(2) Community health lecture (41%)<break/>&#x02003;(3) TV/Radio (24%)<break/>&#x02003;(4) Friends/Family member (24%)</td><td align="left" valign="top" rowspan="1" colspan="1">&#x02003;(1) Internet (76%)<break/>&#x02003;(2) TV/Radio (75%)<break/>&#x02003;(3) Newspapers/books (55%)<break/>&#x02003;(4) Colleagues (50%)</td></tr></tbody></table><table-wrap-foot><fn id="TFN1"><label>a</label><p id="P38">HCW &#x02013; Healthcare worker.</p></fn><fn id="TFN2"><label>b</label><p id="P39">Cost and poor access were listed as options for main barriers to vaccination in the surveys to guardians, adults aged 60 years and older and HCWs, however only adults 60 years and older listed cost as one of the main barriers to vaccination. In 2014, the average cost of the seasonal influenza vaccine in China was 10&#x02013;15 USD. Cost and access were not included as options in the vaccine barrier question to pregnant women.</p></fn></table-wrap-foot></table-wrap></floats-group></article>