Statistics

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    "textoCompleto" => "<span class="elsevierStyleSections"><span id="sec0005" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0015">Introduction</span><p id="par0005" class="elsevierStylePara elsevierViewall">Tuberculosis &#40;TB&#41; and COVID-19 show similarities and differences&#44; as recently discussed in the scientific literature&#46;<a class="elsevierStyleCrossRefs" href="#bib0005"><span class="elsevierStyleSup">1&#8211;7</span></a></p><p id="par0010" class="elsevierStylePara elsevierViewall">Both diseases have similar signs and symptoms&#44;<a class="elsevierStyleCrossRefs" href="#bib0030"><span class="elsevierStyleSup">6&#8211;10</span></a> rendering their differential diagnosis difficult as they may also present concomitantly&#46; They might require hospital admission&#44; although justified by different reasons&#46;</p><p id="par0015" class="elsevierStylePara elsevierViewall">Indications of hospital admission for COVID-19 patients have been changing during the evolution of the ongoing pandemic&#46; The occurrence of clinical deterioration<a class="elsevierStyleCrossRefs" href="#bib0055"><span class="elsevierStyleSup">11&#44;12</span></a> with progressive dyspnoea and desaturation requiring medical therapy &#40;e&#46;g&#46;&#44; dexamethasone&#41; and non-invasive or invasive ventilatory support represents the most important recommendation for an immediate hospitalization as in other respiratory conditions&#46;<a class="elsevierStyleCrossRefs" href="#bib0060"><span class="elsevierStyleSup">12&#8211;14</span></a> Nevertheless&#44; no previously used criteria or scores have been validated for COVID-19 patients to decide in favour of hospitalization or not<a class="elsevierStyleCrossRef" href="#bib0075"><span class="elsevierStyleSup">15</span></a> and new specific criteria are being explored&#46;<a class="elsevierStyleCrossRef" href="#bib0080"><span class="elsevierStyleSup">16</span></a></p><p id="par0020" class="elsevierStylePara elsevierViewall">Indications of hospital admission for TB patients are more complex&#44; and in different countries can go far beyond the occurrence of a life-threatening condition&#46; Moreover&#44; they evolved over time&#46; At the time of sanatoria and during the pre-antibiotic era<a class="elsevierStyleCrossRefs" href="#bib0085"><span class="elsevierStyleSup">17&#44;18</span></a> admission was used as an &#8216;isolation&#8217; intervention to reduce <span class="elsevierStyleItalic">Mycobacterium tuberculosis</span> transmission within the community and as support measure to ensure rest&#44; optimal nutrition and eventually to perform pneumothorax after Carlo Forlanini&#8217;s discovery in 1907&#46;<a class="elsevierStyleCrossRef" href="#bib0095"><span class="elsevierStyleSup">19</span></a> In addition&#44; in children severe extra-pulmonary TB and social circumstances likely contributed to hospitalization&#46;<a class="elsevierStyleCrossRef" href="#bib0100"><span class="elsevierStyleSup">20</span></a></p><p id="par0025" class="elsevierStylePara elsevierViewall">Over time&#44; hospital admission was considered ideal to better monitor the initial phase of anti-TB treatment and eventually drug adverse events&#44; and&#44; in some countries&#44; to ensure adequate adherence to the prescribed regimen&#46;<a class="elsevierStyleCrossRefs" href="#bib0105"><span class="elsevierStyleSup">21&#44;22</span></a> Furthermore&#44; in several countries hospital admission is still considered an administrative measure of infection control&#44; as patients cannot be discharged until they achieve sputum smear and&#47;or culture conversion<a class="elsevierStyleCrossRefs" href="#bib0105"><span class="elsevierStyleSup">21&#44;22</span></a> Although the World Health Organization &#40;WHO&#41; recommends limiting unnecessary hospitalization&#44; this is often complicated by a&#8217; per occupied bed&#8217; refund mechanism prevailing in some countries<a class="elsevierStyleCrossRefs" href="#bib0110"><span class="elsevierStyleSup">22&#8211;24</span></a> and a sub-optimal Directly Observed Treatment &#40;DOT&#41;&#47;patient&#8217;s support practices at outpatient settings&#46;</p><p id="par0030" class="elsevierStylePara elsevierViewall">The present review evaluates the available evidence on hospital admission for TB and TB&#47;COVID-19 and discusses the criteria guiding hospitalization&#46;</p><p id="par0035" class="elsevierStylePara elsevierViewall">Finally&#44; recommendations are made following a recently published WHO &#40;Regional Office for Europe&#41; document on how to reduce <span class="elsevierStyleItalic">Mycobacterium tuberculosis</span> transmission in Europe&#46;<a class="elsevierStyleCrossRefs" href="#bib0105"><span class="elsevierStyleSup">21&#44;22</span></a></p></span><span id="sec0010" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0020">Methods</span><p id="par0040" class="elsevierStylePara elsevierViewall">A non-systematic search of the scientific literature in English was carried out on PubMed without time restrictions using the following key-words&#58; &#8216;hospital admission&#8217; &#8216;COVID-19&#8217;&#44; &#8216;tuberculosis&#8217;&#44; &#8216;length of stay&#8217;&#44; &#8216;ambulatory care&#8217;&#44; &#8216;prevention&#8217;&#44; &#8216;infection control&#8217;&#44; and &#8216;workplace&#8217;&#46;</p><p id="par0045" class="elsevierStylePara elsevierViewall">As hospital admission implies programmatic costs&#44; we report available information on this obtained from the literature review&#46;</p><p id="par0050" class="elsevierStylePara elsevierViewall">Data on TB admissions were retrieved from countries of the WHO European Region &#40;WHO workshop&#58; Lessons learned from finance reforms on TB control&#44; Copenhagen&#44; Denmark&#44; April 26th 2016&#59; unpublished data reporting 2014 data&#41; and from relevant existing cohorts allowing analysis of hospital admission-related information&#46;</p><p id="par0055" class="elsevierStylePara elsevierViewall">They include a secondary analysis of a large GTN cohort &#40;global bedaquiline study&#41;<a class="elsevierStyleCrossRef" href="#bib0125"><span class="elsevierStyleSup">25</span></a> and&#44; for the duration of the hospital stay for TB in patients with COVID-19&#44; from the ongoing global study on TB&#47;COVID-19<a class="elsevierStyleCrossRef" href="#bib0130"><span class="elsevierStyleSup">26</span></a> &#40;interim analysis&#44; November 27th&#44; 2020&#44; see references for details on the two studies&#41;&#46;</p><p id="par0060" class="elsevierStylePara elsevierViewall">WHO definitions of multidrug-resistant &#40;MDR&#41; and extensively drug-resistant &#40;XDR&#41; TB were adopted&#46;<a class="elsevierStyleCrossRef" href="#bib0135"><span class="elsevierStyleSup">27</span></a> Although not approved by WHO &#40;but largely used by clinicians&#41;&#44; pre-XDR TB was defined as a form of TB caused by an MDR-TB strain with additional resistance to either a fluoroquinolone or a second line-injectable agent &#40;amikacin&#44; capreomycin or kanamycin&#41;&#46;<a class="elsevierStyleCrossRefs" href="#bib0125"><span class="elsevierStyleSup">25&#44;28</span></a></p><p id="par0065" class="elsevierStylePara elsevierViewall">A writing committee of international experts including members of the Global Tuberculosis Network &#40;GTN&#41; developed the document after multiple rounds of revision&#46; The document was then proposed for endorsement to the GTN&#46;<a class="elsevierStyleCrossRefs" href="#bib0055"><span class="elsevierStyleSup">11&#44;29</span></a> The number of invited GTN members and those endorsing the document is reported under acknowledgements&#46;</p></span><span id="sec0015" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0025">Evidence on TB hospital admission</span><span id="sec0020" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0030">European data &#40;2016&#44; unpublished and WHO&#47;ECDC tuberculosis surveillance and monitoring 2020&#41;<a class="elsevierStyleCrossRef" href="#bib0150"><span class="elsevierStyleSup">30</span></a></span><p id="par0070" class="elsevierStylePara elsevierViewall">The available data &#40;average length of stay &#91;ALOS&#93; and proportion of hospital admissions for drug-susceptible and MDR-TB&#41; are presented in <a class="elsevierStyleCrossRef" href="#fig0005">Figs&#46; 1</a>&#8211;<a class="elsevierStyleCrossRef" href="#fig0015">3</a>&#44; while implications for hospital admission and discharge are discussed in the following sections&#46;</p><elsevierMultimedia ident="fig0005"></elsevierMultimedia><elsevierMultimedia ident="fig0010"></elsevierMultimedia><elsevierMultimedia ident="fig0015"></elsevierMultimedia><p id="par0075" class="elsevierStylePara elsevierViewall">The Netherlands&#44; Norway&#44; Portugal and Sweden reported the shortest length of stay &#40;LOS&#41; &#40;&#60;20 days&#41;&#44; whereas Hungary the highest &#40;&#62;80 days&#41; &#40;<a class="elsevierStyleCrossRef" href="#fig0005">Fig&#46; 1</a> shows the newly diagnosed 2014 cases reported in 2016&#41;&#46;</p><p id="par0080" class="elsevierStylePara elsevierViewall">Several Eastern Europe and Central Asia &#40;EECA&#41; countries reported LOS&#8239;&#8805;&#8239;60 days&#44; with only Estonia and Georgia showing a LOS&#8239;&#60;&#8239;40 days&#46; The Netherlands&#44; Portugal and Sweden admitted &#60;40&#37; of the diagnosed patients&#44; whereas Norway the vast majority&#46; Other countries admitted from 80&#37; to 100&#37;&#46;</p><p id="par0085" class="elsevierStylePara elsevierViewall">MDR- and XDR-TB patients had a LOS&#8239;&#60;&#8239;50 days in Norway &#40;<a class="elsevierStyleCrossRef" href="#fig0010">Fig&#46; 2</a>&#41;&#59; Estonia&#44; Georgia&#44; Portugal&#44; Romania&#44; Sweden and Uzbekistan reported &#60;100 days&#46; Kyrgyzstan had the lowest proportion of hospitalized patients &#40;&#60;40&#37;&#41;&#46;</p><p id="par0090" class="elsevierStylePara elsevierViewall">In 2018 the Netherlands and Portugal reported the lowest proportion of admitted drug-susceptible TB cases &#40;30&#37;&#41;&#44; Ireland and Sweden &#8764;50&#37;&#44; Estonia and Hungary 60&#37;&#44; and the remaining countries a proportion higher than 80&#37; &#40;<a class="elsevierStyleCrossRef" href="#fig0015">Fig&#46; 3</a>&#41;&#46;<a class="elsevierStyleCrossRefs" href="#bib0135"><span class="elsevierStyleSup">27&#44;30</span></a></p><p id="par0095" class="elsevierStylePara elsevierViewall">The indicator &#8216;percentage of hospitalization for new TB patients&#8217;&#40;1&#46;C&#46;1&#44; <a class="elsevierStyleCrossRef" href="#fig0015">Fig&#46; 3</a>&#41; has been added to allow a comprehensive evaluation of the different aspects of TB management in the Region&#46;</p><p id="par0100" class="elsevierStylePara elsevierViewall">An important note is that the information included in <a class="elsevierStyleCrossRefs" href="#fig0005">Figs&#46; 1&#8211;3</a> refers to countries with different epidemiological characteristics and different rules&#47;practices governing admission and discharge of TB patients&#46;</p></span><span id="sec0025" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0035">Global bedaquiline study &#40;2017&#41;<a class="elsevierStyleCrossRef" href="#bib0125"><span class="elsevierStyleSup">25</span></a></span><p id="par0105" class="elsevierStylePara elsevierViewall">Although the bedaquiline study was not specifically designed to describe hospital admission &#40;its main focus was the programmatic evaluation of safety and effectiveness of bedaquiline-containing regimens&#41;&#44; it included detailed information on this&#44; which is useful to report and discuss&#46;</p><p id="par0110" class="elsevierStylePara elsevierViewall">A total of 364&#47;428 &#40;85&#37;&#41; TB cases from 16 countries &#40;Argentina&#44; Australia&#44; Belarus&#44; Belgium&#44; Greece&#44; India&#44; Italy&#44; the Netherlands&#44; Peru&#44; Portugal&#44; South Africa&#44; Russian Federation&#44; Spain&#44; Sweden&#44; and the United Kingdom&#41; were admitted to hospital&#58; the final anti-TB treatment outcome was reported for 224&#47;368&#44; with 144&#47;368 still on treatment&#44; while no information on hospitalization was available for 60 &#40;14&#37;&#41;&#46; The proportion of patients admitted to hospital with a final outcome was&#58; 5&#47;224 &#40;11&#37;&#41; for MDR-TB&#44; 68&#47;224 &#40;65&#37;&#41; for pre XDR-TB&#44; and 111&#47;224 &#40;24&#37;&#41; for XDR-TB&#46; The proportions of admission for those still on treatment were&#58; 31&#47;144 &#40;21&#46;5&#37;&#41; for MDR-TB&#44; 44&#47;144 &#40;30&#46;5&#37;&#41; for pre XDR-TB and 69&#47;144 &#40;47&#46;9&#37;&#41; for XDR-TB&#46;</p><p id="par0115" class="elsevierStylePara elsevierViewall">The median &#40;IQR&#41; LOS was 178&#46;5 &#40;93&#46;5&#8211;302&#46;5&#41; days for patients who completed their treatment and 180 &#40;91&#8211;217&#41; days for those still on therapy&#46;</p><p id="par0120" class="elsevierStylePara elsevierViewall">In this study&#44; countries from different settings had different rules&#47;practices on TB patients&#8217; admission and discharge&#46; Furthermore&#44; as the study described the early phase of bedaquilne use&#44; a possible bias related to increased hospital admissions due to uncomplete understanding on adverse events severity cannot be excluded&#46;</p></span><span id="sec0030" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0040">Global TB and COVID-19 project &#40;2020&#44; interim analysis&#41;<a class="elsevierStyleCrossRef" href="#bib0130"><span class="elsevierStyleSup">26</span></a></span><p id="par0125" class="elsevierStylePara elsevierViewall">At an interim analysis &#40;preliminary data&#44; unpublished&#41; on the first 381 patients&#44; 222 &#40;58&#37;&#41; were hospitalized for TB &#40;46&#47;222 with final anti-TB treatment outcome and 176&#47;222 still on treatment&#41;&#44; 118 &#40;31&#37;&#41; were not hospitalized&#44; and 41 &#40;11&#37;&#41; with unavailable data&#46;</p><p id="par0130" class="elsevierStylePara elsevierViewall">Importantly&#44; 141 &#40;37&#37;&#41; patients were admitted for concomitant TB and COVID-19&#46; More information on hospital admissions will be possible when the global dataset&#44; in its final format&#44; will be analyzed&#46;</p><p id="par0135" class="elsevierStylePara elsevierViewall">The median &#40;IQR&#41; LOS for TB patients with a final treatment outcome was 29 &#40;10&#46;8&#8211;36&#46;5&#41; days&#44; lower than that for patients still on treatment &#40;47&#44; 13&#46;5&#8211;106&#46;5 days&#41;&#46;</p></span></span><span id="sec0035" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0045">Relevant experiences from the literature in Africa&#44; America and Europe</span><span id="sec0040" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0050">Africa</span><p id="par0140" class="elsevierStylePara elsevierViewall">A cost analysis performed in South Africa<a class="elsevierStyleCrossRef" href="#bib0155"><span class="elsevierStyleSup">31</span></a> clearly demonstrated that significant savings can be obtained by reducing the LOS of MDR-TB cases&#46; A decentralised model of TB care improves case detection and treatment initiation rates&#44; ensuring treatment outcomes comparable to those seen in centralised specialist centre&#46;<a class="elsevierStyleCrossRef" href="#bib0160"><span class="elsevierStyleSup">32</span></a> Adoption of decentralised treatment in South Africa may reduce the overall costs for the national TB programme by 15&#8211;18&#37;&#46;<a class="elsevierStyleCrossRefs" href="#bib0155"><span class="elsevierStyleSup">31&#44;33</span></a></p><p id="par0145" class="elsevierStylePara elsevierViewall">Hospital admission could be limited to patients facing treatment-related issues &#40;such as life-threatening conditions&#44; drug adverse events&#44; failure&#44; need to use injectable medicines or other treatment measures not manageable outside the hospital&#41;&#44; which might more frequently occur in patients with XDR- than with MDR-TB &#40;although XDR-TB does not <span class="elsevierStyleItalic">per se</span> contraindicate the possibility of home management&#41;&#46;<a class="elsevierStyleCrossRef" href="#bib0155"><span class="elsevierStyleSup">31</span></a> Adequate referral system from primary healthcare to specialised services is needed to maintain a continuum of care&#46;</p><p id="par0150" class="elsevierStylePara elsevierViewall">Children are often admitted to hospital for diagnostic reasons&#44; but long-term admission is mainly because of disease severity&#44; including TB meningitis&#44; TB&#47;HIV co-infection and drug-resistant TB&#44; social circumstances or a combination of disease severity and social circumstances&#46;<a class="elsevierStyleCrossRef" href="#bib0170"><span class="elsevierStyleSup">34</span></a></p><p id="par0155" class="elsevierStylePara elsevierViewall">TB meningitis&#44; the most devastating form of TB in children&#44; is often treated in hospital&#46; A study in Cape Town&#44; South Africa showed huge cost savings and improved family interaction with effective home-based treatment with good follow-up in children deemed clinically and socially suitable for home-based TB meningitis treatment&#46;<a class="elsevierStyleCrossRef" href="#bib0175"><span class="elsevierStyleSup">35</span></a></p></span><span id="sec0045" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0055">America</span><p id="par0160" class="elsevierStylePara elsevierViewall">In Montreal&#44; Canada&#44; a study evaluated LOS temporal trends for patients with pulmonary TB between 1993 and 2007&#46;<a class="elsevierStyleCrossRef" href="#bib0180"><span class="elsevierStyleSup">36</span></a> The median LOS was 17&#46;0 days&#44; with positive sputum-smear cases showing a longer hospital stay &#40;&#8805;14 days&#41; in comparison with those without &#40;OR&#8239;&#61;&#8239;1&#46;90&#59; 95&#37; CI&#58; 1&#46;34&#8211;2&#46;70&#41;&#46; Furthermore&#44; older age &#40;&#8805;50 VS&#46; 18&#8211;49 years&#41; was associated with longer LOS &#40;OR&#8239;&#61;&#8239;1&#46;66&#59; 95&#37; CI&#58; 1&#46;15&#8211;2&#46;40&#41;&#46; A LOS&#8239;&#8805;&#8239;14 days was consistent with the minimum length recommended by national guidelines but further evidence was needed to evaluate the impact of hospital admission in reducing the community risk of <span class="elsevierStyleItalic">Mycobacterium tuberculosis</span> transmission&#46;</p><p id="par0165" class="elsevierStylePara elsevierViewall">Another experience from Montreal &#40;January 1997- May 2007&#41; reported on 0&#46;65 hospitalizations per TB case&#44; with 17&#46;8 hospital days per TB patient&#44; and a mean LOS of 27&#46;2 days&#46;<a class="elsevierStyleCrossRef" href="#bib0185"><span class="elsevierStyleSup">37</span></a></p><p id="par0170" class="elsevierStylePara elsevierViewall">In the USA<a class="elsevierStyleCrossRef" href="#bib0190"><span class="elsevierStyleSup">38</span></a> the overall mean annual number of hospitalization events per individual TB patient increased over time from 0&#46;49 &#40;1997&#8211;2000&#41; to 0&#46;57 &#40;2013&#8211;2016&#41;&#46; Moreover&#44; the mean LOS increased from 7&#46;3 to 11&#46;3 days&#44; equal to a change from 3&#46;6 to 6&#46;5 hospital-days per patient&#46;</p><p id="par0175" class="elsevierStylePara elsevierViewall">The mean &#40;standard deviation &#91;SD&#93;&#41; LOS in three Brazilian hospitals in 2013 was 28&#46;2 &#40;32&#46;6&#41; days&#44; without statistically significant differences between HIV-positive and -negative TB patients&#46;<a class="elsevierStyleCrossRef" href="#bib0120"><span class="elsevierStyleSup">24</span></a></p><p id="par0180" class="elsevierStylePara elsevierViewall">Of a cohort of 3991 TB&#47;HIV co-infected patients in Rio de Janeiro&#44; Brazil&#44;<a class="elsevierStyleCrossRef" href="#bib0195"><span class="elsevierStyleSup">39</span></a> evaluated between 2007 and 2013&#44; 46&#46;6&#37; were hospital admitted &#40;10&#46;44 per 100 person-years&#41;&#46; An annual decrease was recorded for both the hospitalization rate &#40;incidence rate ratio 0&#46;92&#41; and LOS &#40;median of 15 days in 2007 VS&#46; 11 days in 2013&#59; p-value for trend &#60;0&#46;001&#41;&#46;</p></span><span id="sec0050" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0060">Europe</span><p id="par0185" class="elsevierStylePara elsevierViewall">A survey conducted in 1999 in an Italian sample recruiting 203 pulmonology centres showed a median LOS of 34 days for sputum smear-positive&#44; 20 days for sputum smear-negative&#44; and 21&#46;5 days for extra-pulmonary TB cases&#46; Sputum smear conversion to negative was considered the key criterion for discharge in 61&#37; of the centres&#46;<a class="elsevierStyleCrossRef" href="#bib0200"><span class="elsevierStyleSup">40</span></a> A switch from hospital- to home-based treatment &#40;limiting hospital admission to severe cases&#41; was recommended based on cost-effectiveness&#46;<a class="elsevierStyleCrossRef" href="#bib0205"><span class="elsevierStyleSup">41</span></a> In the study no information of the patients&#8217; drug resistance profile was available&#46;</p><p id="par0190" class="elsevierStylePara elsevierViewall">In a Portuguese sample of 15&#44;296 TB cases &#40;4&#44;415&#44; 28&#46;9&#37; admitted&#41; enrolled between 2008 and 2013&#44; hospital admission did not influence treatment outcomes&#44; with 13&#46;8&#37; unfavourable outcomes among hospitalized patients compared with 7&#46;6&#37; among non-hospitalized ones&#46;<a class="elsevierStyleCrossRefs" href="#bib0210"><span class="elsevierStyleSup">42&#44;43</span></a></p><p id="par0195" class="elsevierStylePara elsevierViewall">In the Russian Federation&#44; as published in 2007&#44; the LOS was rather longer both before &#40;86 days&#41; and after &#40;90 days&#41; the implementation of the WHO Directly observed treatment&#44; short-course &#40;DOTS&#41; Strategy&#46;<a class="elsevierStyleCrossRef" href="#bib0220"><span class="elsevierStyleSup">44</span></a> This LOS refers to patients with drug-susceptible TB&#46;</p><p id="par0200" class="elsevierStylePara elsevierViewall">In Spain 41&#37; of cases were managed in 2014&#8211;2015 as outpatients&#44;<a class="elsevierStyleCrossRef" href="#bib0225"><span class="elsevierStyleSup">45</span></a> with a mean LOS of 11&#46;3 &#40;&#177;7&#41; days&#46; Out of 319 patients included in the study&#44; only 14 &#40;4&#46;5&#37;&#41; were TB drug-resistant&#46; The authors concluded that an important proportion of the overall management cost of TB patients was related to hospital admission&#44; and recommended to reduce the hospital stay&#46; This prospective study involved 19 hospitals belonging to SEPAR &#40;Sociedad Espa&#241;ola de Aparato Respiratorio&#41; network&#46;</p><p id="par0205" class="elsevierStylePara elsevierViewall">A recent study from Switzerland<a class="elsevierStyleCrossRef" href="#bib0230"><span class="elsevierStyleSup">46</span></a> estimated a TB hospitalization rate of 81&#37; between 2002 and 2015&#44; with a median &#40;IQR&#41; LOS of 14 days &#40;6&#8211;22&#41;&#46; LOS increased in case of miliary TB&#44; older age&#44; and for some hospital locations&#46; The most prevalent comorbidities were HIV infection&#44; liver disease&#44; anaemia&#44; malnutrition&#44; and genito-urinary tract disease&#46; LOS was specifically evaluated in the following sub-groups&#58; 1&#41; malnutrition&#44; cachexia and anaemia &#40;median&#44; IQR&#58; 20&#44; 13&#8211;31&#44; days&#41;&#59; 2&#41; alcoholic liver disease and hepatitis &#40;median&#44; IQR&#58; 23&#44; 14&#8211;37&#46;5&#44; days&#41; and 3&#41; adverse drug events &#40;median&#44; IQR&#58; 20&#44; 13&#8211;30&#44; days&#41;&#46;</p></span><span id="sec0055" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0065">Summary of the findings</span><p id="par0210" class="elsevierStylePara elsevierViewall"><ul class="elsevierStyleList" id="lis0005"><li class="elsevierStyleListItem" id="lsti0005"><span class="elsevierStyleLabel">1&#41;</span><p id="par0215" class="elsevierStylePara elsevierViewall">The proportion of <span class="elsevierStyleItalic">newly diagnosed</span> admitted TB cases ranges between 50&#37; and 100&#37; &#40;47&#37; in Brazil&#44; 57&#37; in USA&#44; 65&#37; in Canada&#44; &#62;80&#37; in the WHO European Region where the proportion of patients hospitalized is higher than in the other settings evaluated&#59;</p></li><li class="elsevierStyleListItem" id="lsti0010"><span class="elsevierStyleLabel">2&#41;</span><p id="par0220" class="elsevierStylePara elsevierViewall">The proportion of <span class="elsevierStyleItalic">MDR-TB</span> admitted patients is &#8764;100&#37; in Europe and 85&#37; in the bedaquiline study&#59;</p></li><li class="elsevierStyleListItem" id="lsti0015"><span class="elsevierStyleLabel">3&#41;</span><p id="par0225" class="elsevierStylePara elsevierViewall">The proportion of <span class="elsevierStyleItalic">TB and COVID-19</span> admitted patients is around 58&#37; according to the limited evidence available&#44; which included about 80&#37; of drug-susceptible TB patients&#46;<a class="elsevierStyleCrossRef" href="#bib0130"><span class="elsevierStyleSup">26</span></a> Different reasons are likely behind this figure&#44; including the need to admit patients after simultaneous diagnosis of both diseases&#44; or to re-hospitalize TB cases already discharged after initial anti-TB treatment and worsened because of COVID-19 &#40;or COVID-19 appearing in already hospitalized TB patients&#41;&#46;</p></li><li class="elsevierStyleListItem" id="lsti0020"><span class="elsevierStyleLabel">4&#41;</span><p id="par0230" class="elsevierStylePara elsevierViewall">LOS of <span class="elsevierStyleItalic">newly diagnosed cases</span> ranges from 20 to 60 days in Europe&#44; similarly to Canada &#40;mean 17 and median 27 days&#41;&#44; Brazil &#40;median 15 days&#41;&#44; and Italy &#40;not included in the European dataset&#58; 31 days for sputum smear-positive patients and 20 days for other cases&#41;&#46; Studies from USA report the lowest LOS &#40;mean 10 days&#41; and the Russian Federation the highest &#40;&#8764;90 days&#41;&#46;</p></li><li class="elsevierStyleListItem" id="lsti0025"><span class="elsevierStyleLabel">5&#41;</span><p id="par0235" class="elsevierStylePara elsevierViewall">LOS of <span class="elsevierStyleItalic">MDR-TB patients</span> was 50&#8211;100 days in most of European countries&#44; &#8764;180 days in the bedaquiline study &#40;which reported severe cases with high proportion of XDR-TB&#41; and 29&#8211;47 days for <span class="elsevierStyleItalic">TB and COVID patients</span>&#46;</p></li></ul></p><p id="par0240" class="elsevierStylePara elsevierViewall">The duration of hospital stay depends on bacteriological conversion in several countries&#46;</p></span></span><span id="sec0060" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0070">TB&#47;COVID-19 admissions</span><span id="sec0065" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0075">Global TB&#47;COVID-19 project &#40;2020&#44; interim analysis&#41;</span><p id="par0245" class="elsevierStylePara elsevierViewall">An interim analysis was conducted on 381 patients from 40 countries&#58; 263&#47;381 &#40;69&#37;&#41; were hospitalized for COVID-19&#44; 31&#47;263 &#40;12&#37;&#41; were still hospitalized&#44; 201&#47;263 &#40;76&#37;&#41; were discharged and 31&#47;263 &#40;12&#37;&#41; died&#44; whereas 113&#47;381 &#40;30&#37;&#41; were not hospitalized&#46; Information on hospital admission was missing in 5 &#40;1&#37;&#41; patients&#46; As reported under &#8216;TB admissions&#8217;&#44; a total of 141&#47;381 &#40;37&#37;&#41; patients underwent hospital admission for concomitant TB and COVID-19&#46;</p><p id="par0250" class="elsevierStylePara elsevierViewall">The median &#40;IQR&#41; LOS attributed to COVID-19 was 16 &#40;10&#8211;22&#41; days&#46;</p><p id="par0255" class="elsevierStylePara elsevierViewall">Hospital admission data for COVID-19 is not yet comprehensively and systematically reported by Member States to WHO&#46; Following different sources of already existing data inputs&#44; however&#44; hospital stay duration can differ widely depending on numerous factors&#44; including age and co-morbidities among others&#46;</p><p id="par0260" class="elsevierStylePara elsevierViewall">A study conducted in 25 European countries by the members of the Paediatric Tuberculosis Network European Trials Group on COVID-19&#44; hospital admissions in children and adolescents identified 582 individuals during April 2020 with polymerase chain reaction &#40;PCR&#41; test confirmed of SARS-CoV-2 infection with a median &#40;IQR&#41; age of 5&#183;0 years &#40;0&#183;5&#8211;12&#183;0&#41;&#58; TB was not documented as comorbidity in any of these individuals&#46;<a class="elsevierStyleCrossRef" href="#bib0235"><span class="elsevierStyleSup">47</span></a></p></span></span><span id="sec0070" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0080">Recommendations on hospital admission</span><p id="par0265" class="elsevierStylePara elsevierViewall">Several documents consistently reported recommendations for TB-related hospital admission in Europe<a class="elsevierStyleCrossRefs" href="#bib0105"><span class="elsevierStyleSup">21&#44;22&#44;48</span></a> summarised as follows&#58;<ul class="elsevierStyleList" id="lis0010"><li class="elsevierStyleListItem" id="lsti0030"><span class="elsevierStyleLabel">a&#41;</span><p id="par0270" class="elsevierStylePara elsevierViewall">TB-related conditions requiring hospital treatment &#40;i&#46;e&#46;&#44; respiratory failure and surgical emergencies e&#46;g -haemorrhage&#44; pneumothorax&#44; and pleural effusion&#41;&#59;</p></li><li class="elsevierStyleListItem" id="lsti0035"><span class="elsevierStyleLabel">b&#41;</span><p id="par0275" class="elsevierStylePara elsevierViewall">Severe forms of TB and&#47;or pre-existing co-morbidities exacerbated by TB which cannot be managed in outpatient settings &#40;e&#46;g&#46;&#44; coma&#44; liver or renal disease&#44; uncontrolled diabetes&#44; etc&#46;&#41;<a class="elsevierStyleCrossRef" href="#bib0245"><span class="elsevierStyleSup">49</span></a>&#59;</p></li><li class="elsevierStyleListItem" id="lsti0040"><span class="elsevierStyleLabel">c&#41;</span><p id="par0280" class="elsevierStylePara elsevierViewall">Life-threatening or severe adverse effects associated to anti-TB drugs &#40;e&#46;g&#46;&#44; arrhythmias&#44; psychosis&#44; renal failure&#44; hearing loss&#41;&#44; particularly in fragile&#47;non-self-sufficient patients&#46;</p></li></ul></p><p id="par0285" class="elsevierStylePara elsevierViewall">Additional considerations on hospitalization include&#58;<ul class="elsevierStyleList" id="lis0015"><li class="elsevierStyleListItem" id="lsti0045"><span class="elsevierStyleLabel">1&#41;</span><p id="par0290" class="elsevierStylePara elsevierViewall">Patients where effective and safe treatment cannot be ensured in outpatient&#44; community&#44; and home settings &#40;e&#46;g&#46;&#44; homelessness&#44; overcrowding&#44; exposure of children aged &#60;5 years and pregnant women in households&#44; children with severe TB and unreliable caregivers&#41; or difficult geographical accessibility &#40;e&#46;g&#46;&#44; long distance to outpatient facilities or problematic travel conditions&#41;&#59;</p></li><li class="elsevierStyleListItem" id="lsti0050"><span class="elsevierStyleLabel">2&#41;</span><p id="par0295" class="elsevierStylePara elsevierViewall">Involuntary isolation of non-adherent patients once all other healthcare options have been unsuccessfully tried&#46;</p></li></ul></p><p id="par0300" class="elsevierStylePara elsevierViewall">It was recommended to care for admitted patients in single rooms&#46; In hospital settings&#44; people with presumed infectious TB or confirmed pulmonary TB should be assessed rapidly for MDR-TB&#44; using existing rapid diagnostic methods to allow adequate management and reducing the risk of transmission&#44; especially to those patients with immune-compromised conditions&#47;status&#46;</p><p id="par0305" class="elsevierStylePara elsevierViewall">Importantly&#44; several pre-conditions have been proposed to allow safe in-hospital management&#58;<ul class="elsevierStyleList" id="lis0020"><li class="elsevierStyleListItem" id="lsti0055"><span class="elsevierStyleLabel">a&#41;</span><p id="par0310" class="elsevierStylePara elsevierViewall">Appropriate infection control and prevention measures should be in place and continuously assessed<a class="elsevierStyleCrossRef" href="#bib0250"><span class="elsevierStyleSup">50</span></a>&#59;</p></li><li class="elsevierStyleListItem" id="lsti0060"><span class="elsevierStyleLabel">b&#41;</span><p id="par0315" class="elsevierStylePara elsevierViewall">Respiratory isolation rooms should be available for TB patients until they are smear&#47;culture-negative&#59;</p></li><li class="elsevierStyleListItem" id="lsti0065"><span class="elsevierStyleLabel">c&#41;</span><p id="par0320" class="elsevierStylePara elsevierViewall">Staff should be trained and adequately supervised&#44; and adhere to administrative measures included in the facility&#8217;s infection control and prevention plan&#59;</p></li><li class="elsevierStyleListItem" id="lsti0070"><span class="elsevierStyleLabel">d&#41;</span><p id="par0325" class="elsevierStylePara elsevierViewall">Trained staff should be available to ensure quality patient-centred care&#59;</p></li><li class="elsevierStyleListItem" id="lsti0075"><span class="elsevierStyleLabel">e&#41;</span><p id="par0330" class="elsevierStylePara elsevierViewall">Open and safe space should be available for patients to socialize according to infectiousness status and resistance patterns &#40;ideally not mixing infectious with non-infectious patients or drug-susceptible and drug-resistant patients&#41;&#59;</p></li><li class="elsevierStyleListItem" id="lsti0080"><span class="elsevierStyleLabel">f&#41;</span><p id="par0335" class="elsevierStylePara elsevierViewall">&#8220;Friendly&#8221; but effective administrative procedures should be in place to facilitate regular access of visitors&#59;</p></li><li class="elsevierStyleListItem" id="lsti0085"><span class="elsevierStyleLabel">g&#41;</span><p id="par0340" class="elsevierStylePara elsevierViewall">Protocols should be in place for effective communication and coordination&#44; detailing terms of reference for involved staff including accountability and responsibility&#44; for laboratories providing services during treatment and for peripheral units receiving patients after hospital discharge&#59;</p></li><li class="elsevierStyleListItem" id="lsti0090"><span class="elsevierStyleLabel">h&#41;</span><p id="par0345" class="elsevierStylePara elsevierViewall">Reference clinical centres located in low TB incidence countries should ensure quality services based on a minimum number of patients necessary to maintain proficiency&#46;</p></li></ul></p><p id="par0350" class="elsevierStylePara elsevierViewall">Specific recommendations on hospitalization of TB&#47;COVID-19 patients are not yet available&#46; As of today&#44; we need to consider the existing criteria for the most severe prevalent condition&#46; If TB is the most relevant condition&#44; the criteria defined above can be used to guide decisions&#46; COVID-19 hospitalization will be needed when the disease is clinically severe&#44; i&#46;e&#46; in presence of respiratory failure &#40;desaturations&#44; and need for oxygen supplementation or mechanical ventilation&#41; or&#44; in the future&#44; when the patient will meet specific clinical-radiological scores that are under study&#46;<a class="elsevierStyleCrossRef" href="#bib0060"><span class="elsevierStyleSup">12</span></a></p></span><span id="sec0075" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0085">Criteria guiding hospital discharge</span><p id="par0355" class="elsevierStylePara elsevierViewall">Criteria for hospital discharge of co-infected &#40;SARS-COV-2 and TB&#41; patients should be based mainly on the TB clinical course given that COVID-19 is a disease with a fast clinical evolution and it can stop requiring hospitalization more rapidly than TB&#46;</p><p id="par0360" class="elsevierStylePara elsevierViewall">The criteria for hospital discharge are&#58;<ul class="elsevierStyleList" id="lis0025"><li class="elsevierStyleListItem" id="lsti0095"><span class="elsevierStyleLabel">a&#41;</span><p id="par0365" class="elsevierStylePara elsevierViewall">Clinical improvement of TB &#40;e&#46;g&#46; improvement of signs and symptoms&#44; radiological improvement&#44; weight gain&#41;&#59;</p></li><li class="elsevierStyleListItem" id="lsti0100"><span class="elsevierStyleLabel">b&#41;</span><p id="par0370" class="elsevierStylePara elsevierViewall">Clinical improvement of the co-morbidities and&#47;or of the adverse events precipitating the hospital admission&#59;</p></li><li class="elsevierStyleListItem" id="lsti0105"><span class="elsevierStyleLabel">c&#41;</span><p id="par0375" class="elsevierStylePara elsevierViewall">Effective treatment and continuity of care ensured with a patient-centred model of care as per WHO and national guidelines&#46;</p></li></ul></p><p id="par0380" class="elsevierStylePara elsevierViewall">Bacteriological conversion <span class="elsevierStyleItalic">per se</span> is not a mandatory criterion for hospital discharge&#44; given that precautions are recommended to educate family members on basic infection control and prevention requirements and to monitor the continuation of treatment at home&#46; Adequate treatment can render patients rapidly non-infectious&#44; although sputum smear positivity can be present for a longer period &#40;dead bacilli&#41;&#46;<a class="elsevierStyleCrossRefs" href="#bib0105"><span class="elsevierStyleSup">21&#44;22</span></a> Nevertheless&#44; transmission can occur if an ineffective regimen is prescribed &#8211; for example&#44; when a first-line or sub-optimal regimen is used in MDR-TB patients&#46; Thus&#44; MDR- and XDR-TB regimens need to be guided by rapid drug susceptibility testing&#46;<a class="elsevierStyleCrossRefs" href="#bib0105"><span class="elsevierStyleSup">21&#44;22&#44;29&#44;51</span></a><span class="elsevierStyleSup">&#44;</span><a class="elsevierStyleCrossRef" href="#bib0260"><span class="elsevierStyleSup">52</span></a></p><p id="par0385" class="elsevierStylePara elsevierViewall">Typically&#44; patients have already infected their household members prior to diagnosis&#46;<a class="elsevierStyleCrossRefs" href="#bib0105"><span class="elsevierStyleSup">21&#44;22</span></a> Therefore&#44; contact-tracing of household members and other close contacts is essential to rapidly diagnose and treat them and reduce transmission of <span class="elsevierStyleItalic">Mycobacterium tuberculosis</span> within the community&#46;</p><p id="par0390" class="elsevierStylePara elsevierViewall">In summary&#44; ambulatory treatment of TB &#40;regardless of smear and drug-susceptibility patterns&#41; is possible from the beginning to reduce the risk of hospital transmission and improve treatment adherence&#46; Importantly&#44; outpatient care should be organised following strict infection control and prevention measures&#46;</p></span><span id="sec0080" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0090">Conclusions</span><p id="par0395" class="elsevierStylePara elsevierViewall">Existing evidence from WHO guidance and the literature review indicate that a high proportion of TB cases continue to be admitted in hospitals&#44; and for relatively long length of stay&#46; This is particularly evident in Europe&#46;</p><p id="par0400" class="elsevierStylePara elsevierViewall">Among the different reasons behind this finding&#44; existing legislation on infection control &#40;e&#46;g&#46; patients cannot be discharged until bacteriological conversion has been achieved&#41; and funding mechanisms &#40;focus on per bed occupancy&#41; play a role&#44; slowing down the &#8216;reduction of unnecessary hospital admission&#8217; recommended by WHO&#46;</p><p id="par0405" class="elsevierStylePara elsevierViewall">A collaboration of all stakeholders involved in TB prevention&#44; diagnosis and treatment is necessary to support the WHO recommendations in order to reduce patient suffering&#44; TB transmission and lower costs within a patient-centred vision&#46;</p></span><span id="sec0085" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0095">Declarations of interest</span><p id="par0410" class="elsevierStylePara elsevierViewall">None&#46;</p></span><span id="sec0090" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0100">Funding source</span><p id="par0415" class="elsevierStylePara elsevierViewall">This research did not receive any specific grant from funding agencies in the public&#44; commercial&#44; or not-for-profit sectors&#46;</p></span></span>"
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          "titulo" => "Introduction"
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          "titulo" => "Methods"
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          "titulo" => "Evidence on TB hospital admission"
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              "titulo" => "European data &#40;2016&#44; unpublished and WHO&#47;ECDC tuberculosis surveillance and monitoring 2020&#41;"
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              "titulo" => "Global bedaquiline study &#40;2017&#41;"
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              "titulo" => "Global TB and COVID-19 project &#40;2020&#44; interim analysis&#41;"
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          "titulo" => "Relevant experiences from the literature in Africa&#44; America and Europe"
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              "titulo" => "Africa"
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              "titulo" => "Summary of the findings"
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          "titulo" => "TB&#47;COVID-19 admissions"
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              "titulo" => "Global TB&#47;COVID-19 project &#40;2020&#44; interim analysis&#41;"
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          "titulo" => "Recommendations on hospital admission"
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          "titulo" => "Criteria guiding hospital discharge"
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          "titulo" => "Declarations of interest"
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    "fechaRecibido" => "2020-12-16"
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            0 => "TB"
            1 => "COVID-19"
            2 => "Hospital admission"
            3 => "Discharge"
            4 => "Hospitalization criteria"
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        "resumen" => "<span id="abst0005" class="elsevierStyleSection elsevierViewall"><p id="spar0035" class="elsevierStyleSimplePara elsevierViewall">The scientific debate on the criteria guiding hospitalization of tuberculosis &#40;TB&#41; and COVID-19 patients is ongoing&#46;</p><p id="spar0040" class="elsevierStyleSimplePara elsevierViewall">The aim of this review is to present the available evidence on admission for TB and TB&#47;COVID-19 patients and discuss the criteria guiding hospitalization&#46; Furthermore&#44; recommendations are made as derived from recently published World Health Organization documents&#44; based on Global Tuberculosis Network &#40;GTN&#41; expert opinion&#46;</p><p id="spar0045" class="elsevierStyleSimplePara elsevierViewall">The core published documents and guidelines on the topic have been reviewed&#46;</p><p id="spar0050" class="elsevierStyleSimplePara elsevierViewall">The proportion of new TB cases admitted to hospital ranges between 50&#37; and 100&#37; while for multidrug-resistant &#40;MDR&#41; TB patients it ranges between 85 and 100&#37; globally&#46; For TB patients with COVID-19 the proportion of cases admitted is 58&#37;&#44; probably reflecting different scenarios related to the diagnosis of COVID-19 before&#44; after or at the same time of the active TB episode&#46; The hospital length of stay for drug-susceptible TB ranges from 20 to 60 days in most of countries&#44; ranging from a mean of 10 days &#40;USA&#41; to around 90 days in the Russian Federation&#46; Hospitalization is longer for MDR-TB &#40;50&#8211;180 days&#41;&#46;</p><p id="spar0055" class="elsevierStyleSimplePara elsevierViewall">The most frequently stated reasons for recommending hospital admission include&#58; severe TB&#44; infection control concerns&#44; co-morbidities and drug adverse events which cannot be managed at out-patient level&#46; The review also provides suggestions on hospital requirements for safe admissions as well as patient discharge criteria&#44; while underlining the relevance of patient-centred care through community&#47;home-based care&#46;</p></span>"
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        "nota" => "<p class="elsevierStyleNotepara" id="npar0005">The GTN Collaborators who contributed to this article are&#58; Tamila Abu Arkub &#40;Russia&#41;&#59; Onno W&#46; Akkerman &#40;The Netherlands&#41;&#59; Timothy R&#46; Aksamit &#40;USA&#41;&#59; Riccardo Alagna &#40;Italy&#41;&#59; Jan-Willem Alffenaar &#40;Australia&#41;&#59; Pedro Eduardo Almeida da Silva &#40;Brazil&#41;&#59; Evgeny Belilovski &#40;Russia&#41;&#59; Fran&#231;ois-Xavier Blanc&#44; &#40;France&#41;&#59; Sergey Borisov &#40;Russia&#41;&#59; Anna Cristina C&#46; Carvalho &#40;Brazil&#41;&#59; Luigi Ruffo Codecasa &#40;Italy&#41;&#59; Anh-Tuan Dinh Xuan &#40;France&#41;&#59; Luis Gustavo do Valle Bastos &#40;USA&#41;&#59; Jos&#233; Mar&#237;a Garc&#237;a Garc&#237;a &#40;Spain&#41;&#59; Laura Gillini &#40;Italy&#41;&#59; Devasena Gnanashanmugam &#40;USA&#41;&#59; Mishra Gyanshankar &#40;India&#41;&#59; Scott Hysell &#40;USA&#41;&#59; Benjamin Choon Heng Ho &#40;Singapore&#41;&#59; Rafael Laniado-Laborin &#40;Mexico&#41;&#59; Mark Lipman &#40;UK&#41;&#59; Selene Manga &#40;Peru&#41;&#59; Fernanda Mello &#40;Brazil&#41;&#59; Walter P&#46; Mukhwana &#40;Somalia&#41;&#59; Marcela Mu&#241;oz Torrico &#40;Mexico&#41;&#59; Catherine WM Ong &#40;Singapore&#41;&#59; Chizaram Onyeaghala &#40;Nigeria&#41;&#59; Domingo Palmero &#40;Argentina&#41;&#59; Apostolos Papavasileiou &#40;Greece&#41;&#59; Alberto Piubello &#40;Niger&#41;&#59; Mikhail Sinytsin &#40;Russia&#41;&#59; Ivan Solovi&#269; &#40;Slovakia&#41;&#59; Marina Tadolini &#40;Italy&#41;&#59; Zarir F Udwadia &#40;India&#41;&#59; Alessandro Wasum Mariani &#40;Brazil&#41;&#59; Richard Zaleskis &#40;Latvia&#41;&#59; Dominik Zenner &#40;UK&#41;&#46;</p>"
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        "texto" => "<p id="par0420" class="elsevierStylePara elsevierViewall">Out of 39 GTN members responding&#44; a single member&#44; although agreeing with the paper&#44; was unable to endorse it as needing the institutional clearance&#46; Of the remaining 38&#44; 37 endorsed the document &#40;97&#46;4&#37;&#41;&#46;</p><p id="par0425" class="elsevierStylePara elsevierViewall">This article belongs to the scientific activities of the WHO Collaborating Centre for Tuberculosis and Lung Diseases&#44; Tradate&#44; ITA-80&#44; 2017-2020- GBM&#47;RC&#47;LDA and of the European Research Initiative &#40;ERI&#41;&#46;</p><p id="par0430" class="elsevierStylePara elsevierViewall">The Authors wish to thank Szabolcs Szigeti and Alexandre Lourenco for providing data on hospital admission in Europe as well as Alberto L&#46; Garcia-Basteiro &#40;Barcelona Institute for Global Health&#44; Barcelona&#44; Spain&#41; and Askar Yedilbayev &#40;WHO Regional Office for Europe&#44; Copenhagen&#44; Denmark&#41; for their useful comments on the manuscript&#46;</p>"
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