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style="fill:#FFF" d="m320,350a153,153 0 1,0-2,2l170,170m-91-117 110,110-26,26-110-110"></path></svg></a><a id="jr-fip-done" class="wsprkl btn" title="Dismiss find">✘</a></nav><nav id="jr-fip-info-p"><a id="jr-fip-prev" class="wsprkl btn" title="Jump to previuos match">◀</a><button id="jr-fip-matches">no matches yet</button><a id="jr-fip-next" class="wsprkl btn" title="Jump to next match">▶</a></nav></nav></div><div id="jr-epub-interstitial" class="hidden"></div><div id="jr-content"><article data-type="main"><div class="main-content lit-style"><div class="fm-sec bkr_bottom_sep"><div class="bkr_thumb"><a href="https://www.nice.org.uk" title="National Institute for Health and Care Excellence (NICE)" class="img_link icnblk_img" ref="pagearea=logo&targetsite=external&targetcat=link&targettype=publisher"><img class="source-thumb" src="/corehtml/pmc/pmcgifs/bookshelf/thumbs/th-niceng188er3-lrg.png" alt="Cover of COVID-19 rapid guideline: managing the long-term effects of COVID-19 (NG188)" /></a></div><div class="bkr_bib"><h1 id="_NBK567263_"><span itemprop="name">COVID-19 rapid guideline: managing the long-term effects of COVID-19 (NG188)</span></h1><div class="subtitle">Evidence review 4: investigations</div><p><i>NICE Guideline, No. 188</i></p><div class="half_rhythm">London: <a href="https://www.nice.org.uk" ref="pagearea=meta&targetsite=external&targetcat=link&targettype=publisher"><span itemprop="publisher">National Institute for Health and Care Excellence (NICE)</span></a>; <span itemprop="datePublished">2020 Dec</span>.</div><div><a href="/books/about/copyright/">Copyright</a> © NICE 2020.</div></div><div class="bkr_clear"></div></div><div id="niceng188er3.s1"><h2 id="_niceng188er3_s1_">Literature search</h2><p>NICE’s information services team identified relevant evidence through focused evidence searches between 22 and 28 October 2020 (see <a href="#niceng188er3.app3">appendix 3</a>). Additional studies were also considered from NICE surveillance up to 28 October 2020. The studies identified in the searches and through NICE surveillance were subsequently assessed for inclusion (see <a href="#niceng188er3.app3">appendix 3</a> for further details). Results from the literature searches were screened using their titles and abstracts for relevance against the criteria from the protocol (see <a href="#niceng188er3.app2">appendix 2</a>). Four reviewers screened titles and abstracts. Having identified the evidence, four reviewers assessed the full text references of potentially relevant evidence to determine whether they met the inclusion criteria for this evidence review. All uncertainties were discussed amongst the reviewers and referred to an adviser if needed. See <a href="#niceng188er3.app4">appendix 4</a> for the study flow chart of included studies.</p><p>Healthcare Improvement Scotland knowledge management team also conducted a search to identify qualitative evidence to support the questions in this review. See <a href="https://www.sign.ac.uk/our-guidelines/managing-the-long-term-effects-of-covid-19" ref="pagearea=body&targetsite=external&targetcat=link&targettype=uri">Management of the long-term effects of COVID-19: the views and experience of patients, their families and carers</a> for more information. This review will be referred to in this document as ‘patient lived experience’.</p></div><div id="niceng188er3.s2"><h2 id="_niceng188er3_s2_">Methods and process</h2><p>This evidence review was developed using the methods and processes described the <a href="/books/NBK567263/bin/niceng188er3_bm1.pdf">methods chapter</a>.</p></div><div id="niceng188er3.s3"><h2 id="_niceng188er3_s3_">Review question 4</h2><p>
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<b>What investigations should be carried out to determine appropriate management or treatment of symptoms?</b>
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</p><p>The review protocol is shown in <a href="#niceng188er3.app2">appendix 2</a>.</p><div id="niceng188er3.s3.1"><h3>Included studies</h3><p>In total 4104 references were identified through the searches. Of these 505 were included and ordered for full text assessment. A total of 58 references were included for the whole guideline, 18 of which were included for this review. Of these 12 were cohort studies and 1 was a cross-sectional study. There was also 1 case study, 1 narrative review and consensus recommendations included for this review due to the indirectness of the cohort studies identified.</p><p>See <a href="/books/NBK567263/table/niceng188er3.tab1/?report=objectonly" target="object" rid-ob="figobniceng188er3tab1">table 1</a> for more details on the identified studies.</p><div class="iconblock whole_rhythm clearfix ten_col table-wrap" id="figniceng188er3tab1"><a href="/books/NBK567263/table/niceng188er3.tab1/?report=objectonly" target="object" title="Table 1" class="img_link icnblk_img" rid-ob="figobniceng188er3tab1"><img class="small-thumb" src="/corehtml/pmc/css/bookshelf/2.26/img/table-icon.gif" alt="Table Icon" /></a><div class="icnblk_cntnt"><h4 id="niceng188er3.tab1"><a href="/books/NBK567263/table/niceng188er3.tab1/?report=objectonly" target="object" rid-ob="figobniceng188er3tab1">Table 1</a></h4><p class="float-caption no_bottom_margin">Included studies for review question 4: Follow-up after acute COVID-19. </p></div></div></div><div id="niceng188er3.s3.2"><h3>Key results</h3><p>Out of the 18 studies identified, 17 did not strictly meet all of the PICO criteria. This was because the people included were not specifically enrolled into the studies for persistent and ongoing symptoms. These studies followed up people approximately 1 to 3 months following acute COVID-19. During this follow up, several investigations and assessments were carried out. These fell into the following categories: screening or assessment with questionnaires, physical tests, imaging or laboratory investigations. Only 4 of the 18 studies included only people who had not been hospitalised.</p></div><div id="niceng188er3.s3.3"><h3>Questionnaires and screening tools</h3><p>Four of the studies used tools for mental health screening for people who had been hospitalised. These tools included GAD7, PHQ9, PTSD-5 and trauma screening and cognitive impairment assessments. All four studies reported adverse mental health outcomes based on these assessments. One study, <a class="bibr" href="#niceng188er3.app5.ref14" rid="niceng188er3.app5.ref14">Raman 2020</a>, reported a significantly higher PHQ-9 scores 2 to 3 months after COVID-19 compared to controls who had not had COVID-19 (p=0.009).</p><p>There were also four studies that performed a level of functional assessment during follow up. Only 1 (<a class="bibr" href="#niceng188er3.app5.ref1" rid="niceng188er3.app5.ref1">Aliae 2020</a>) of the 4 studies included people who had not been hospitalised. These included assessments such as the SF-36 questionnaire, Epworth Sleepiness Scale, Fatigue Severity Scale, the Modified Rankin score and the pain, enjoyment of life and general activity scale. Two studies used a new Post-COVID-19 functional status assessment (PCFS). <a class="bibr" href="#niceng188er3.app5.ref14" rid="niceng188er3.app5.ref14">Raman 2020</a>, one of the few studies to include a control group, found that functional status (including physical functioning, role limitations due to physical or emotional health, energy and social functioning) was significantly worse in people 2-3 months after acute COVID-19 compared to those who did not have COVID-19 (all p values <0.05). <a class="bibr" href="#niceng188er3.app5.ref1" rid="niceng188er3.app5.ref1">Aliae 2020</a> found that most people approximately 35 days since acute COVID-19 had a range of functional restrictions ranging from negligible to severe on PCFS.</p><p><a class="bibr" href="#niceng188er3.app5.ref3" rid="niceng188er3.app5.ref3">D’Cruz 2020</a> was the only study to report on how to go about conducting assessments. They concluded that assessment should ideally be a face to face, holistic approach with a focus on rehabilitation and general wellbeing.</p></div><div id="niceng188er3.s3.4"><h3>Physical tests, imaging or laboratory investigations</h3><p>Respiratory tests were commonly used in the studies. These included pulmonary function tests such as spirometry and assessment using the Medical Research Council (MRC) Breathlessness Scale. Most studies found that people were still experiencing significant breathlessness at follow-up after acute COVID-19. <a class="bibr" href="#niceng188er3.app5.ref14" rid="niceng188er3.app5.ref14">Raman 2020</a> found that people who had been hospitalised for COVID-19 reported breathlessness (MRC dyspnoea score ≥2) 2-3 months after acute COVID-19 36/53 (64%) compared to 3/29 (10.3%) who had not had COVID-19 (p<0.0001).</p><p>Exercise tests were performed in many of the studies. The most common investigation was the 6-minute walk test. Other tests included the sit to stand test and the 4-metre gait speed test. Studies reported limitations in exercise such as limited distance walked and desaturation in people followed up after acute COVID-19.</p><p>Many studies used imaging when following up people after acute COVID-19. These were mostly chest X-ray, CT and MRI. <a class="bibr" href="#niceng188er3.app5.ref3" rid="niceng188er3.app5.ref3">D’Cruz 2020</a> reported that only 15/119 (13%) of people had evidence of COVID-related lung disease at 4-6 weeks after hospital discharge. However, they concluded that a chest X-ray is a poor marker of recovery, as people were showing abnormalities in other investigations, regardless of chest X-ray results. <a class="bibr" href="#niceng188er3.app5.ref5" rid="niceng188er3.app5.ref5">Dennis 2020</a> found that multi-organ MRI showed 70% of a population at low-risk of COVID-19 complications with ongoing symptoms had impairment of 1 or more organs at 4 months after initial symptoms. <a class="bibr" href="#niceng188er3.app5.ref10" rid="niceng188er3.app5.ref10">Huang 2020a</a> found that cardiac MRI in 15/26 (58%) people experiencing cardiac symptoms around 47 days after onset of symptoms had abnormal findings. These manifestations included myocardial oedema, fibrosis and impaired right ventricle function.</p><p>Blood investigations carried out in the studies included routine tests, inflammatory markers and markers for iron deficiency and anaemia. <a class="bibr" href="#niceng188er3.app5.ref5" rid="niceng188er3.app5.ref5">Dennis 2020</a> found that triglycerides (p=0.002), cholesterol (p=0.021), LDL-cholesterol (p=0.005) and transferrin saturation (p=0.005) were more likely to be abnormal in hospitalised (n=164) versus non-hospitalised individuals (n=37). <a class="bibr" href="#niceng188er3.app5.ref17" rid="niceng188er3.app5.ref17">Sonnweber 2020</a> reported that COVID-19 is associated with prolonged alterations of iron homeostasis, which may be linked to severity initial disease.</p></div><div id="niceng188er3.s3.5"><h3>Strengths and limitations</h3><p>This evidence is considered as very low quality for a variety of reasons. The primary aims of the studies were not to investigate ongoing symptoms in people, so can be considered as indirect evidence for this review. Most of the sample sizes were very small and usually recruited people following hospital discharge, which may limit the generalisability of the evidence. The majority of the data in the studies was collected around 4-6 weeks after acute COVID-19 so is limited to short-term follow-up only.</p></div><div id="niceng188er3.s3.6"><h3>Expert panel discussion</h3><p>This section describes how the expert panel considered the evidence in relation to the recommendations within the guidance.</p><div id="niceng188er3.s3.6.1"><h4>Relative value of different outcomes</h4><p>The expert panel would have expected to see outcomes of investigations carried out to rule out other diagnoses or confirm post-COVID-19 syndrome or dual diagnoses. As the evidence was indirect for this question, the panel were unable to draw conclusions from this evidence. However, they were able to identify the most commonly used tests in the literature during follow-up from acute COVID-19 and determine where abnormalities were often seen in these cohorts of people.</p></div><div id="niceng188er3.s3.6.2"><h4>Quality of the evidence</h4><p>The overall certainty in the evidence was very low. The study designs were limited to mainly cohort studies. Whilst this was expected in terms of SARS-CoV-2 being a novel virus, it means that the data is limited and unlikely to lead to any firm conclusions at this point in time. The aims of the studies did not directly answer the question on which investigations to carry out in people with ongoing symptoms. The panel were also particularly concerned with the generalisability of the evidence. They acknowledged that most of the participants recruited were previously hospitalised with acute COVID-19 and some of the results of the investigations carried out would be reflective of this. The panel also considered that the type of investigations carried out in the literature were more likely to be carried out in secondary care settings.</p><p>In addition to this, the panel considered that comorbidities and history of related illness were important in understanding the outcomes of investigations but these were not consistently reported across the studies. The panel highlighted that the quantitative evidence often excluded children and older people and were unable to extrapolate the evidence for these groups of people.</p></div><div id="niceng188er3.s3.6.3"><h4>Trade-off between benefits and harms</h4><p>The panel were minded that when carrying out investigations for ongoing symptoms following acute COVID-19, it was important that other potential diagnoses are not ignored whilst trying to determine if the symptoms are due to post-COVID-19 syndrome. The panel suggested that it would be useful to carry out blood tests that are commonly carried out to rule out or confirm other conditions. They also considered that people might not associate their symptoms with COVID-19, particularly if another event, for example, a stroke, has happened since. The panel were also aware that people might not always present in a typical way, which may particularly be the case with older adults and children. For these reasons, the panel agreed with the conclusions from <a class="bibr" href="#niceng188er3.app5.ref3" rid="niceng188er3.app5.ref3">D’Cruz 2020</a> that a holistic and preferably face to face assessment is very important from both a clinical and patient perspective. If a clinician can see the patient, then they may identify concerns that the patient may not be aware of themself and may not have reported in a telephone consultation for example.</p><p>Blood tests, chest X-rays and exercise tolerance tests, e.g. sit-to-stand test were the most commonly reported tests in the evidence. The panel considered that these tests would be useful for most people as investigations and to obtain baseline measures. The panel however agreed that clinical judgment would be needed for exercise tolerance tests because it could be harmful to some people (for example, people with chest pain or severe fatigue). The evidence showed that chest X-ray may be a poor marker of improvement so the panel suggested it should only be used to inform a holistic assessment on further care needs.</p></div><div id="niceng188er3.s3.6.4"><h4>Implementation and resource considerations</h4><p>The panel were concerned that some of the investigations reported in the literature were unlikely to be readily available everywhere. For example, spirometry currently has a long waiting list in the UK, due to it being an aerosol-generating procedure and therefore fewer tests are being carried out. Many of the tests in the literature are generally not carried out in primary care so the panel agreed it is important to consider the setting, availability and resources needed to carry out investigations. The panel had concerns about further over-loading both primary and secondary care clinicians. The evidence suggests that a face-to-face consultation is preferable, but this is currently difficult in the pandemic setting.</p></div><div id="niceng188er3.s3.6.5"><h4>Other considerations</h4><p>The panel agreed that it would be difficult to do a full examination and fully comprehensive history for a patient, especially considering the time constraints. However, they concluded that a full examination, including clinical history was very important. The panel emphasised the need to focus the examination on both what was appropriate to the patient and their symptoms and what matters most to the patient. The panel also highlighted that in their experience there are people who have had mild symptoms of COVID-19 and not realised, then later develop new symptoms. This also supports the need for taking a full history.</p><p>The panel did not think a specific battery of tests should be carried out in patients presenting with ongoing symptoms as this might include tests that will not affect how the patient is managed as well as being time and resource intensive. In addition, the evidence reviewed did not provide conclusive information on a battery of tests that should be conducted for this population. Instead, the panel considered that investigations should be focused on what a patient presents with, covering any ‘red flags’ that require urgent referral, as well as picking up on any ‘pink flags’ which would be less critical, but cumulatively would be causing significant problems for the patient. These tests should include assessment of cognitive, psychological, and psychiatric symptoms, as well as any physical assessments. As the panel were unable to recommend specific screening tools to be used in these assessments, they suggested research recommendations to determine which tools are the most useful. These research recommendations are outlined in the guideline.</p><p>The panel were aware from their experience that postural symptoms are common in people with ongoing symptoms of COVID-19 and therefore should be investigated.</p><p>The panel experience was consistent with the patient lived experience evidence. Patient data and consensus asserted that people feel more reassured when investigations are carried out. However, the panel were also mindful that some investigations could be anxiety-inducing. For example, some panel members reported that some patients are being asked to record pulse-oximetry readings at home. These readings can fluctuate and therefore cause a patient to worry unnecessarily.</p><p>The patient lived experience evidence indicated that having someone in a supportive role who could co-ordinate and guide investigations would be beneficial. The panel concluded that whilst such investigations are important, clinicians should ensure that people have clear instructions and know who to contact for support if needed.</p></div></div></div><div id="niceng188er3.app1"><h2 id="_niceng188er3_app1_">Appendix 1. Methods used to develop the guidance</h2><p>Please refer to <a href="/books/NBK567263/bin/niceng188er3_bm1.pdf">methods document</a> for details of the methods used to develop the guidance.</p></div><div id="niceng188er3.app2"><h2 id="_niceng188er3_app2_">Appendix 2. Review protocols</h2><div id="niceng188er3.app2.s1"><h3>RQ 4: What investigations should be carried out to determine appropriate management or treatment of symptoms?</h3><div class="iconblock whole_rhythm clearfix ten_col table-wrap" id="figniceng188er3app2tab1"><a href="/books/NBK567263/table/niceng188er3.app2.tab1/?report=objectonly" target="object" title="Table" class="img_link icnblk_img" rid-ob="figobniceng188er3app2tab1"><img class="small-thumb" src="/corehtml/pmc/css/bookshelf/2.26/img/table-icon.gif" alt="Table Icon" /></a><div class="icnblk_cntnt"><h4 id="niceng188er3.app2.tab1"><a href="/books/NBK567263/table/niceng188er3.app2.tab1/?report=objectonly" target="object" rid-ob="figobniceng188er3app2tab1">Table</a></h4><p class="float-caption no_bottom_margin">4 to 12 weeks from onset of acute COVID-19 12 weeks from onset of acute COVID-19</p></div></div></div></div><div id="niceng188er3.app3"><h2 id="_niceng188er3_app3_">Appendix 3. Literature search strategy</h2><div id="niceng188er3.app3.s1"><h3>Database strategies</h3><p>Please refer to the <a href="/books/NBK567263/bin/niceng188er3_bm2.pdf">search history record</a> for full details of the search.</p></div></div><div id="niceng188er3.app4"><h2 id="_niceng188er3_app4_">Appendix 4. Study flow diagram</h2><div id="niceng188er3.app4.fig1" class="figure"><div class="graphic"><a href="/core/lw/2.0/html/tileshop_pmc/tileshop_pmc_inline.html?title=Image%20niceng188er3app4f1&p=BOOKS&id=567263_niceng188er3app4f1.jpg" target="tileshopwindow" class="inline_block pmc_inline_block ts_canvas img_link" title="Click on image to zoom"><div class="ts_bar small" title="Click on image to zoom"></div><img src="/books/NBK567263/bin/niceng188er3app4f1.jpg" alt="Image niceng188er3app4f1" class="tileshop" title="Click on image to zoom" /></a></div></div></div><div id="niceng188er3.app5"><h2 id="_niceng188er3_app5_">Appendix 5. Included studies</h2><ul class="simple-list"><li class="half_rhythm"><p><div class="bk_ref" id="niceng188er3.app5.ref1">Aliae, Mohamed-Hussein, Islam, Galal, Mahmoud, Saad
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et al (2020) Post-COVID-19 Functional Status: Relation to age, smoking, hospitalization and comorbidities. medRxiv [<a href="/pmc/articles/PMC8388571/" ref="pagearea=cite-ref&targetsite=entrez&targetcat=link&targettype=pmc">PMC free article<span class="bk_prnt">: PMC8388571</span></a>] [<a href="https://pubmed.ncbi.nlm.nih.gov/34484441" ref="pagearea=cite-ref&targetsite=entrez&targetcat=link&targettype=pubmed">PubMed<span class="bk_prnt">: 34484441</span></a>]</div></p></li><li class="half_rhythm"><p><div class="bk_ref" id="niceng188er3.app5.ref2">Arnold, David T., Hamilton, Fergus W., Milne, Alice
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et al (2020) Patient outcomes after hospitalisation with COVID-19 and implications for follow-up; results from a prospective UK cohort. medRxiv: 2020081220173526 [<a href="/pmc/articles/PMC7716340/" ref="pagearea=cite-ref&targetsite=entrez&targetcat=link&targettype=pmc">PMC free article<span class="bk_prnt">: PMC7716340</span></a>] [<a href="https://pubmed.ncbi.nlm.nih.gov/33273026" ref="pagearea=cite-ref&targetsite=entrez&targetcat=link&targettype=pubmed">PubMed<span class="bk_prnt">: 33273026</span></a>]</div></p></li><li class="half_rhythm"><p><div class="bk_ref" id="niceng188er3.app5.ref3">D’Cruz, Rebecca F., Waller, Michael D., Perrin, Felicity
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et al (2020) Chest radiography is a poor predictor of respiratory symptoms and functional impairment in survivors of severe COVID-19 pneumonia. ERJ Open Research [<a href="/pmc/articles/PMC7585700/" ref="pagearea=cite-ref&targetsite=entrez&targetcat=link&targettype=pmc">PMC free article<span class="bk_prnt">: PMC7585700</span></a>] [<a href="https://pubmed.ncbi.nlm.nih.gov/33575312" ref="pagearea=cite-ref&targetsite=entrez&targetcat=link&targettype=pubmed">PubMed<span class="bk_prnt">: 33575312</span></a>]</div></p></li><li class="half_rhythm"><p><div class="bk_ref" id="niceng188er3.app5.ref4">Daher, Ayham, Balfanz, Paul, Cornelissen, Christian
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et al (2020) Follow up of patients with severe coronavirus disease 2019 (COVID-19): Pulmonary and extrapulmonary disease sequelae. Respiratory Medicine: 106197 to 106197
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[<a href="/pmc/articles/PMC7573668/" ref="pagearea=cite-ref&targetsite=entrez&targetcat=link&targettype=pmc">PMC free article<span class="bk_prnt">: PMC7573668</span></a>] [<a href="https://pubmed.ncbi.nlm.nih.gov/33120193" ref="pagearea=cite-ref&targetsite=entrez&targetcat=link&targettype=pubmed">PubMed<span class="bk_prnt">: 33120193</span></a>]</div></p></li><li class="half_rhythm"><p><div class="bk_ref" id="niceng188er3.app5.ref5">Dennis, Andrea, Wamil, Malgorzata, Kapur, Sandeep
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et al (2020) Multi-organ impairment in low-risk individuals with long COVID. medRxiv: 2020101420212555</div></p></li><li class="half_rhythm"><p><div class="bk_ref" id="niceng188er3.app5.ref6">Eiros, Rocio, Perez Manuel, Barreiro-Perez, Garcia Ana, Martin-Garcia
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et al
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Pericarditis and myocarditis long after SARS-CoV-2 infection: a cross-sectional descriptive study in health-care workers. medrxiv preprint</div></p></li><li class="half_rhythm"><p><div class="bk_ref" id="niceng188er3.app5.ref7">Frija-Masson, Justine, Debray, Marie-Pierre, Gilbert, Marie
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et al (2020) Functional characteristics of patients with SARS-CoV-2 pneumonia at 30 days post-infection. Eur. respir. j
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56(2) [<a href="/pmc/articles/PMC7301832/" ref="pagearea=cite-ref&targetsite=entrez&targetcat=link&targettype=pmc">PMC free article<span class="bk_prnt">: PMC7301832</span></a>] [<a href="https://pubmed.ncbi.nlm.nih.gov/32554533" ref="pagearea=cite-ref&targetsite=entrez&targetcat=link&targettype=pubmed">PubMed<span class="bk_prnt">: 32554533</span></a>]</div></p></li><li class="half_rhythm"><p><div class="bk_ref" id="niceng188er3.app5.ref8">Greenhalgh, T; Ladds, E; Knight, M
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‘Long Covid’: evidence, recommendations and priority research.</div></p></li><li class="half_rhythm"><p><div class="bk_ref" id="niceng188er3.app5.ref9">Hacettepe, University (2020) Investigation of Validity and Reliability of Post-COVID-19 Functional Status Scale. <a href="https://clinicaltrials.gov/" ref="pagearea=cite-ref&targetsite=external&targetcat=link&targettype=uri">clinicaltrials<wbr style="display:inline-block"></wbr>​.gov</a></div></p></li><li class="half_rhythm"><p><div class="bk_ref" id="niceng188er3.app5.ref10">Huang, Lu, Zhao, Peijun, Tang, Dazhong
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et al (2020) Cardiac Involvement in Patients Recovered From COVID-2019 Identified Using Magnetic Resonance Imaging. JACC. Cardiovascular imaging [<a href="/pmc/articles/PMC7214335/" ref="pagearea=cite-ref&targetsite=entrez&targetcat=link&targettype=pmc">PMC free article<span class="bk_prnt">: PMC7214335</span></a>] [<a href="https://pubmed.ncbi.nlm.nih.gov/32763118" ref="pagearea=cite-ref&targetsite=entrez&targetcat=link&targettype=pubmed">PubMed<span class="bk_prnt">: 32763118</span></a>]</div></p></li><li class="half_rhythm"><p><div class="bk_ref" id="niceng188er3.app5.ref11">Huang, Yiying, Tan, Cuiyan, Wu, Jian
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et al (2020) Impact of coronavirus disease 2019 on pulmonary function in early convalescence phase. Respiratory research
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21(1): 163
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[<a href="/pmc/articles/PMC7323373/" ref="pagearea=cite-ref&targetsite=entrez&targetcat=link&targettype=pmc">PMC free article<span class="bk_prnt">: PMC7323373</span></a>] [<a href="https://pubmed.ncbi.nlm.nih.gov/32600344" ref="pagearea=cite-ref&targetsite=entrez&targetcat=link&targettype=pubmed">PubMed<span class="bk_prnt">: 32600344</span></a>]</div></p></li><li class="half_rhythm"><p><div class="bk_ref" id="niceng188er3.app5.ref12">Mazza, Mario Gennaro, De Lorenzo, Rebecca, Conte, Caterina
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et al (2020) Anxiety and depression in COVID-19 survivors: Role of inflammatory and clinical predictors. Brain, behavior, and immunity
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89: 594 to 600
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[<a href="/pmc/articles/PMC7390748/" ref="pagearea=cite-ref&targetsite=entrez&targetcat=link&targettype=pmc">PMC free article<span class="bk_prnt">: PMC7390748</span></a>] [<a href="https://pubmed.ncbi.nlm.nih.gov/32738287" ref="pagearea=cite-ref&targetsite=entrez&targetcat=link&targettype=pubmed">PubMed<span class="bk_prnt">: 32738287</span></a>]</div></p></li><li class="half_rhythm"><p><div class="bk_ref" id="niceng188er3.app5.ref13">Podlasin, Regina B, Kowalska, Justyna D, Pihowicz, Andrzej
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et al (2020) How to follow-up a patient who received tocilizumab in severe COVID-19: a case report. European journal of medical research
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25(1): 37
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[<a href="/pmc/articles/PMC7450912/" ref="pagearea=cite-ref&targetsite=entrez&targetcat=link&targettype=pmc">PMC free article<span class="bk_prnt">: PMC7450912</span></a>] [<a href="https://pubmed.ncbi.nlm.nih.gov/32854774" ref="pagearea=cite-ref&targetsite=entrez&targetcat=link&targettype=pubmed">PubMed<span class="bk_prnt">: 32854774</span></a>]</div></p></li><li class="half_rhythm"><p><div class="bk_ref" id="niceng188er3.app5.ref14">Raman, Mp, Cassar, Em, Tunnicliffe
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et al (2020) Medium-term effects of SARS-CoV-2 infection on multiple vital organs, exercise capacity, cognition, quality of life and mental health, post-hospital discharge. [<a href="/pmc/articles/PMC7808914/" ref="pagearea=cite-ref&targetsite=entrez&targetcat=link&targettype=pmc">PMC free article<span class="bk_prnt">: PMC7808914</span></a>] [<a href="https://pubmed.ncbi.nlm.nih.gov/33490928" ref="pagearea=cite-ref&targetsite=entrez&targetcat=link&targettype=pubmed">PubMed<span class="bk_prnt">: 33490928</span></a>]</div></p></li><li class="half_rhythm"><p><div class="bk_ref" id="niceng188er3.app5.ref15">Savarraj, Jude PJ, Burkett, Angela B., Hinds, Sarah N.
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et al (2020) Three-month outcomes in hospitalized COVID-19 patients. medRxiv: 2020101620211029</div></p></li><li class="half_rhythm"><p><div class="bk_ref" id="niceng188er3.app5.ref16">Savastano, Alfonso, Crincoli, Emanuele, Savastano, Maria Cristina
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et al (2020) Peripapillary Retinal Vascular Involvement in Early Post-COVID-19 Patients. Journal of clinical medicine
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9(9) [<a href="/pmc/articles/PMC7565672/" ref="pagearea=cite-ref&targetsite=entrez&targetcat=link&targettype=pmc">PMC free article<span class="bk_prnt">: PMC7565672</span></a>] [<a href="https://pubmed.ncbi.nlm.nih.gov/32911619" ref="pagearea=cite-ref&targetsite=entrez&targetcat=link&targettype=pubmed">PubMed<span class="bk_prnt">: 32911619</span></a>]</div></p></li><li class="half_rhythm"><p><div class="bk_ref" id="niceng188er3.app5.ref17">Sonnweber, T., Boehm, A., Sahanic, S.
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et al (2020) Persisting alterations of iron homeostasis in COVID-19 are associated with non-resolving lung pathologies and poor patients’ performance: a prospective observational cohort study. Respiratory Research
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21(1): 276
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[<a href="/pmc/articles/PMC7575703/" ref="pagearea=cite-ref&targetsite=entrez&targetcat=link&targettype=pmc">PMC free article<span class="bk_prnt">: PMC7575703</span></a>] [<a href="https://pubmed.ncbi.nlm.nih.gov/33087116" ref="pagearea=cite-ref&targetsite=entrez&targetcat=link&targettype=pubmed">PubMed<span class="bk_prnt">: 33087116</span></a>]</div></p></li><li class="half_rhythm"><p><div class="bk_ref" id="niceng188er3.app5.ref18">Zhao, Yu-Miao, Shang, Yao-Min, Song, Wen-Bin
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et al (2020) Follow-up study of the pulmonary function and related physiological characteristics of COVID-19 survivors three months after recovery. EClinicalMedicine
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25: 100463
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[<a href="/pmc/articles/PMC7361108/" ref="pagearea=cite-ref&targetsite=entrez&targetcat=link&targettype=pmc">PMC free article<span class="bk_prnt">: PMC7361108</span></a>] [<a href="https://pubmed.ncbi.nlm.nih.gov/32838236" ref="pagearea=cite-ref&targetsite=entrez&targetcat=link&targettype=pubmed">PubMed<span class="bk_prnt">: 32838236</span></a>]</div></p></li></ul></div><div id="niceng188er3.app6"><h2 id="_niceng188er3_app6_">Appendix 6. Evidence tables</h2><p id="niceng188er3.app6.et1"><a href="/books/NBK567263/bin/niceng188er3-app6-et1.pdf" class="bk_dwnld_icn bk_dwnld_pdf">
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Aliae 2020
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</a><span class="small"> (PDF, 175K)</span></p><p id="niceng188er3.app6.et2"><a href="/books/NBK567263/bin/niceng188er3-app6-et2.pdf" class="bk_dwnld_icn bk_dwnld_pdf">
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Arnold 2020
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</a><span class="small"> (PDF, 187K)</span></p><p id="niceng188er3.app6.et3"><a href="/books/NBK567263/bin/niceng188er3-app6-et3.pdf" class="bk_dwnld_icn bk_dwnld_pdf">
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D’Cruz 2020
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</a><span class="small"> (PDF, 169K)</span></p><p id="niceng188er3.app6.et4"><a href="/books/NBK567263/bin/niceng188er3-app6-et4.pdf" class="bk_dwnld_icn bk_dwnld_pdf">
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Daher 2020
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</a><span class="small"> (PDF, 193K)</span></p><p id="niceng188er3.app6.et5"><a href="/books/NBK567263/bin/niceng188er3-app6-et5.pdf" class="bk_dwnld_icn bk_dwnld_pdf">
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Dennis 2020
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</a><span class="small"> (PDF, 226K)</span></p><p id="niceng188er3.app6.et6"><a href="/books/NBK567263/bin/niceng188er3-app6-et6.pdf" class="bk_dwnld_icn bk_dwnld_pdf">
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Frija-Masson 2020
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</a><span class="small"> (PDF, 184K)</span></p><p id="niceng188er3.app6.et7"><a href="/books/NBK567263/bin/niceng188er3-app6-et7.pdf" class="bk_dwnld_icn bk_dwnld_pdf">
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Eiros 2020
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</a><span class="small"> (PDF, 238K)</span></p><p id="niceng188er3.app6.et8"><a href="/books/NBK567263/bin/niceng188er3-app6-et8.pdf" class="bk_dwnld_icn bk_dwnld_pdf">
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Huang 2020a
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</a><span class="small"> (PDF, 142K)</span></p><p id="niceng188er3.app6.et9"><a href="/books/NBK567263/bin/niceng188er3-app6-et9.pdf" class="bk_dwnld_icn bk_dwnld_pdf">
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Huang 2020b
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</a><span class="small"> (PDF, 144K)</span></p><p id="niceng188er3.app6.et10"><a href="/books/NBK567263/bin/niceng188er3-app6-et10.pdf" class="bk_dwnld_icn bk_dwnld_pdf">
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Mazza 2020
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</a><span class="small"> (PDF, 178K)</span></p><p id="niceng188er3.app6.et11"><a href="/books/NBK567263/bin/niceng188er3-app6-et11.pdf" class="bk_dwnld_icn bk_dwnld_pdf">
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Podlasin 2020
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</a><span class="small"> (PDF, 144K)</span></p><p id="niceng188er3.app6.et12"><a href="/books/NBK567263/bin/niceng188er3-app6-et12.pdf" class="bk_dwnld_icn bk_dwnld_pdf">
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Raman 2020
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</a><span class="small"> (PDF, 206K)</span></p><p id="niceng188er3.app6.et13"><a href="/books/NBK567263/bin/niceng188er3-app6-et13.pdf" class="bk_dwnld_icn bk_dwnld_pdf">
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Savastano 2020
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</a><span class="small"> (PDF, 197K)</span></p><p id="niceng188er3.app6.et14"><a href="/books/NBK567263/bin/niceng188er3-app6-et14.pdf" class="bk_dwnld_icn bk_dwnld_pdf">
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Savarraj 2020
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</a><span class="small"> (PDF, 160K)</span></p><p id="niceng188er3.app6.et15"><a href="/books/NBK567263/bin/niceng188er3-app6-et15.pdf" class="bk_dwnld_icn bk_dwnld_pdf">
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Sonnweber 2020
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</a><span class="small"> (PDF, 182K)</span></p><p id="niceng188er3.app6.et16"><a href="/books/NBK567263/bin/niceng188er3-app6-et16.pdf" class="bk_dwnld_icn bk_dwnld_pdf">Valiente De-Santis 2020</a><span class="small"> (PDF, 191K)</span></p><p id="niceng188er3.app6.et17"><a href="/books/NBK567263/bin/niceng188er3-app6-et17.pdf" class="bk_dwnld_icn bk_dwnld_pdf">
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Zhao 2020
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</a><span class="small"> (PDF, 161K)</span></p><p id="niceng188er3.app6.et18"><a href="/books/NBK567263/bin/niceng188er3-app6-et18.pdf" class="bk_dwnld_icn bk_dwnld_pdf">
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Greenhalgh 2020a
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</a><span class="small"> (PDF, 148K)</span></p></div><div id="niceng188er3.app7"><h2 id="_niceng188er3_app7_">Appendix 7. Excluded studies</h2><p>Please refer to the full list of <a href="/books/NBK567263/bin/niceng188er3_bm3.pdf">excluded studies</a> for this guideline.</p></div><div id="niceng188er3.app8"><h2 id="_niceng188er3_app8_">Appendix 8. Supporting evidence</h2><p id="niceng188er3.app8.et1"><a href="/books/NBK567263/bin/niceng188er3-app8-et1.pdf" class="bk_dwnld_icn bk_dwnld_pdf">Spruit 2020</a><span class="small"> (PDF, 130K)</span></p></div></div><div class="fm-sec"><div class="half_rhythm"><a href="/books/about/copyright/">Copyright</a> © NICE 2020.</div><div class="small"><span class="label">Bookshelf ID: NBK567263</span><span class="label">PMID: <a href="https://pubmed.ncbi.nlm.nih.gov/33555767" title="PubMed record of this title" ref="pagearea=meta&targetsite=entrez&targetcat=link&targettype=pubmed">33555767</a></span></div></div><div class="small-screen-prev"></div><div class="small-screen-next"></div></article><article data-type="table-wrap" id="figobniceng188er3tab1"><div id="niceng188er3.tab1" class="table"><h3><span class="label">Table 1</span><span class="title">Included studies for review question 4: Follow-up after acute COVID-19</span></h3><p class="large-table-link" style="display:none"><span class="right"><a href="/books/NBK567263/table/niceng188er3.tab1/?report=objectonly" target="object">View in own window</a></span></p><div class="large_tbl" id="__niceng188er3.tab1_lrgtbl__"><table><thead><tr><th id="hd_h_niceng188er3.tab1_1_1_1_1" rowspan="1" colspan="1" style="text-align:left;vertical-align:top;">Study</th><th id="hd_h_niceng188er3.tab1_1_1_1_2" rowspan="1" colspan="1" style="text-align:left;vertical-align:top;">Country, study design, dates</th><th id="hd_h_niceng188er3.tab1_1_1_1_3" rowspan="1" colspan="1" style="text-align:left;vertical-align:top;">Population (n)</th><th id="hd_h_niceng188er3.tab1_1_1_1_4" rowspan="1" colspan="1" style="text-align:left;vertical-align:top;">Investigations</th><th id="hd_h_niceng188er3.tab1_1_1_1_5" rowspan="1" colspan="1" style="text-align:left;vertical-align:top;">Mean follow-up time since COVID-19</th><th id="hd_h_niceng188er3.tab1_1_1_1_6" rowspan="1" colspan="1" style="text-align:left;vertical-align:top;">Main results</th></tr></thead><tbody><tr><td headers="hd_h_niceng188er3.tab1_1_1_1_1" rowspan="1" colspan="1" style="text-align:left;vertical-align:top;">
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<a class="bibr" href="#niceng188er3.app5.ref1" rid="niceng188er3.app5.ref1">Aliae 2020</a>
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</td><td headers="hd_h_niceng188er3.tab1_1_1_1_2" rowspan="1" colspan="1" style="text-align:left;vertical-align:top;">Egypt, Cross sectional, 15th July to 13th August 2020</td><td headers="hd_h_niceng188er3.tab1_1_1_1_3" rowspan="1" colspan="1" style="text-align:left;vertical-align:top;">
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<p>Patients who have had COVID-19 (positive or indeterminate COVID-19 PCR test or presumed presence of COVID-19 based on clinical & radiological criteria).</p>
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<p>(n=444)</p>
|
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</td><td headers="hd_h_niceng188er3.tab1_1_1_1_4" rowspan="1" colspan="1" style="text-align:left;vertical-align:top;">Post-COVID-19 Functional Status Scale (PCFS) scale</td><td headers="hd_h_niceng188er3.tab1_1_1_1_5" rowspan="1" colspan="1" style="text-align:left;vertical-align:top;">35.31±18.75 days</td><td headers="hd_h_niceng188er3.tab1_1_1_1_6" rowspan="1" colspan="1" style="text-align:left;vertical-align:top;">Most of the COVID-19 recovered cases have diverse degrees of functional restrictions ranging from negligible to severe based on PCFS.</td></tr><tr><td headers="hd_h_niceng188er3.tab1_1_1_1_1" rowspan="1" colspan="1" style="text-align:left;vertical-align:top;">
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<a class="bibr" href="#niceng188er3.app5.ref2" rid="niceng188er3.app5.ref2">Arnold 2020</a>
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</td><td headers="hd_h_niceng188er3.tab1_1_1_1_2" rowspan="1" colspan="1" style="text-align:left;vertical-align:top;">UK, Prospective cohort, 30 March to 3 June 2020.</td><td headers="hd_h_niceng188er3.tab1_1_1_1_3" rowspan="1" colspan="1" style="text-align:left;vertical-align:top;">Patients hospitalised with COVID-19 (Positive PCR result for SARS-CoV-2 or a clinico-radiological diagnosis of COVID-19 disease) (n=110); No control group</td><td headers="hd_h_niceng188er3.tab1_1_1_1_4" rowspan="1" colspan="1" style="text-align:left;vertical-align:top;">
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<p>At 8 to 12 week follow up:</p>
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<p>Face to face review with a respiratory or infectious disease clinician</p>
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<p>Chest radiograph</p>
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<p>Spirometry</p>
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<p>Exercise testing (sit to stand)</p>
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<p>Routine bloods</p>
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<p>Routine observations</p>
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<p>HRQoL questionnaires</p>
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<p>Health status questionnaire</p>
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</td><td headers="hd_h_niceng188er3.tab1_1_1_1_5" rowspan="1" colspan="1" style="text-align:left;vertical-align:top;">28 days after admission (remotely to review hospital/ GP notes)</td><td headers="hd_h_niceng188er3.tab1_1_1_1_6" rowspan="1" colspan="1" style="text-align:left;vertical-align:top;">Patients with COVID-19 remain highly symptomatic at 8 to 12 weeks, however, clinical abnormalities requiring action are infrequent, especially in those without a supplementary oxygen requirement during their acute illness. This has significant implications for physicians assessing patients with persistent symptoms, suggesting that a more holistic approach focussing on rehabilitation and general wellbeing is paramount</td></tr><tr><td headers="hd_h_niceng188er3.tab1_1_1_1_1" rowspan="1" colspan="1" style="text-align:left;vertical-align:top;">
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<a class="bibr" href="#niceng188er3.app5.ref3" rid="niceng188er3.app5.ref3">D’Cruz 2020</a>
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</td><td headers="hd_h_niceng188er3.tab1_1_1_1_2" rowspan="1" colspan="1" style="text-align:left;vertical-align:top;">UK, Cohort study (prospective), June to July 2020</td><td headers="hd_h_niceng188er3.tab1_1_1_1_3" rowspan="1" colspan="1" style="text-align:left;vertical-align:top;">COVID-19 survivors who had been hospitalised with PCR-confirmed severe COVID-19 pneumonia (n=119); No control group</td><td headers="hd_h_niceng188er3.tab1_1_1_1_4" rowspan="1" colspan="1" style="text-align:left;vertical-align:top;">
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<p>Chest radiography</p>
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<p>Symptom questionnaires</p>
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<p>Mental health screening</p>
|
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<p>Physiological testing</p>
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<p>Computed tomography and pulmonary angiography (CTPA)</p>
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</td><td headers="hd_h_niceng188er3.tab1_1_1_1_5" rowspan="1" colspan="1" style="text-align:left;vertical-align:top;">
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<p>Median (IQR) times between hospital admission and discharge to follow-up assessment were 76 (71 to 83) days and 61 (51 to 67) days, respectively</p>
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<p>(4 to 12 weeks grouping)</p>
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</td><td headers="hd_h_niceng188er3.tab1_1_1_1_6" rowspan="1" colspan="1" style="text-align:left;vertical-align:top;">Persistent symptoms, adverse mental health outcomes and physiological impairment are common 2 months after severe COVID-19 pneumonia. Follow-up chest radiograph is a poor marker of recovery, therefore holistic face-to-face assessment is recommended to facilitate early recognition and management of post-COVID sequelae</td></tr><tr><td headers="hd_h_niceng188er3.tab1_1_1_1_1" rowspan="1" colspan="1" style="text-align:left;vertical-align:top;">
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<a class="bibr" href="#niceng188er3.app5.ref4" rid="niceng188er3.app5.ref4">Daher 2020</a>
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</td><td headers="hd_h_niceng188er3.tab1_1_1_1_2" rowspan="1" colspan="1" style="text-align:left;vertical-align:top;">Germany, Cohort (retrospective), February to May 2020</td><td headers="hd_h_niceng188er3.tab1_1_1_1_3" rowspan="1" colspan="1" style="text-align:left;vertical-align:top;">
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<p>Patients with COVID-19 who were discharged from the isolation ward and followed up 6 weeks after discharge (n=33)</p>
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<p>No control group</p>
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<p>All 33 patients had a severe disease during their hospital stay</p>
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</td><td headers="hd_h_niceng188er3.tab1_1_1_1_4" rowspan="1" colspan="1" style="text-align:left;vertical-align:top;">
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<p>Pulmonary function tests (PFTs)</p>
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<p>Electrocardiography</p>
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<p>Transthoracic echocardiography</p>
|
|
<p>Whole-body plethysmography</p>
|
|
<p>Blood tests</p>
|
|
<p>Heath-related quality of life</p>
|
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<p>6-min walk test</p>
|
|
</td><td headers="hd_h_niceng188er3.tab1_1_1_1_5" rowspan="1" colspan="1" style="text-align:left;vertical-align:top;">Time from discharge to follow up 56 (48 to 71) days</td><td headers="hd_h_niceng188er3.tab1_1_1_1_6" rowspan="1" colspan="1" style="text-align:left;vertical-align:top;">Hospitalized patients with severe COVID-19, who did not require mechanical ventilation, are unlikely to develop pulmonary long-term impairments, thromboembolic complications or cardiac impairments after discharge but frequently suffer from symptoms of fatigue.</td></tr><tr><td headers="hd_h_niceng188er3.tab1_1_1_1_1" rowspan="1" colspan="1" style="text-align:left;vertical-align:top;">
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<a class="bibr" href="#niceng188er3.app5.ref5" rid="niceng188er3.app5.ref5">Dennis 2020</a>
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</td><td headers="hd_h_niceng188er3.tab1_1_1_1_2" rowspan="1" colspan="1" style="text-align:left;vertical-align:top;">UK, Prospective cohort (ongoing), April to August 2020</td><td headers="hd_h_niceng188er3.tab1_1_1_1_3" rowspan="1" colspan="1" style="text-align:left;vertical-align:top;">
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<p>Patients with previous SARS-CoV-2 infection and low risk for COVID-19 severity and mortality (n=201)</p>
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<p>No control group</p>
|
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</td><td headers="hd_h_niceng188er3.tab1_1_1_1_4" rowspan="1" colspan="1" style="text-align:left;vertical-align:top;">
|
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<p>Symptom assessment</p>
|
|
<p>Multi-organ MRI</p>
|
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<p>Blood investigations for inflammatory markers</p>
|
|
</td><td headers="hd_h_niceng188er3.tab1_1_1_1_5" rowspan="1" colspan="1" style="text-align:left;vertical-align:top;">Around 3 to 5 months</td><td headers="hd_h_niceng188er3.tab1_1_1_1_6" rowspan="1" colspan="1" style="text-align:left;vertical-align:top;">In a young, low-risk population with ongoing symptoms, almost 70% of individuals have impairment in one or more organs four months after initial symptoms of SARS-CoV-2 infection.</td></tr><tr><td headers="hd_h_niceng188er3.tab1_1_1_1_1" rowspan="1" colspan="1" style="text-align:left;vertical-align:top;">
|
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<a class="bibr" href="#niceng188er3.app5.ref7" rid="niceng188er3.app5.ref7">Frija-Masson 2020</a>
|
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</td><td headers="hd_h_niceng188er3.tab1_1_1_1_2" rowspan="1" colspan="1" style="text-align:left;vertical-align:top;">France, Letter to editor (retrospective cohort), 4 March 2020 and 1 April 2020</td><td headers="hd_h_niceng188er3.tab1_1_1_1_3" rowspan="1" colspan="1" style="text-align:left;vertical-align:top;">
|
|
<p>Patients under the age of 85 years with confirmed SARS-CoV-2 infection</p>
|
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<p>(n=50)</p>
|
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<p>No control group</p>
|
|
</td><td headers="hd_h_niceng188er3.tab1_1_1_1_4" rowspan="1" colspan="1" style="text-align:left;vertical-align:top;">All tests included spirometry, functional residual capacity (FRC), total lung capacity (TLC) and DLCO (single breath real-time CO/NH4) measurements</td><td headers="hd_h_niceng188er3.tab1_1_1_1_5" rowspan="1" colspan="1" style="text-align:left;vertical-align:top;">1 month since symptom onset</td><td headers="hd_h_niceng188er3.tab1_1_1_1_6" rowspan="1" colspan="1" style="text-align:left;vertical-align:top;">1 month after SARS-CoV-2 infection, a majority of patients have mild alterations of lung function</td></tr><tr><td headers="hd_h_niceng188er3.tab1_1_1_1_1" rowspan="1" colspan="1" style="text-align:left;vertical-align:top;">
|
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<a class="bibr" href="#niceng188er3.app5.ref10" rid="niceng188er3.app5.ref10">Huang 2020a</a>
|
|
</td><td headers="hd_h_niceng188er3.tab1_1_1_1_2" rowspan="1" colspan="1" style="text-align:left;vertical-align:top;">China, Retrospective cohort, study date not reported (March 2020?)</td><td headers="hd_h_niceng188er3.tab1_1_1_1_3" rowspan="1" colspan="1" style="text-align:left;vertical-align:top;">
|
|
<p>Consecutive patients who were initially referred for cardiac CMR examination due to cardiac symptoms (n=26)</p>
|
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<p>Healthy controls of a similar age and gender who previously underwent the same CMR examinations were selected from a database of healthy subjects without cardiovascular disease or systemic inflammation (n=11)</p>
|
|
</td><td headers="hd_h_niceng188er3.tab1_1_1_1_4" rowspan="1" colspan="1" style="text-align:left;vertical-align:top;">Cardiac magnetic resonance (CMR)</td><td headers="hd_h_niceng188er3.tab1_1_1_1_5" rowspan="1" colspan="1" style="text-align:left;vertical-align:top;">Duration between cardiac symptoms onset to CMR examination mean 47 days (range 36-58 days)</td><td headers="hd_h_niceng188er3.tab1_1_1_1_6" rowspan="1" colspan="1" style="text-align:left;vertical-align:top;">Cardiac involvement was found in a proportion (58%) of patients recovered from COVID-19. CMR manifestation included myocardial oedema, fibrosis, and impaired right ventricle function.</td></tr><tr><td headers="hd_h_niceng188er3.tab1_1_1_1_1" rowspan="1" colspan="1" style="text-align:left;vertical-align:top;">
|
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<a class="bibr" href="#niceng188er3.app5.ref11" rid="niceng188er3.app5.ref11">Huang 2020b</a>
|
|
</td><td headers="hd_h_niceng188er3.tab1_1_1_1_2" rowspan="1" colspan="1" style="text-align:left;vertical-align:top;">China, Cohort (retrospective), study date not reported</td><td headers="hd_h_niceng188er3.tab1_1_1_1_3" rowspan="1" colspan="1" style="text-align:left;vertical-align:top;">
|
|
<p>Hospitalised COVID-19 patients that had been released from hospital over a period of 1 month (n=57)</p>
|
|
<p>No control group</p>
|
|
</td><td headers="hd_h_niceng188er3.tab1_1_1_1_4" rowspan="1" colspan="1" style="text-align:left;vertical-align:top;">
|
|
<p>Pulmonary function testing</p>
|
|
<p>Lung imaging (high resolution spiral CT)</p>
|
|
<p>6-min walk test</p>
|
|
</td><td headers="hd_h_niceng188er3.tab1_1_1_1_5" rowspan="1" colspan="1" style="text-align:left;vertical-align:top;">At least 30 days</td><td headers="hd_h_niceng188er3.tab1_1_1_1_6" rowspan="1" colspan="1" style="text-align:left;vertical-align:top;">Impaired diffusing-capacity, lower respiratory muscle strength, and lung imaging abnormalities were detected in more than half of the COVID-19 patients in early convalescence phase. Compared with non-severe cases, severe patients had a higher incidence of DLCO impairment and encountered more TLC decrease and 6MWD decline.</td></tr><tr><td headers="hd_h_niceng188er3.tab1_1_1_1_1" rowspan="1" colspan="1" style="text-align:left;vertical-align:top;">
|
|
<a class="bibr" href="#niceng188er3.app5.ref14" rid="niceng188er3.app5.ref14">Raman 2020</a>
|
|
</td><td headers="hd_h_niceng188er3.tab1_1_1_1_2" rowspan="1" colspan="1" style="text-align:left;vertical-align:top;">
|
|
<p>UK, Prospective cohort,</p>
|
|
<p>14 March to 25 May 2020</p>
|
|
</td><td headers="hd_h_niceng188er3.tab1_1_1_1_3" rowspan="1" colspan="1" style="text-align:left;vertical-align:top;">
|
|
<p>Patients hospitalised with moderate to severe laboratory-confirmed (SARS-CoV-2 polymerase chain reaction positive) COVID-19 (n=58)</p>
|
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<p>Uninfected controls group-matched for age, sex, body mass index (BMI) and risk factors (smoking, diabetes, and hypertension) from the community (during the same period) were prospectively enrolled in this study (n=30)</p>
|
|
</td><td headers="hd_h_niceng188er3.tab1_1_1_1_4" rowspan="1" colspan="1" style="text-align:left;vertical-align:top;">
|
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<p>Multiorgan magnetic resonance imaging (MRI) of the brain, lungs, heart, liver, kidneys</p>
|
|
<p>6-min walk test</p>
|
|
<p>Cardiopulmonary exercise test (CPET)</p>
|
|
<p>Spirometry</p>
|
|
<p>Questionnaires</p>
|
|
<p>Blood tests</p>
|
|
</td><td headers="hd_h_niceng188er3.tab1_1_1_1_5" rowspan="1" colspan="1" style="text-align:left;vertical-align:top;">Patients were assessed between 2 and 3 months from disease-onset at median interval of 2 to 3 months (IQR 2·06 to 2·53)</td><td headers="hd_h_niceng188er3.tab1_1_1_1_6" rowspan="1" colspan="1" style="text-align:left;vertical-align:top;">Persistent lung and extra-pulmonary organ MRI findings are common. In COVID-19 survivors, chronic inflammation may underlie multiorgan abnormalities and contribute to impaired quality of life</td></tr><tr><td headers="hd_h_niceng188er3.tab1_1_1_1_1" rowspan="1" colspan="1" style="text-align:left;vertical-align:top;">
|
|
<a class="bibr" href="#niceng188er3.app5.ref15" rid="niceng188er3.app5.ref15">Savarraj 2020</a>
|
|
</td><td headers="hd_h_niceng188er3.tab1_1_1_1_2" rowspan="1" colspan="1" style="text-align:left;vertical-align:top;">USA, Prospective cohort, May 2020 to July 2020</td><td headers="hd_h_niceng188er3.tab1_1_1_1_3" rowspan="1" colspan="1" style="text-align:left;vertical-align:top;">
|
|
<p>Hospitalised COVID-19 patients (n=48)</p>
|
|
<p>No control group</p>
|
|
</td><td headers="hd_h_niceng188er3.tab1_1_1_1_4" rowspan="1" colspan="1" style="text-align:left;vertical-align:top;">
|
|
<p>Telephone questionnaires to assess functional, cognitive, and psychiatric symptoms.</p>
|
|
<p>Functional outcome was evaluated using the modified Rankin Score (mRS).</p>
|
|
<p>Cognitive status was evaluated using the brief neurocognitive screening test (BNST).</p>
|
|
<p>Depression symptoms were evaluated using the Patient Health Questionnaire (PHQ-9).</p>
|
|
<p>Anxiety symptoms were assessed using the Generalized Anxiety Disorder (GAD-7).</p>
|
|
<p>Pain, fatigue, and sleepiness were evaluated using the Pain, Enjoyment of life and General activity (PEG), the Fatigue Severity Scale (FSS) and Epworth Sleepiness Scale (ESS).</p>
|
|
<p>Post-traumatic stress disorder was evaluated using the Primary Care PTSD Screen for DSM-5 (PC-PTSD-5).</p>
|
|
</td><td headers="hd_h_niceng188er3.tab1_1_1_1_5" rowspan="1" colspan="1" style="text-align:left;vertical-align:top;">
|
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<p>3 months</p>
|
|
<p>4 to 12 weeks grouping</p>
|
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</td><td headers="hd_h_niceng188er3.tab1_1_1_1_6" rowspan="1" colspan="1" style="text-align:left;vertical-align:top;">
|
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<p>71% had continued neurologic symptoms</p>
|
|
<p>The most common symptom was fatigue (42%) followed by PTSD symptoms (29%)</p>
|
|
</td></tr><tr><td headers="hd_h_niceng188er3.tab1_1_1_1_1" rowspan="1" colspan="1" style="text-align:left;vertical-align:top;">
|
|
<a class="bibr" href="#niceng188er3.app5.ref17" rid="niceng188er3.app5.ref17">Sonnweber 2020</a>
|
|
</td><td headers="hd_h_niceng188er3.tab1_1_1_1_2" rowspan="1" colspan="1" style="text-align:left;vertical-align:top;">Austria, Cohort (prospective), study date not reported</td><td headers="hd_h_niceng188er3.tab1_1_1_1_3" rowspan="1" colspan="1" style="text-align:left;vertical-align:top;">
|
|
<p>Patients who previously suffered from mild to critical COVID-19 (n=109)</p>
|
|
<p>No control group</p>
|
|
</td><td headers="hd_h_niceng188er3.tab1_1_1_1_4" rowspan="1" colspan="1" style="text-align:left;vertical-align:top;">
|
|
<p>Medical history assessment</p>
|
|
<p>Structured COVID-19 symptom questionnaire</p>
|
|
<p>Performance evaluation (e.g. 6-min walking test)</p>
|
|
<p>Blood sampling and analysis</p>
|
|
<p>Computed tomography</p>
|
|
</td><td headers="hd_h_niceng188er3.tab1_1_1_1_5" rowspan="1" colspan="1" style="text-align:left;vertical-align:top;">Approximately 2 months</td><td headers="hd_h_niceng188er3.tab1_1_1_1_6" rowspan="1" colspan="1" style="text-align:left;vertical-align:top;">COVID19 is associated with prolonged alterations of iron homeostasis which may be linked to severe initial disease but also persisting radiological pathologies in the lung and impaired physical performance.</td></tr><tr><td headers="hd_h_niceng188er3.tab1_1_1_1_1" rowspan="1" colspan="1" style="text-align:left;vertical-align:top;">
|
|
<a class="bibr" href="#niceng188er3.app5.ref13" rid="niceng188er3.app5.ref13">Podlasin 2020</a>
|
|
</td><td headers="hd_h_niceng188er3.tab1_1_1_1_2" rowspan="1" colspan="1" style="text-align:left;vertical-align:top;">Poland, Case study, study date not reported</td><td headers="hd_h_niceng188er3.tab1_1_1_1_3" rowspan="1" colspan="1" style="text-align:left;vertical-align:top;">
|
|
<p>A 27-year-old, otherwise healthy man with no health risks, was admitted to infectious disease ward with a week history of weakness, fever, and sore throat.</p>
|
|
<p>The patient was discharged from the hospital on day 21 after confirming significant improvement in his CT scan and two negative SARS-CoV-2 RT-PCR from nasopharyngeal swabs</p>
|
|
</td><td headers="hd_h_niceng188er3.tab1_1_1_1_4" rowspan="1" colspan="1" style="text-align:left;vertical-align:top;">
|
|
<p>X-ray</p>
|
|
<p>RT-PCR</p>
|
|
<p>Blood investigations</p>
|
|
</td><td headers="hd_h_niceng188er3.tab1_1_1_1_5" rowspan="1" colspan="1" style="text-align:left;vertical-align:top;">Follow up hospitalisation on day 35</td><td headers="hd_h_niceng188er3.tab1_1_1_1_6" rowspan="1" colspan="1" style="text-align:left;vertical-align:top;">There were no radiological changes on chest X-ray, negative SASR-CoV-2 RT-PCR from nasopharyngeal swab. However, the level of IL-6 and alanine aminotransferase activity were increased. The patient reported improving tolerance for physical activity, but he was unable to perform his previous activities with the same strength, e.g. singing</td></tr><tr><td headers="hd_h_niceng188er3.tab1_1_1_1_1" rowspan="1" colspan="1" style="text-align:left;vertical-align:top;">Valiente-De Santis 2020</td><td headers="hd_h_niceng188er3.tab1_1_1_1_2" rowspan="1" colspan="1" style="text-align:left;vertical-align:top;">Spain, Prospective cohort, 14 March to 15 April</td><td headers="hd_h_niceng188er3.tab1_1_1_1_3" rowspan="1" colspan="1" style="text-align:left;vertical-align:top;">
|
|
<p>Patients with previous acute SARS-CoV-2 infection contacted by telephone (n=108)</p>
|
|
<p>No control group</p>
|
|
</td><td headers="hd_h_niceng188er3.tab1_1_1_1_4" rowspan="1" colspan="1" style="text-align:left;vertical-align:top;">
|
|
<p>Blood test</p>
|
|
<p>Chest radiograph</p>
|
|
<p>Chest CT</p>
|
|
<p>Spirometry</p>
|
|
<p>Serological test</p>
|
|
</td><td headers="hd_h_niceng188er3.tab1_1_1_1_5" rowspan="1" colspan="1" style="text-align:left;vertical-align:top;">12 weeks after acute phase</td><td headers="hd_h_niceng188er3.tab1_1_1_1_6" rowspan="1" colspan="1" style="text-align:left;vertical-align:top;">The persistence of symptoms in patents with COVID is usually 12 weeks after the 27 acute episode, especially in patients <65 years and health-care workers.</td></tr><tr><td headers="hd_h_niceng188er3.tab1_1_1_1_1" rowspan="1" colspan="1" style="text-align:left;vertical-align:top;">
|
|
<a class="bibr" href="#niceng188er3.app5.ref18" rid="niceng188er3.app5.ref18">Zhao 2020</a>
|
|
</td><td headers="hd_h_niceng188er3.tab1_1_1_1_2" rowspan="1" colspan="1" style="text-align:left;vertical-align:top;">China, Cohort (retrospective), Jan 20, 2020 to Feb 24, 2020</td><td headers="hd_h_niceng188er3.tab1_1_1_1_3" rowspan="1" colspan="1" style="text-align:left;vertical-align:top;">
|
|
<p>Patients previously hospitalised COVID-19 survivors (n=55)</p>
|
|
<p>No control group</p>
|
|
</td><td headers="hd_h_niceng188er3.tab1_1_1_1_4" rowspan="1" colspan="1" style="text-align:left;vertical-align:top;">
|
|
<p>Chest CT scan</p>
|
|
<p>Pulmonary function test</p>
|
|
<p>SARS-COV-2 IgG test</p>
|
|
</td><td headers="hd_h_niceng188er3.tab1_1_1_1_5" rowspan="1" colspan="1" style="text-align:left;vertical-align:top;">Up to 3 months</td><td headers="hd_h_niceng188er3.tab1_1_1_1_6" rowspan="1" colspan="1" style="text-align:left;vertical-align:top;">Radiological and physiological abnormalities were still found in a considerable proportion of COVID-19 survivors without critical cases 3 months after discharge. Higher level of D-dimer on admission could effectively predict impaired carbon monoxide diffusion capacity after 3 months discharge.</td></tr><tr><td headers="hd_h_niceng188er3.tab1_1_1_1_1" rowspan="1" colspan="1" style="text-align:left;vertical-align:top;">
|
|
<a class="bibr" href="#niceng188er3.app5.ref6" rid="niceng188er3.app5.ref6">Eiros 2020</a>
|
|
</td><td headers="hd_h_niceng188er3.tab1_1_1_1_2" rowspan="1" colspan="1" style="text-align:left;vertical-align:top;">Spain, Cross sectional observational cohort, 25 May 2020 to 12 June 2020</td><td headers="hd_h_niceng188er3.tab1_1_1_1_3" rowspan="1" colspan="1" style="text-align:left;vertical-align:top;">Health-care workers with confirmed past SARS-CoV-2 infection (103 diagnosed by RT-PCR between March 13 and April 25 and 36 by serology April 10 and May 22) (n=139)</td><td headers="hd_h_niceng188er3.tab1_1_1_1_4" rowspan="1" colspan="1" style="text-align:left;vertical-align:top;">
|
|
<p>Complete medical history</p>
|
|
<p>Physical examination</p>
|
|
<p>Questionnaire</p>
|
|
<p>ECG</p>
|
|
<p>Blood investigations</p>
|
|
<p>CMR</p>
|
|
</td><td headers="hd_h_niceng188er3.tab1_1_1_1_5" rowspan="1" colspan="1" style="text-align:left;vertical-align:top;">Approximately 10 weeks after infection onset</td><td headers="hd_h_niceng188er3.tab1_1_1_1_6" rowspan="1" colspan="1" style="text-align:left;vertical-align:top;">Pericarditis and myocarditis with clinical stability are frequent long after SARS-CoV-2 infection, even in presently asymptomatic subjects.</td></tr><tr><td headers="hd_h_niceng188er3.tab1_1_1_1_1" rowspan="1" colspan="1" style="text-align:left;vertical-align:top;">
|
|
<a class="bibr" href="#niceng188er3.app5.ref12" rid="niceng188er3.app5.ref12">Mazza 2020</a>
|
|
</td><td headers="hd_h_niceng188er3.tab1_1_1_1_2" rowspan="1" colspan="1" style="text-align:left;vertical-align:top;">
|
|
<p>Italy, Cross sectional,</p>
|
|
<p>April 6 to June 9, 2020</p>
|
|
</td><td headers="hd_h_niceng188er3.tab1_1_1_1_3" rowspan="1" colspan="1" style="text-align:left;vertical-align:top;">Patients surviving COVID-19 who had previously been hospitalised (n=402)</td><td headers="hd_h_niceng188er3.tab1_1_1_1_4" rowspan="1" colspan="1" style="text-align:left;vertical-align:top;">
|
|
<p>Psychiatric assessments</p>
|
|
<p>Inflammatory biomarkers</p>
|
|
</td><td headers="hd_h_niceng188er3.tab1_1_1_1_5" rowspan="1" colspan="1" style="text-align:left;vertical-align:top;">4 weeks</td><td headers="hd_h_niceng188er3.tab1_1_1_1_6" rowspan="1" colspan="1" style="text-align:left;vertical-align:top;">
|
|
<p>COVID-19 survivors presented a high prevalence of emergent psychiatric sequelae, with 55% of the sample presenting a pathological score for at least one disorder.</p>
|
|
<p>Higher than average incidence of PTSD, major depression, and anxiety, all high-burden non-communicable conditions associated with years of life lived with disability, is expected in survivors.</p>
|
|
</td></tr><tr><td headers="hd_h_niceng188er3.tab1_1_1_1_1" rowspan="1" colspan="1" style="text-align:left;vertical-align:top;">
|
|
<a class="bibr" href="#niceng188er3.app5.ref8" rid="niceng188er3.app5.ref8">Greenhalgh 2020a</a>
|
|
</td><td headers="hd_h_niceng188er3.tab1_1_1_1_2" rowspan="1" colspan="1" style="text-align:left;vertical-align:top;">
|
|
<p>International/primary care, Narrative review, and expert opinion,</p>
|
|
<p>11/8/20</p>
|
|
</td><td headers="hd_h_niceng188er3.tab1_1_1_1_3" rowspan="1" colspan="1" style="text-align:left;vertical-align:top;">Expert opinion for management of people who have a delayed recovery from an episode of covid-19 that was managed in the community or in a standard hospital ward.</td><td headers="hd_h_niceng188er3.tab1_1_1_1_4" rowspan="1" colspan="1" style="text-align:left;vertical-align:top;">
|
|
<p>Medical and self-management</p>
|
|
<p>Blood investigations</p>
|
|
<p>For patients who have had a significant respiratory illness: community follow-up with a chest x ray at 12 weeks.</p>
|
|
<p>For those with evidence of lung damage (such as persistent abnormal chest x ray and oximeter readings), referral to a respiratory service is recommended</p>
|
|
</td><td headers="hd_h_niceng188er3.tab1_1_1_1_5" rowspan="1" colspan="1" style="text-align:left;vertical-align:top;">Post-acute COVID-19 defined as extending beyond three weeks from the onset of first symptoms and chronic COVID-19 as extending beyond 12 weeks.</td><td headers="hd_h_niceng188er3.tab1_1_1_1_6" rowspan="1" colspan="1" style="text-align:left;vertical-align:top;">Recommended clinical assessment should include:
|
|
<ul><li class="half_rhythm"><div>Full history from date of fist symptoms</div></li><li class="half_rhythm"><div>Nature and severity of current symptoms</div></li><li class="half_rhythm"><div>Examination</div></li></ul>
|
|
Recommended investigations should include:
|
|
<ul><li class="half_rhythm"><div>Blood tests for specific clinical indications</div></li><li class="half_rhythm"><div>Anaemia should be excluded for the breathless patient</div></li><li class="half_rhythm"><div>Follow up CXR at 12 weeks for patients who were not admitted to ICU but had significant respiratory illness</div></li></ul></td></tr></tbody></table></div></div></article><article data-type="table-wrap" id="figobniceng188er3app2tab1"><div id="niceng188er3.app2.tab1" class="table"><p class="large-table-link" style="display:none"><span class="right"><a href="/books/NBK567263/table/niceng188er3.app2.tab1/?report=objectonly" target="object">View in own window</a></span></p><div class="large_tbl" id="__niceng188er3.app2.tab1_lrgtbl__"><table><thead><tr><th id="hd_h_niceng188er3.app2.tab1_1_1_1_1" rowspan="1" colspan="1" style="text-align:left;vertical-align:top;">Criteria</th><th id="hd_h_niceng188er3.app2.tab1_1_1_1_2" rowspan="1" colspan="1" style="text-align:left;vertical-align:top;">Notes</th></tr></thead><tbody><tr><td headers="hd_h_niceng188er3.app2.tab1_1_1_1_1" rowspan="1" colspan="1" style="text-align:left;vertical-align:top;">Population</td><td headers="hd_h_niceng188er3.app2.tab1_1_1_1_2" rowspan="1" colspan="1" style="text-align:left;vertical-align:top;">Adults and children who are experiencing new or ongoing symptoms or clusters of symptoms (physical and mental health):
|
|
<ul><li class="half_rhythm"><div>4 to 12 weeks from onset of acute COVID-19</div></li><li class="half_rhythm"><div>12 weeks from onset of acute COVID-19</div></li></ul></td></tr><tr><td headers="hd_h_niceng188er3.app2.tab1_1_1_1_1" rowspan="1" colspan="1" style="text-align:left;vertical-align:top;">Diagnostics tests or assessments</td><td headers="hd_h_niceng188er3.app2.tab1_1_1_1_2" rowspan="1" colspan="1" style="text-align:left;vertical-align:top;">Diagnostic tests or assessments appropriate for the presenting symptoms and the care setting that can be used to:
|
|
<ul><li class="half_rhythm"><div>Rule out or confirm other diagnoses</div></li><li class="half_rhythm"><div>Understand end organ damage effects</div></li></ul></td></tr><tr><td headers="hd_h_niceng188er3.app2.tab1_1_1_1_1" rowspan="1" colspan="1" style="text-align:left;vertical-align:top;">Comparators</td><td headers="hd_h_niceng188er3.app2.tab1_1_1_1_2" rowspan="1" colspan="1" style="text-align:left;vertical-align:top;">Any or no comparator</td></tr><tr><td headers="hd_h_niceng188er3.app2.tab1_1_1_1_1" rowspan="1" colspan="1" style="text-align:left;vertical-align:top;">Outcomes</td><td headers="hd_h_niceng188er3.app2.tab1_1_1_1_2" rowspan="1" colspan="1" style="text-align:left;vertical-align:top;">
|
|
<ul><li class="half_rhythm"><div>Post COVID-19 syndrome (as defined by the study)</div></li><li class="half_rhythm"><div>Other diagnoses</div></li><li class="half_rhythm"><div>Dual diagnoses and other multimorbidities (e.g. post-COVID-19 syndrome plus another condition)</div></li></ul>
|
|
</td></tr><tr><td headers="hd_h_niceng188er3.app2.tab1_1_1_1_1" rowspan="1" colspan="1" style="text-align:left;vertical-align:top;">Settings</td><td headers="hd_h_niceng188er3.app2.tab1_1_1_1_2" rowspan="1" colspan="1" style="text-align:left;vertical-align:top;">Any</td></tr><tr><td headers="hd_h_niceng188er3.app2.tab1_1_1_1_1" rowspan="1" colspan="1" style="text-align:left;vertical-align:top;">Subgroups</td><td headers="hd_h_niceng188er3.app2.tab1_1_1_1_2" rowspan="1" colspan="1" style="text-align:left;vertical-align:top;">
|
|
<ul><li class="half_rhythm"><div>Groups as defined in the EIA for example, age, sex, ethnicity</div></li><li class="half_rhythm"><div>Diagnosis of COVID-19 (e.g. confirmed or high clinical suspicion)</div></li><li class="half_rhythm"><div>Duration of symptoms</div></li><li class="half_rhythm"><div>Care setting</div></li></ul>
|
|
</td></tr><tr><td headers="hd_h_niceng188er3.app2.tab1_1_1_1_1" rowspan="1" colspan="1" style="text-align:left;vertical-align:top;">Study types</td><td headers="hd_h_niceng188er3.app2.tab1_1_1_1_2" rowspan="1" colspan="1" style="text-align:left;vertical-align:top;">
|
|
<p>Any</p>
|
|
<p>The following study design types for this question are preferred. Where these studies are not identified, other study designs will be considered.
|
|
<ul><li class="half_rhythm"><div>Cohort studies</div></li><li class="half_rhythm"><div>Case series</div></li><li class="half_rhythm"><div>Cross sectional studies</div></li></ul></p>
|
|
</td></tr><tr><td headers="hd_h_niceng188er3.app2.tab1_1_1_1_1" rowspan="1" colspan="1" style="text-align:left;vertical-align:top;">Countries</td><td headers="hd_h_niceng188er3.app2.tab1_1_1_1_2" rowspan="1" colspan="1" style="text-align:left;vertical-align:top;">Any</td></tr><tr><td headers="hd_h_niceng188er3.app2.tab1_1_1_1_1" rowspan="1" colspan="1" style="text-align:left;vertical-align:top;">Timepoints</td><td headers="hd_h_niceng188er3.app2.tab1_1_1_1_2" rowspan="1" colspan="1" style="text-align:left;vertical-align:top;">Any</td></tr><tr><td headers="hd_h_niceng188er3.app2.tab1_1_1_1_1" rowspan="1" colspan="1" style="text-align:left;vertical-align:top;">Other exclusions</td><td headers="hd_h_niceng188er3.app2.tab1_1_1_1_2" rowspan="1" colspan="1" style="text-align:left;vertical-align:top;">None</td></tr></tbody></table></div></div></article><article data-type="fig" id="figobniceng188er3app4fig1"><div id="niceng188er3.app4.fig1" class="figure"><div class="graphic"><a href="/core/lw/2.0/html/tileshop_pmc/tileshop_pmc_inline.html?title=Image%20niceng188er3app4f1&p=BOOKS&id=567263_niceng188er3app4f1.jpg" target="tileshopwindow" class="inline_block pmc_inline_block ts_canvas img_link" title="Click on image to zoom"><div class="ts_bar small" title="Click on image to zoom"></div><img data-src="/books/NBK567263/bin/niceng188er3app4f1.jpg" alt="Image niceng188er3app4f1" class="tileshop" title="Click on image to zoom" /></a></div></div></article></div><div id="jr-scripts"><script src="/corehtml/pmc/jatsreader/ptpmc_3.22/js/libs.min.js"> </script><script src="/corehtml/pmc/jatsreader/ptpmc_3.22/js/jr.min.js"> </script></div></div>
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