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Editorials
Liver fibrosis: More than meets the eye
Amedeo Lonardo
Department of Internal Medicine – AOU Modena (-2023), Italy
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    "textoCompleto" => "<span class="elsevierStyleSections"><span id="sec0001" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleLabel">1</span><span class="elsevierStyleSectionTitle" id="cesectitle0002">Steatotic liver disease and accelerated micro-macro-angiopathy</span><p id="para0001" class="elsevierStylePara elsevierViewall">Steatotic liver disease &#40;SLD&#41;&#44; owing to metabolic etiology&#44; is variously defined&#58; nonalcoholic fatty liver disease&#47;nonalcoholic steatohepatitis &#40;NAFLD&#47;NASH&#41; and metabolic dysfunction-associated fatty liver disease&#47;metabolic dysfunction-associated SLD &#40;MAFLD&#47;MASLD&#41; &#91;<a class="elsevierStyleCrossRef" href="#bib0001">1</a>&#44;<a class="elsevierStyleCrossRef" href="#bib0002">2</a>&#93;&#46; NAFLD&#47;NASH and MAFLD&#47;MASLD are strongly associated with accelerated macrovascular disease&#44; whose risk parallels the severity of the stage of liver fibrosis &#91;<a class="elsevierStyleCrossRef" href="#bib0003">3</a>&#44;<a class="elsevierStyleCrossRef" href="#bib0004">4</a>&#93;&#46; This suggests that appropriate management of SLD owing to metabolic etiology might also prevent such cardiovascular conditions effectively <a class="elsevierStyleCrossRef" href="#bib0005">&#91;5&#93;</a>&#46;</p><p id="para0002" class="elsevierStylePara elsevierViewall">The retinal neurovascular unit is typically dysfunctional in diabetes and&#44; among patients living with diabetes&#44; clinical manifestations&#44; and epidemiological features of microvascular disease &#8211; as opposed to macrovascular damage &#8211; vary &#91;<a class="elsevierStyleCrossRef" href="#bib0006">6</a>&#44;<a class="elsevierStyleCrossRef" href="#bib0007">7</a>&#93;&#46; Therefore&#44; it is important to ascertain whether - among individuals with diabetes &#8211; SLD&#44; owing to metabolic etiology and its fibrosis progression&#44; are also a risk factor for microangiopathy&#44; including chronic kidney disease &#40;CKD&#41;&#44; retinopathy and neuropathy&#46;</p></span><span id="sec0002" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleLabel">2</span><span class="elsevierStyleSectionTitle" id="cesectitle0003">The paper by Dr&#46; LI&#44; and colleagues</span><p id="para0003" class="elsevierStylePara elsevierViewall">In this issue of <span class="elsevierStyleItalic">Annals of Hepatology</span>&#44; Doctor Li&#44; and colleagues report on their cross-sectional research conducted among 5413 participants from the NHANES 2005&#8211;2008 database <a class="elsevierStyleCrossRef" href="#bib0008">&#91;8&#93;</a>&#46; These investigators found retinopathy&#44; categorized into four levels of severity based on retinal imaging&#44; as an independent predictor of significant hepatic fibrosis&#44; assessed with Fibrosis-4 &#40;FIB-4&#41; among individuals with type 2 diabetes <a class="elsevierStyleCrossRef" href="#bib0008">&#91;8&#93;</a>&#46;</p><p id="para0004" class="elsevierStylePara elsevierViewall">The findings of this study confirm another study recently published in Annals of Hepatology <a class="elsevierStyleCrossRef" href="#bib0002">&#91;2&#93;</a>&#46; In this second cross-sectional study&#44; Trivedi <span class="elsevierStyleItalic">et al</span>&#46;&#44; globally evaluating 2389 participants from primary care practice&#44; found that the complications of type 2 diabetes &#40;T2D&#41; &#40;namely diabetic nephropathy&#44; retinopathy&#44; or neuropathy&#41; were associated&#44; irrespective of hemoglobin A1c levels&#44; with the stage of liver fibrosis&#44; assessed with FIB-4 evaluated as a continuous and categorical measure using linear and ordinal logistic regression <a class="elsevierStyleCrossRef" href="#bib0009">&#91;9&#93;</a>&#46;</p><p id="para0005" class="elsevierStylePara elsevierViewall">Previous studies have found that liver fibrosis was associated with microangiopathic complications among patients with diabetes&#46; While evidence regarding CKD has extensively been reviewed elsewhere <a class="elsevierStyleCrossRef" href="#bib0010">&#91;10&#93;</a>&#44; <a class="elsevierStyleCrossRef" href="#tbl0001">Table 1</a> specifically focuses on retinopathy &#40;Research strategy&#58; PubMed accessed on Jan 23&#44; 2024&#44; utilizing the following keywords&#58; &#40;liver fibrosis&#91;Title&#47;Abstract&#93;&#41; AND &#40;retinopathy&#91;Title&#47;Abstract&#93;&#41;&#46;</p><elsevierMultimedia ident="tbl0001"></elsevierMultimedia></span><span id="sec0003" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleLabel">3</span><span class="elsevierStyleSectionTitle" id="cesectitle0004">What do these studies&#44; collectively&#44; teach us&#63;</span><p id="para0006" class="elsevierStylePara elsevierViewall">First&#44; the association linking more advanced stages of liver fibrosis with the risk of DR occurs irrespective of the non-invasive technique used to assess steatosis&#44; namely either liver stiffness measurement or FIB-4&#46; In this connection&#44; it should be emphasized that liver stiffness measurement&#44; in the context of individuals with chronic liver disease&#44; has been found to be an easy-to-use&#44; non-invasive continuous scale tool to rule out clinically significant portal hypertension in &#62;95 &#37; of patients <a class="elsevierStyleCrossRef" href="#bib0015">&#91;15&#93;</a>&#46; To this end&#44; also a variety of biomarkers&#44; including aspartate aminotransferase &#40;AST&#41; to alanine aminotransferase &#40;ALT&#41; ratio &#40;ARR&#41;&#44; AST to Platelet Ratio Index &#40;APRI&#41;&#44; FiB-4&#44; Forns index&#44; NAFLD fibrosis score &#40;NFS&#41;&#44; BARD &#40;body mass index&#44; AAR&#44; Diabetes&#41; score&#44; and Hepamet fibrosis score &#40;HFS&#41;&#44; are accurate in ruling out advanced liver fibrosis and positively correlate with scores of cardiovascular risk in patients with chronic liver disease <a class="elsevierStyleCrossRef" href="#bib0016">&#91;16&#93;</a>&#46; Of concern&#44; age and diabetes negatively impact the accuracy of non-invasive tests for liver fibrosis &#91;<a class="elsevierStyleCrossRef" href="#bib0017">17</a>&#44;<a class="elsevierStyleCrossRef" href="#bib0018">18</a>&#93;&#46;</p></span><span id="sec0004" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleLabel">4</span><span class="elsevierStyleSectionTitle" id="cesectitle0005">Role of the liver</span><p id="para0007" class="elsevierStylePara elsevierViewall">Second&#44; these associations linking liver fibrosis and DR occur irrespective of the duration of diabetes and the degree of metabolic compensation of diabetes&#44; assessed with HbA1c <a class="elsevierStyleCrossRef" href="#bib0008">&#91;8&#93;</a>&#44; supporting the notion that it is probably the liver &#40;rather than diabetes&#41; that plays a major pathogenic role in the &#8220;hepato-retinal&#8221; axis <a class="elsevierStyleCrossRef" href="#bib0019">&#91;19&#93;</a>&#46; The pathomechanisms underlying this &#8220;hepato-retinal&#8221; axis&#44; although incompletely understood&#44; are increasingly being elucidated <a class="elsevierStyleCrossRef" href="#bib0019">&#91;19&#93;</a>&#46; To this end&#44; lessons from human disease models&#44; such as the so-called ciliopathies <a class="elsevierStyleCrossRef" href="#bib0020">&#91;20&#93;</a> and the Senior-L&#248;ken Syndrome <a class="elsevierStyleCrossRef" href="#bib0021">&#91;21&#93;</a> may shed light on the role of genetics in facilitating&#44; among predisposed individuals with diabetes&#44; the development of eye-kidney-liver complications&#46; In this regard&#44; Olbrich and Colleagues have identified mutations in a novel gene&#44; <span class="elsevierStyleItalic">NPHP3</span>&#44; to cause nephronophthisis&#44; tapeto-retinal degeneration and hepatic fibrosis among teenagers <a class="elsevierStyleCrossRef" href="#bib0022">&#91;22&#93;</a>&#46; However&#44; the relevance of such polymorphisms in the <span class="elsevierStyleItalic">NPHP3</span> gene to the development of DR in adults remains to be ascertained&#46;</p></span><span id="sec0005" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleLabel">5</span><span class="elsevierStyleSectionTitle" id="cesectitle0006">Role of hepatic fibrosis</span><p id="para0008" class="elsevierStylePara elsevierViewall">Third&#44; liver fibrosis&#44; teleologically aimed at limiting tissue integrity by circumscribing offending agents&#44; describes an excess accumulation of extracellular matrix components <a class="elsevierStyleCrossRef" href="#bib0023">&#91;23&#93;</a>&#46; Liver fibrosis results from persistent liver injury owing to variable insults&#44; including i&#41; chronic viral hepatitis&#59; ii&#41; toxic injury&#44; for example&#44; owing to chronic excess alcohol consumption&#59; iii&#41; injury associated with metabolic dysfunction&#44; such as typically observed in the NAFLD&#47;NASH arena <a class="elsevierStyleCrossRef" href="#bib0024">&#91;24&#93;</a>&#46; Whenever liver fibrosis&#44; from a mechanism of organ defense&#44; turns dysfunctional owing to prolonged inflammation and excessive fibrotic response&#44; liver regeneration and function will be compromised&#44; culminating in portal hypertension&#44; risk of complicated cirrhosis and development of hepatocellular carcinoma&#44; which&#44; globally&#44; result in increased clinical burden and healthcare expenditures &#91;<a class="elsevierStyleCrossRef" href="#bib0023">23</a>&#44;<a class="elsevierStyleCrossRef" href="#bib0025">25</a>&#93;&#46; The grounds underlying the association of liver fibrosis and DR are incompletely defined&#46; On the one hand&#44; both liver fibrosis and DR may result from a &#8220;common soil&#8221; of insulin resistance&#44; metabolic dysfunction&#44; increased oxidative stress&#44; and sterile metabolic inflammation &#40;i&#46;e&#46;&#44; metaflammation&#41;&#44; eventually conducive to repeated bouts of cell stress&#44; death&#44; and fibrosing wound response in the liver&#44; the kidneys &#91;<a class="elsevierStyleCrossRef" href="#bib0026">26</a>&#44;<a class="elsevierStyleCrossRef" href="#bib0027">27</a>&#93;&#44; and&#44; by inference&#44; the retinal tissue&#46; On the other hand&#44; the steatotic and chronically inflamed liver&#44; particularly in NASH&#44; and MASH could serve as an amplifier and a perpetuator of systemic insulin resistance and subclinical low-grade chronic inflammatory state <a class="elsevierStyleCrossRef" href="#bib0028">&#91;28&#93;</a>&#44; eventually conducive to damage of the microvasculature of retina in a proportion of individuals&#46;</p></span><span id="sec0006" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleLabel">6</span><span class="elsevierStyleSectionTitle" id="cesectitle0007">How can these epidemiological associations be used in clinical arena&#63;</span><p id="para0009" class="elsevierStylePara elsevierViewall">Probably&#44; one of the most difficult challenges in clinical practice is to push clinicians from different areas of expertise to work together in the setting of multi-disciplinary teams&#46; However&#44; such multi-expert teams are exactly what we would need to utilize the mutually interactive information deriving from the retina and from the liver&#46; For example&#44; the hepatologist should be aware of the risk of DR and refer his&#47;her patients with advanced dysmetabolic SLD to the ophthalmologist&#46; Similarly&#44; the opthalmologist&#47;diabetologist who happens to observe a case of DR should promptly refer the patient for hepatological assessment&#46;</p></span><span id="sec0007" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleLabel">7</span><span class="elsevierStyleSectionTitle" id="cesectitle0008">Conclusion and research agenda</span><p id="para0010" class="elsevierStylePara elsevierViewall">Individuals presenting with NAFLD&#47;NASH&#44; MAFLD&#47;MASLD and concurrent DR are likely to harbor CKD&#44; diabetic neuropathy&#44; and enhanced cardiovascular risk in the context of more advanced liver fibrosis&#46; Prompt recognition of this syndromic picture by expert and dedicated clinicians will trigger comprehensive multi-organ assessment&#44; such as appropriate for a potentially severe systemic disorder&#46;</p><p id="para0011" class="elsevierStylePara elsevierViewall">In this context&#44; strategies aimed at targeting triage for advanced liver fibrosis among those at-risk groups of individuals undoubtedly play a major role <a class="elsevierStyleCrossRef" href="#bib0029">&#91;29&#93;</a>&#46; From the therapeutic point of view&#44; these patients exhibiting advanced liver fibrosis in the setting of diabetes may benefit from a variety of marketed drugs and others in the pipeline&#44; including pioglitazone&#44; glucagon-like peptide 1 receptor antagonists&#44; sodium&#8211;glucose transporter 2 inhibitors&#44; Fibroblast Growth Factor analogues&#44; Farnesoid X receptor agonists&#44; peroxisomeproliferator&#8211;activated receptor agonists&#44; and the liver-directed&#44; &#946;-selective THR agonist resmetirom &#91;<a class="elsevierStyleCrossRef" href="#bib0030">30</a>&#44;<a class="elsevierStyleCrossRef" href="#bib0031">31</a>&#93;&#46;</p><p id="para0012" class="elsevierStylePara elsevierViewall">Additional studies should explore the role of serum levels of mac-2 binding protein and galectin 1 &#91;<a class="elsevierStyleCrossRef" href="#bib0032">32</a>&#44;<a class="elsevierStyleCrossRef" href="#bib0033">33</a>&#93; as biomarkers of systemic fibrosing disease potentially involving eyes&#44; the kidneys&#44; and the liver&#44; as well as of galectin 1 as a target of selective anti-fibrotic pharmacological intervention <a class="elsevierStyleCrossRef" href="#bib0033">&#91;33&#93;</a>&#46;</p></span></span>"
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          "leyenda" => "<p id="spara002" class="elsevierStyleSimplePara elsevierViewall">aOR&#44; adjusted odds ratio&#59; CAP&#44; controlled attenuation parameter&#59; CKD&#44; chronic kidney disease&#59; DKD&#44; diabetic kidney disease&#59; DR&#44; diabetic retinopathy&#59; HbA1c&#44; glycated hemoglobin&#59; LSM&#44; liver stiffness measurement&#59; NFS&#44; NAFLD fibrosis score&#59; T1D&#44; type 1 diabetes&#59; T2D&#44; type 2 diabetes&#46;</p>"
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                  \t\t\t\t\ttable-head\n
                  \t\t\t\t  " align="" valign="top" scope="col" style="border-bottom: 2px solid black">Author&#44; year &#91;Ref&#93;&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t\t\t</th><a name="en0002"></a><th class="td" title="\n
                  \t\t\t\t\ttable-head\n
                  \t\t\t\t  " align="" valign="top" scope="col" style="border-bottom: 2px solid black">Method&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t\t\t</th><a name="en0003"></a><th class="td" title="\n
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                  \t\t\t\t  " align="" valign="top" scope="col" style="border-bottom: 2px solid black">Finding&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t\t\t</th><a name="en0004"></a><th class="td" title="\n
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                  \t\t\t\t  " align="" valign="top" scope="col" style="border-bottom: 2px solid black">Conclusion&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t\t\t</th></tr></thead><tbody title="tbody"><tr title="table-row"><a name="en0005"></a><td class="td" title="\n
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                  \t\t\t\t  " align="" valign="top">Lombardi&#44; 2020<a class="elsevierStyleCrossRef" href="#bib0011">&#91;11&#93;</a>&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><a name="en0006"></a><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="" valign="top">Liver fibrosis was evaluated with Fibro Scan&#174; among 394 Italian out-patients with T2D&#46;&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><a name="en0007"></a><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="" valign="top">LSM &#8805; 7&#46;0&#47;6&#46;2 kPa was independently associated with microvascular complications &#40;aOR 4&#46;2&#44; 95 &#37;CI 1&#46;5&#8208;11&#46;4&#59; <span class="elsevierStyleItalic">P</span> &#61; 0&#46;005&#41;&#44; mainly CKD &#40;adjusted OR 3&#46;6&#44; 95 &#37;CI 1&#46;3&#8208;10&#46;1&#59; <span class="elsevierStyleItalic">P</span> &#61; 0&#46;01&#41; and retinopathy &#40;adjusted OR 3&#46;7&#44; CI 95 &#37; 1&#46;2&#8208;11&#46;9&#59; <span class="elsevierStyleItalic">P</span> &#61; 0&#46;02&#41; irrespective of diabetes duration and HbA1c&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><a name="en0008"></a><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="" valign="top">Significant fibrosis&#44; detected by FibroScan&#174;&#44; was independently associated with microvascular complications among T2D patients&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td></tr><tr title="table-row"><a name="en0009"></a><td class="td" title="\n
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                  \t\t\t\t  " align="" valign="top">Mikolasevic&#44; 2021 <a class="elsevierStyleCrossRef" href="#bib0012">&#91;12&#93;</a>&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><a name="en0010"></a><td class="td" title="\n
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                  \t\t\t\t  " align="" valign="top">442 T2DM out-patients underwent VCTE and extensive assessment of chronic vascular complications of diabetes&#46;&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><a name="en0011"></a><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="" valign="top">Significant liver fibrosis &#40;&#40;LSM &#8805; 7&#46;0&#47;6&#46;2 kPa&#41;&#44; &#8211; but not steatosis defined as CAP &#8805; 238 dB&#47;m &#8211; was associated with an increased risk of&#44; peripheral polyneuropathy &#40;aOR 4&#46;55&#44; 95 &#37;CI 1&#46;25&#8211;16&#46;6&#41;&#44; CKD &#40;aOR 4&#46;54&#44; 95 &#37;CI 1&#46;24&#8211;16&#46;6&#41; or retinopathy &#40;aOR 1&#46;81&#44; 95 &#37;CI 1&#46;62&#8211;1&#46;97&#41;&#44; independently of cardiometabolic confounding factors macro-&#47;microvascular complications of diabetes&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><a name="en0012"></a><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="" valign="top">Significant liver fibrosis is independently associated with microvascular complications among individuals living with T2D&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td></tr><tr title="table-row"><a name="en0013"></a><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="" valign="top">Zhang&#44; 2022 <a class="elsevierStyleCrossRef" href="#bib0013">&#91;13&#93;</a>&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><a name="en0014"></a><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="" valign="top">Meta-analysis of 18 studies involving 12&#44;757 patients&#46;&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><a name="en0015"></a><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="" valign="top">Liver fibrosis&#44; &#40;OR &#61; 1&#46;69&#44; 95 &#37;CI 1&#46;30&#8211;2&#46;20&#59; <span class="elsevierStyleItalic">p</span> &#60; 0&#46;0001&#59; but not NAFLD &#40;OR &#61; 1&#46;15&#44; 95 &#37;CI 0&#46;75&#8211;1&#46;76&#59; <span class="elsevierStyleItalic">p</span> &#61; 0&#46;51&#41; NAFLD was positively correlated with DR&#46; NAFLD was associated with DR in patients with T1D &#40;OR &#61; 2&#46;96&#44; 95 &#37;CI 1&#46;48&#8211;5&#46;94&#59; <span class="elsevierStyleItalic">p</span> &#61; 0&#46;002&#41;&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><a name="en0016"></a><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="" valign="top">There is a significant correlation between liver fibrosis and DR&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td></tr><tr title="table-row"><a name="en0017"></a><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="" valign="top">Wen&#44; 2022 <a class="elsevierStyleCrossRef" href="#bib0014">&#91;14&#93;</a>&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><a name="en0018"></a><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="" valign="top">Among 1982 T2D patients&#44; the risk for advanced liver fibrosis was categorized as &#8220;low&#44; &#8220;indeterminate&#44; &#8220;and &#8220;high&#8221; with NFS&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><a name="en0019"></a><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="" valign="top">The presence of DR and DKD was inversely associated with NAFLD after adjusting for covariates&#46; The presence of DR and DKD was higher in the &#8220;indeterminate risk&#8221; and &#8220;high risk&#8221; groups than in the &#8220;low risk&#8221; group after adjusting for the same covariates&#46; Only the presence of DKD significantly increased with high NFS&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><a name="en0020"></a><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="" valign="top">The presence of DR and DKD was inversely associated with NAFLD among hospitalized T2D patients&#46; DKD was closely associated with high NFS&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td></tr></tbody></table>
                  """
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          "en" => "<p id="spara001" class="elsevierStyleSimplePara elsevierViewall">Recent studies disclosing an association between liver fibrosis and retinopathy <a class="elsevierStyleCrossRefs" href="#bib0011">&#91;11&#8211;14&#93;</a>&#46;</p>"
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Article information
ISSN: 16652681
Original language: English
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es en pt

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Você é um profissional de saúde habilitado a prescrever ou dispensar medicamentos