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Retinal vein occlusion in solid organ transplant recipients. Study of 4 cases and literature review
Obstrucción venosa retiniana en receptores de trasplante de órgano sólido. Estudio de 4 casos y revisión de la literatura
A. Cerveróa,
Corresponding author
andreacervero27@gmail.com

Corresponding author.
, P. González Boresb, A. Casadoa, M.D. Ruiz Sanchoa, J.L. Hernández Hernándezb,c, J.J. Napal Lecumberrib
a Servicio de Oftalmología, Hospital Universitario Marqués de Valdecilla-IDIVAL, Santander, Spain
b Departamento de Medicina Interna, Hospital Universitario Marqués de Valdecilla-IDIVAL, Santander, Spain
c Universidad de Cantabria, Santander, Spain
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it facilitates the development of RVO&#44; generally in its central location&#46;<a class="elsevierStyleCrossRef" href="#bib0055"><span class="elsevierStyleSup">1</span></a></p><p id="par0010" class="elsevierStylePara elsevierViewall">Even though isolated cases or small series of transplanted patients who have developed RVO have been reported&#44;<a class="elsevierStyleCrossRefs" href="#bib0070"><span class="elsevierStyleSup">4&#44;5</span></a> none of said publications relates to our country&#46; Accordingly&#44; we consider that sharing our experience in a broad cohort of patients with RVO in a follow-up spanning over 10 years would be of interest&#46; Accordingly&#44; the objective of this paper is to describe the characteristic of patients with solid organ transplant who developed RVO compared to the rest of patients with RVO&#46;</p></span><span id="sec0010" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0030">Patients and methods</span><p id="par0015" class="elsevierStylePara elsevierViewall">In the course of 10 years &#40;between December 2008 and November 2018&#41; all patients diagnosed with RVO at the ophthalmology department on the basis of clinic&#44; funduscopic and angiographic criteria &#40;the <span class="elsevierStyleItalic">Valdecilla</span> cohort&#41; were checked in the internal medicine Dept&#46; of the Marqu&#233;s de Valdecilla hospital in order to diagnose and treat VRF associated to RVO&#46; The treatment of acquired thrombophilia &#40;hyperhomocysteinemia and the antiphospholipid syndrome&#41; was also studied and assessed in all patients with RVO&#44; while the study of genetic thrombophilia was limited to patients under 50 years of age or without VRF&#46;<a class="elsevierStyleCrossRef" href="#bib0065"><span class="elsevierStyleSup">3</span></a> Said hospital is a reference center for a population of 350&#44;000 inhabitants and features a significant transplant program including patients of the Community of Cantabria and neighboring regions&#44; in addition to being certified as a national reference center &#40;CSUR&#41; for renal&#44; lung and pancreatic transplants&#46;<a class="elsevierStyleCrossRef" href="#bib0080"><span class="elsevierStyleSup">6</span></a> Between 2009 and 2018&#44; 1370 solid organ transplants were carried out at the Marqu&#233;s de Valdecilla hospital &#40;468 kidney&#44; 209 heart&#44; 228 liver&#44; 403 long and 62 pancreas&#41;&#46;</p><p id="par0020" class="elsevierStylePara elsevierViewall">The study of patients with RVO was approved by the ethics committee of the hospital and all patients signed the informed consent to be included in the study&#46;</p><p id="par0025" class="elsevierStylePara elsevierViewall">Collected data comprised RVO type &#40;branch or central&#41;&#44; the presence of RVO as first episode or relapse at the time of admission in the study&#44; age&#44; sex&#44; arterial hypertension &#40;defined as 140<span class="elsevierStyleHsp" style=""></span>mm<span class="elsevierStyleHsp" style=""></span>Hg or over and&#47;or 90<span class="elsevierStyleHsp" style=""></span>mm<span class="elsevierStyleHsp" style=""></span>Hg&#44; or receiving hypotensive treatment&#41;&#44; DM &#40;according to the criteria of the <span class="elsevierStyleItalic">American Diabetes Association</span>&#41;&#44; dyslipidemia &#40;total cholesterol<span class="elsevierStyleHsp" style=""></span>&#62;<span class="elsevierStyleHsp" style=""></span>230<span class="elsevierStyleHsp" style=""></span>mg&#47;dl or triglycerides<span class="elsevierStyleHsp" style=""></span>&#62;<span class="elsevierStyleHsp" style=""></span>150<span class="elsevierStyleHsp" style=""></span>mg&#47;dl&#44; in at least 2D terminations after 24<span class="elsevierStyleHsp" style=""></span>h on an empty stomach&#44; or receiving lipid lowering treatment&#41;&#46;</p><p id="par0030" class="elsevierStylePara elsevierViewall">Collected data about the 4 transplanted patients included the transplanted organ data&#44; the disease that gave rise to the transplant&#44; the time elapsed between the transplants and RVO as well as immunosuppressive treatments&#46; In addition&#44; the prescribed ophthalmological treatment was analyzed together with the best corrected visual acuity &#40;BCVA&#41;&#44; intraocular pressure &#40;IOP&#41;&#44; eye fundus&#44; optical coherence tomography and the appearance of complications&#46;</p></span><span id="sec0015" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0035">Results</span><p id="par0035" class="elsevierStylePara elsevierViewall">Overall&#44; the study analyzed 331 patients with RVO in the following types&#58; RVBO in 226 &#40;68&#37;&#41; of cases &#40;220 temporal and 6 nasal&#41;&#44; and CRVO in 105 patients &#40;32&#37;&#41;&#46; In 317 &#40;96&#37;&#41; patients&#44; RVO was the first episode and in 14 &#40;4&#37;&#41; it was a recurrence&#46;</p><p id="par0040" class="elsevierStylePara elsevierViewall">Mean age of transplanted patients was 58 years&#44; one decade below the rest of our <span class="elsevierStyleItalic">Valdecilla</span> cohort &#40;67&#46;8<span class="elsevierStyleHsp" style=""></span>&#177;<span class="elsevierStyleHsp" style=""></span>12&#46;3 years&#41;&#46; The 4 transplanted patients were male&#44; whereas in the cohort 47&#37; were male &#40;156&#47;331 cases&#41;&#46; The prevalence of vascular risk factors in cohort patients was&#58; hypertension <span class="elsevierStyleItalic">n</span><span class="elsevierStyleHsp" style=""></span>&#61;<span class="elsevierStyleHsp" style=""></span>238 &#40;72&#37;&#41;&#59; dyslipidemia <span class="elsevierStyleItalic">n</span><span class="elsevierStyleHsp" style=""></span>&#61;<span class="elsevierStyleHsp" style=""></span>216 &#40;65&#37;&#41; and DM <span class="elsevierStyleItalic">n</span><span class="elsevierStyleHsp" style=""></span>&#61;<span class="elsevierStyleHsp" style=""></span>82 &#40;25&#37;&#41;&#46; Seven patients with RVO were in treatment with corticoids&#44; of which 4 had a transplant&#44; while 3 patients with tacrolimus also had a transplant&#46;</p><p id="par0045" class="elsevierStylePara elsevierViewall"><a class="elsevierStyleCrossRef" href="#tbl0005">Table 1</a> summarizes clinical data&#44; ophthalmological treatment and BCVA of the 4 transplanted patients with RVO&#46;</p><elsevierMultimedia ident="tbl0005"></elsevierMultimedia><p id="par0050" class="elsevierStylePara elsevierViewall">In what concerns the ophthalmological characteristics of RVO cases in patients with transplants&#44; all 4 patients exhibited ischemic RVO with BCVA<span class="elsevierStyleHsp" style=""></span>&#8804;<span class="elsevierStyleHsp" style=""></span>0&#46;1 associating cystic macular edema&#44; with the baseline macular thickness being 728&#44; 808&#44; 1216 and 840<span class="elsevierStyleHsp" style=""></span>&#956;m respectively&#46; Patients received intravitreous antiangiogenic treatment &#40;aflibercept or ranibizumab&#41; and&#47;or intravitreous dexamethasone implant as per protocol&#46; <a class="elsevierStyleCrossRef" href="#fig0005">Figure 1</a> shows the evolution of macular edema and BCVA at baseline and after one year of treatment&#46; The 4 patients exhibited improvement of macular edema and visual acuity one year after RVO&#44; although one &#40;case 3&#41; presented a recurring macular edema during 2 years follow-up that required occasional intravitreal injections&#46; The fourth patient &#40;case 4&#41; required a third kidney transplant immediately after RVO and this limited the intravitreal treatment&#46; However&#44; the macular edema resolved spontaneously&#46; This patient had exhibited an episode of pre-thrombosis in the same eyes 3 years after the second kidney transplant&#44; which evolved positively without requiring treatment&#46;</p><elsevierMultimedia ident="fig0005"></elsevierMultimedia><p id="par0055" class="elsevierStylePara elsevierViewall">Despite the relationship between glaucoma and CRVO&#44; none of the patients exhibited previous glaucoma&#46; During the follow-up&#44; IOP was checked and one patient &#40;case 2&#41; presented with neovascular glaucoma 3 months after the CRVO episode&#44; with regression of iris neo-vascularization and IOP normalization after treatment with retinal panphotocoagulation&#46; One of the patients &#40;case 1&#41; exhibited vitreomacular traction&#46;</p></span><span id="sec0020" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0040">Discussion</span><p id="par0060" class="elsevierStylePara elsevierViewall">It was observed that in the cohort of the present study RVO appeared at earlier ages in transplanted patients than in the rest of patients with RVO&#46; In transplanted patients as well as in non-transplanted patients&#44; RVO was basically related to arteriosclerosis&#44; a consequence of VRF&#46;<a class="elsevierStyleCrossRefs" href="#bib0055"><span class="elsevierStyleSup">1&#8211;3</span></a> In patients with transplants&#44; arteriosclerosis could develop at earlier ages due to the use of corticoids&#44; higher prevalence of DM&#44; comorbidities and immunosuppressant medication&#44; particularly tacrolimus due to its frequent utilization&#46;<a class="elsevierStyleCrossRef" href="#bib0085"><span class="elsevierStyleSup">7</span></a> On the other hand&#44; steroidal treatment could also influence the appearance of glaucoma&#44; acting as a local factor facilitating the development of RVO&#46; Patients with transplants exhibited CRVO in contrast with the rest of patients who exhibited a predominance of RVBO&#44; which usually entails poor prognosis in what concerns loss of vision&#46;<a class="elsevierStyleCrossRef" href="#bib0055"><span class="elsevierStyleSup">1</span></a> In the present study&#44; RVO developed in different types of solid organ transplants&#44; predominantly liver and kidney&#44; and in 3 of these it was diagnosed before 2 years after the transplant&#44; suggesting an early occurrence in these cases&#46;</p><p id="par0065" class="elsevierStylePara elsevierViewall">The literature comprises very few cases of RVO in patients with solid organ transplant&#44; all of which are retrospective studies&#46; In a study with 3656 patients that received a solid organ or bone marrow transplant&#44; 1198 of which were examined by the ophthalmology department&#44; Chung et al&#46;<a class="elsevierStyleCrossRef" href="#bib0070"><span class="elsevierStyleSup">4</span></a> reported 3 cases of RVO&#44; all with central compromise in patients with liver transplant who were receiving corticoids&#44; tacrolimus and mycophenolate&#46; These characteristics are very similar to those reported in the present series&#46; Similarly&#44; Donnadieu et al&#46;<a class="elsevierStyleCrossRef" href="#bib0090"><span class="elsevierStyleSup">8</span></a> described central RVO in a patient who received a liver transplant and was in treatment with tacrolimus&#44; and Malerbi et al&#46;<a class="elsevierStyleCrossRef" href="#bib0095"><span class="elsevierStyleSup">9</span></a> studied 108 patients who underwent solid organ transplant and observed 7 cases of RVO&#44; 2 of them in patients with kidney transplant&#44; 2 with liver transplant and 3 with pancreas-kidney transplants&#46; In addition&#44; Su et al&#46;<a class="elsevierStyleCrossRef" href="#bib0075"><span class="elsevierStyleSup">5</span></a> analyzed 311 heart transplant patients and described 6 cases &#40;1&#46;93&#37;&#41; of RVO &#40;3 with RVBO and 3 with CRVO&#41; and&#44; in a further study with 860 patients who underwent heart&#44; lung and liver transplants&#44; Ng et al&#46;<a class="elsevierStyleCrossRef" href="#bib0100"><span class="elsevierStyleSup">10</span></a> reported one CRVO episode in a patient with heart transplant&#46; However&#44; in the present series none of the 209 heart transplant patients exhibited RVO&#46;</p><p id="par0070" class="elsevierStylePara elsevierViewall">The main strength of the present study is that it includes all patients diagnosed with RVO in a health area during an extended period of time&#46; However&#44; despite being a series that contributes one of the highest number of transplant patients with RVO&#44; the number is still small to draw definitive conclusions&#46; One of the limitations of the study is that the 1370 transplant patients did not undergo an ophthalmological examination&#44; and therefore the incidence of RVO in said group is unknown because it was not possible to determine the number of asymptomatic cases or those that have taken place beyond the coverage area of the hospital&#46; Even so&#44; it can be said that RVO is more prevalent than in the general population due to the fact that 4 patients with transplants exhibited the disorder against only one with the same characteristics in the control population&#46;</p></span><span id="sec0025" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0045">Conclusions</span><p id="par0075" class="elsevierStylePara elsevierViewall">In the present study&#44; RVO in solid organ transplant patients appeared at earlier ages than in the group who did not undergo transplants&#44; and in the present study RVO of patients with solid organ transplants appeared at earlier ages compared to said group&#44; associated to DM and treatment with steroids and immunosuppressants &#40;mainly tacrolimus and mycophenolate&#41;&#46; In addition&#44; RVO compromised the central retinal vein with greater frequency&#44; giving rise to ischemic RVO and cystic macular edema which improved when treated with antiangiogenics and intravitreous dexamethasone implants&#46;</p></span><span id="sec0030" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0050">Conflict of interests</span><p id="par0080" class="elsevierStylePara elsevierViewall">No conflict of interests was declared by the authors&#46;</p></span></span>"
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          "identificador" => "xres1438266"
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          "titulo" => "Introduction"
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          "titulo" => "Patients and methods"
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          "identificador" => "sec0025"
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          "identificador" => "sec0030"
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          "titulo" => "References"
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    "fechaRecibido" => "2019-11-17"
    "fechaAceptado" => "2020-02-11"
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          "clase" => "keyword"
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          "palabras" => array:3 [
            0 => "Retinal vein occlusion"
            1 => "Vascular risk factors"
            2 => "Solid organ transplant"
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        0 => array:4 [
          "clase" => "keyword"
          "titulo" => "Palabras clave"
          "identificador" => "xpalclavsec1312864"
          "palabras" => array:3 [
            0 => "Obstrucci&#243;n venosa retiniana"
            1 => "Factores de riesgo vascular"
            2 => "Trasplante de &#243;rgano s&#243;lido"
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        "titulo" => "Abstract"
        "resumen" => "<span id="abst0005" class="elsevierStyleSection elsevierViewall"><p id="spar0005" class="elsevierStyleSimplePara elsevierViewall">Although retinal venous obstruction &#40;RVO&#41; has been primarily related to vascular risk factors and glaucoma&#44; there are a few studies of RVO in patients with solid organ transplants&#46;</p><p id="spar0010" class="elsevierStyleSimplePara elsevierViewall">An analysis was performed on total of 331 patients who presented with RVO &#40;branch RVO in 226 cases and central RVO in 105 cases&#41; over a 10 year period&#44; and the characteristics were compared with the 4 patients with a history of solid organ transplant &#40;liver&#44; renal&#44; or bipulmonary&#41; who presented with RVO&#46; In this series&#44; the onset of RVO in transplant patients occurred at earlier ages than in other patients with RVO &#40;58 vs&#46; 68 years&#44; respectively&#41;&#44; affected the central vein of the retina &#40;100&#37; vs&#46; 32&#37;&#41;&#44; and was associated with diabetes mellitus &#40;75&#37; vs&#46; 25&#37;&#41;&#44; as well as with steroidal &#40;100&#37; vs&#46; 1&#37;&#41; and immunosuppressive &#40;tacrolimus 75&#37; vs&#46; 0&#37;&#41; treatments&#46;</p></span>"
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      "es" => array:2 [
        "titulo" => "Resumen"
        "resumen" => "<span id="abst0010" class="elsevierStyleSection elsevierViewall"><p id="spar0015" class="elsevierStyleSimplePara elsevierViewall">La obstrucci&#243;n venosa retiniana &#40;OVR&#41; se ha relacionado fundamentalmente con los factores de riesgo vascular y con el glaucoma&#59; sin embargo&#44; existen pocos estudios de la OVR en pacientes con trasplante de &#243;rgano s&#243;lido&#46;</p><p id="spar0020" class="elsevierStyleSimplePara elsevierViewall">Se analiz&#243; una serie de 331 pacientes que presentaron OVR &#40;de rama en 226 casos y central en 105 casos&#41; a lo largo de 10 a&#241;os y se compararon las caracter&#237;sticas entre los 4 pacientes con antecedente de trasplante de &#243;rgano s&#243;lido &#40;hep&#225;tico&#44; renal o bipulmonar&#41; que presentaron una OVR y el resto&#46; En nuestra serie la OVR en los trasplantados comenz&#243; a edades m&#225;s tempranas que en el resto de pacientes con OVR &#40;58 vs&#46; 68 a&#241;os&#44; respectivamente&#41;&#44; afect&#243; a la vena central de la retina &#40;100&#37; vs&#46; 32&#37;&#41; y se asoci&#243; con la diabetes mellitus &#40;75&#37; vs&#46; 25&#37;&#41; y con los tratamientos esteroideo &#40;100&#37; vs&#46; 1&#37;&#41; e inmunosupresor &#40;tacrolimus 75&#37; vs&#46; 0&#37;&#41;&#46;</p></span>"
      ]
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    "NotaPie" => array:1 [
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        "etiqueta" => "&#9734;"
        "nota" => "<p class="elsevierStyleNotepara" id="npar0020">Please cite this article as&#58; Cerver&#243; A&#44; Gonz&#225;lez Bores P&#44; Casado A&#44; Ruiz Sancho MD&#44; Hern&#225;ndez Hern&#225;ndez JL&#44; Napal Lecumberri JJ&#46; Obstrucci&#243;n venosa retiniana en receptores de trasplante de &#243;rgano s&#243;lido&#46; Estudio de 4 casos y revisi&#243;n de la literatura&#46; Arch Soc Esp Oftalmol&#46; 2020&#59;95&#58;615&#8211;618&#46;</p>"
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          "en" => "<p id="spar0025" class="elsevierStyleSimplePara elsevierViewall">Evolution of macular edema in 4 RVO patients with transplant&#46; Retinal thickness &#40;&#956;m&#41;&#44; best corrected visual acuity &#40;BCVA&#41; and optical coherence tomography at baseline &#40;left&#41; and after one year of treatment &#40;right&#41;&#46;</p>"
        ]
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        "etiqueta" => "Table 1"
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          "leyenda" => "<p id="spar0035" class="elsevierStyleSimplePara elsevierViewall">DM&#58; diabetes mellitus&#59; DL&#58; dyslipidemia&#59; AHT&#58; arterial hypertension&#59; BCVA&#58; best corrected visual acuity&#59; RVO&#58; retinal venous obstruction&#46;</p>"
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                  <table border="0" frame="\n
                  \t\t\t\t\tvoid\n
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                  \t\t\t\t\ttable-head\n
                  \t\t\t\t  " align="" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t" scope="col" style="border-bottom: 2px solid black">&nbsp;\t\t\t\t\t\t\n
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                  \t\t\t\t\ttable-head\n
                  \t\t\t\t  " align="center" valign="\n
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                  \t\t\t\t" scope="col" style="border-bottom: 2px solid black">Case 1&nbsp;\t\t\t\t\t\t\n
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                  \t\t\t\t\ttable-head\n
                  \t\t\t\t  " align="center" valign="\n
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                  \t\t\t\t" scope="col" style="border-bottom: 2px solid black">Case 2&nbsp;\t\t\t\t\t\t\n
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                  \t\t\t\t\ttable-head\n
                  \t\t\t\t  " align="center" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t" scope="col" style="border-bottom: 2px solid black">Case 3&nbsp;\t\t\t\t\t\t\n
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                  \t\t\t\t\ttable-head\n
                  \t\t\t\t  " align="center" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t" scope="col" style="border-bottom: 2px solid black">Case 4&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t\t\t</th></tr></thead><tbody title="tbody"><tr title="table-row"><td class="td-with-role" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t ; entry_with_role_rowhead " align="left" valign="\n
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                  \t\t\t\t">Age&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
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                  \t\t\t\t  " align="left" valign="\n
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                  \t\t\t\t">58 years&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="left" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">66 years&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="left" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">63 years&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="left" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">45 years&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td></tr><tr title="table-row"><td class="td-with-role" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t ; entry_with_role_rowhead " align="left" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">Sex&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="left" valign="\n
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                  \t\t\t\t">Male&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="left" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">Male&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="left" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">Male&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="left" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">Male&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td></tr><tr title="table-row"><td class="td-with-role" title="\n
                  \t\t\t\t\ttable-entry\n
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                  \t\t\t\t">Transplant typeTransplant cause&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="left" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">LiverAlcoholic cirrhosis&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="left" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">Liver-kidneyLiver cirrhosis<a class="elsevierStyleCrossRef" href="#tblfn0005"><span class="elsevierStyleSup">a</span></a>IgA nephropathy&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="left" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">BipulmonaryAsbestosis&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="left" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">Renal &#40;3&#41;<a class="elsevierStyleCrossRef" href="#tblfn0010"><span class="elsevierStyleSup">b</span></a>IgA nephropathy&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td></tr><tr title="table-row"><td class="td-with-role" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t ; entry_with_role_rowhead " align="left" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">AHT&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="left" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">Yes&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="left" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">No&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="left" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">Yes&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="left" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">Yes&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td></tr><tr title="table-row"><td class="td-with-role" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t ; entry_with_role_rowhead " align="left" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">DL&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="left" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">Yes&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="left" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">Yes&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="left" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">No&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="left" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">Yes&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td></tr><tr title="table-row"><td class="td-with-role" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t ; entry_with_role_rowhead " align="left" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">DM&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="left" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">Yes&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="left" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">No&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="left" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">Yes&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="left" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">Yes&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td></tr><tr title="table-row"><td class="td-with-role" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t ; entry_with_role_rowhead " align="left" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">Corticoids&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="left" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">Yes&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="left" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">Yes&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="left" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">Yes&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="left" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">Yes&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td></tr><tr title="table-row"><td class="td-with-role" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t ; entry_with_role_rowhead " align="left" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">Immunosuppressants&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="left" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">Tacrolimus mycophenolate&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="left" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">Tacrolimus mycophenolate&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="left" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">Tacrolimus&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="left" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">No&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td></tr><tr title="table-row"><td class="td-with-role" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t ; entry_with_role_rowhead " align="left" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">RVO&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="left" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">Central&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="left" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">Central&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="left" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">Central&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="left" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">Central&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td></tr><tr title="table-row"><td class="td-with-role" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t ; entry_with_role_rowhead " align="left" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">Time between transplant and RVO &#40;months&#41;&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="left" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">18&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="left" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">20&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="left" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">12&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="left" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">108&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td></tr><tr title="table-row"><td class="td-with-role" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t ; entry_with_role_rowhead " align="left" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">BCVA at baseline-one year &#40;decimal&#41;&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="left" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">0&#46;1&#8211;0&#46;5&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="left" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">&#60;0&#46;05&#8211;0&#46;2&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="left" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">&#60;0&#46;05&#8211;0&#46;3&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="left" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">0&#46;1&#8211;1&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td></tr><tr title="table-row"><td class="td-with-role" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t ; entry_with_role_rowhead " align="left" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">Ophthalmological treatment during first year&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="left" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">Aflibercept&#40;&#215;6&#41;&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="left" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">Ozurdex &#40;&#215;<span class="elsevierStyleHsp" style=""></span>1&#41;Retinal panphotocoagulation&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="left" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">Ranibizumab &#40;&#215;7&#41;&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="left" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">Aflibercept &#40;&#215;1&#41;<a class="elsevierStyleCrossRef" href="#tblfn0015"><span class="elsevierStyleSup">c</span></a>&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td></tr><tr title="table-row"><td class="td-with-role" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t ; entry_with_role_rowhead " align="left" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">Glaucoma&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="left" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">No&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="left" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">Neovascular glaucoma at 3 months&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="left" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">No&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="left" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">No&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td></tr><tr title="table-row"><td class="td-with-role" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t ; entry_with_role_rowhead " align="left" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">Neovascularization&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="left" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">No&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="left" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">Iris neovascularization&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="left" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">No&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="left" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">No&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td></tr></tbody></table>
                  """
              ]
              "imagenFichero" => array:1 [
                0 => "xTab2474140.png"
              ]
            ]
          ]
          "notaPie" => array:3 [
            0 => array:3 [
              "identificador" => "tblfn0005"
              "etiqueta" => "a"
              "nota" => "<p class="elsevierStyleNotepara" id="npar0005">Alcoholic liver disease<span class="elsevierStyleHsp" style=""></span>&#43;<span class="elsevierStyleHsp" style=""></span>hemochromatosis&#46;</p>"
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              "identificador" => "tblfn0010"
              "etiqueta" => "b"
              "nota" => "<p class="elsevierStyleNotepara" id="npar0010">Treatment could not be completed due to new kidney transplant</p>"
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              "etiqueta" => "c"
              "nota" => "<p class="elsevierStyleNotepara" id="npar0015">Treatment could not be completed due to new kidney transplant</p>"
            ]
          ]
        ]
        "descripcion" => array:1 [
          "en" => "<p id="spar0030" class="elsevierStyleSimplePara elsevierViewall">Clinic characteristics and ophthalmological treatment of 4 RVO patients with transplants &#40;cases 1&#8211;4&#41;&#46;</p>"
        ]
      ]
    ]
    "bibliografia" => array:2 [
      "titulo" => "References"
      "seccion" => array:1 [
        0 => array:2 [
          "identificador" => "bibs0015"
          "bibliografiaReferencia" => array:10 [
            0 => array:3 [
              "identificador" => "bib0055"
              "etiqueta" => "1"
              "referencia" => array:1 [
                0 => array:2 [
                  "contribucion" => array:1 [
                    0 => array:2 [
                      "titulo" => "Risk factors for central and branch retinal vein occlusion&#58; a meta-analysis of published clinical data"
                      "autores" => array:1 [
                        0 => array:2 [
                          "etal" => false
                          "autores" => array:1 [
                            0 => "P&#46; Kolar"
                          ]
                        ]
                      ]
                    ]
                  ]
                  "host" => array:1 [
                    0 => array:1 [
                      "Revista" => array:5 [
                        "tituloSerie" => "J Ophthalmol"
                        "fecha" => "2014"
                        "volumen" => "2014"
                        "paginaInicial" => "724"
                        "paginaFinal" => "780"
                      ]
                    ]
                  ]
                ]
              ]
            ]
            1 => array:3 [
              "identificador" => "bib0060"
              "etiqueta" => "2"
              "referencia" => array:1 [
                0 => array:2 [
                  "contribucion" => array:1 [
                    0 => array:2 [
                      "titulo" => "Trombofilia y factores de riesgo vascular en la obstrucci&#243;n venosa retiniana"
                      "autores" => array:1 [
                        0 => array:2 [
                          "etal" => false
                          "autores" => array:4 [
                            0 => "J&#46;J&#46; Napal Lecumberri"
                            1 => "C&#46; Sedano Balbas"
                            2 => "J&#46; Canal Villanueva"
                            3 => "J&#46;L&#46; Hernandez Hernandez"
                          ]
                        ]
                      ]
                    ]
                  ]
                  "host" => array:1 [
                    0 => array:2 [
                      "doi" => "10.1016/j.rce.2013.01.012"
                      "Revista" => array:6 [
                        "tituloSerie" => "Rev Clin Esp"
                        "fecha" => "2013"
                        "volumen" => "213"
                        "paginaInicial" => "229"
                        "paginaFinal" => "234"
                        "link" => array:1 [
                          0 => array:2 [
                            "url" => "https://www.ncbi.nlm.nih.gov/pubmed/23566482"
                            "web" => "Medline"
                          ]
                        ]
                      ]
                    ]
                  ]
                ]
              ]
            ]
            2 => array:3 [
              "identificador" => "bib0065"
              "etiqueta" => "3"
              "referencia" => array:1 [
                0 => array:2 [
                  "contribucion" => array:1 [
                    0 => array:2 [
                      "titulo" => "The role of coagulation disorders in patients with retinal vein occlusion"
                      "autores" => array:1 [
                        0 => array:2 [
                          "etal" => false
                          "autores" => array:6 [
                            0 => "J&#46;J&#46; Napal"
                            1 => "S&#46; Neila"
                            2 => "R&#46; P&#233;rez-Montes"
                            3 => "I&#46; Sierra"
                            4 => "S&#46; Ruiz"
                            5 => "J&#46;L&#46; Hernandez"
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