Renal function, nephrogenic systemic fibrosis and other adverse reactions associated with gadolinium-based contrast media

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Unidad Central de Radiodiagnóstico, Madrid, " "etiqueta" => "e" "identificador" => "affe" ] 5 => array:3 [ "entidad" => "Servicio de Radiodiagnóstico., Hospital Universitario Dr. Peset Valencia, " "etiqueta" => "f" "identificador" => "afff" ] 6 => array:3 [ "entidad" => " Servicio de Nefrología, Hospital Universitario Marqués de Valdecilla, Santander, Cantabria, Spain, " "etiqueta" => "g" "identificador" => "affg" ] ] ] ] "titulosAlternativos" => array:1 [ "es" => array:1 [ "titulo" => "Función renal, fibrosis sistémica nefrogénica y otras reacciones adversas asociadas a los medios de contraste basados en el gadolinio" ] ] "resumenGrafico" => array:2 [ "original" => 0 "multimedia" => array:8 [ "identificador" => "fig1" "etiqueta" => "Fig. 1" "tipo" => "MULTIMEDIAFIGURA" "mostrarFloat" => true "mostrarDisplay" => false "copyright" => "Elsevier España" "figura" => array:1 [ 0 => array:4 [ "imagen" => "12375_19904_59997_en_12375_f1.jpg" "Alto" => 671 "Ancho" => 874 "Tamanyo" => 396611 ] ] "descripcion" => array:1 [ "en" => "Classification of the different gadolinium-based contrasts according to their distribution" ] ] ] "textoCompleto" => "INTRODUCTIONSince 1997, when it was reported by Cowper for the first time1, a condition called nephrogenic systemic fibrosis (NSF) has drawn the attention of nephrologists and radiologists from all over the world. It has been defined as a fibrosing disease that predominantly affects patients who have received gadolinium-based contrasts, with an estimated glomerular filtration rate (GFR) of less than 30ml/min/1.73m2 or those on haemodialysis2,3. In this document, we aim to summarise the clinical expression of NSF, the data known about different gadolinium-based contrasts, the possibilities of identifying patients at risk in order to prevent its onset and the types of treatment for this disease. GADOLINIUMGadolinium-based contrast media (GBCM) are used in magnetic resonance imaging (MRI) studies due to their magnetic ability to change the position of the protons of water molecules in tissues, which is a change that improves the study’s diagnostic capacity. These contrast media act by shorting the T1 and T2 relaxation time of the tissues to which they are distributed, which fundamentally leads to an increased signal in T1-weighted sequences. However, if the GBCM concentration is high, T2 shortening is predominant, which causes a decrease in the signal. Nine agents have currently been approved and are available in Europe; their characteristics are summarised in Table 1. Structure and pharmacokineticsGadolinium (Gd) is a heavy metal with a high paramagnetic capacity and which is not soluble in water. In its free form (Gd3) it is very toxic, and as such, it is necessary to chelate it with different organic ligands, creating gadolinium chelates4. There is a certain tendency for the ion to separate from the ligand in a process called chelation blocking5. If this process continues, there is transmetalation and this causes NSF6. Transmetalation is a chemical reaction whereby a secondary free metal with affinity for the chelate allows gadolinium release (Gd3). In renal failure patients, it decreases the renal elimination of GBCM; its half-life is extended, which increases the possibility of Gd3 dissociating from the chelate. This facilitates the recruitment of circulating fibrocytes, triggering the fibrosing reaction7,8. The structure of gadolinium chelates may be linear or macrocyclic, with the latter being that which shows higher thermodynamic stability constants. Being hydrophilic compounds, they can be classified9 as ionic and non-ionic, with the latter having lower osmolarity for the same concentration (Table 1). Of all the agents, non-ionic linear agents are the least stable and they increase the risk of transmetalation. As such, they are associated with a higher risk of NSF10,11.In terms of the distribution after their intravenous administration (Table 1), GBCM are classified into three types: non-specific extracellular, mixed (hepatospecific extracellular and intracellular distribution with a variable percentage of biliary elimination) and intravascular (they remain in the intravascular space for longer). The vast majority of GBCM used in daily practice are from the first group12.GD chelates have a molecular weight that ranges between 500 and 1,000Da, they are not bound to plasma proteins and are not lipophilic, which means that after their intravenous administration, there is a distribution and balance within the extracellular space. All of these characteristics help to create the good glomerular filtration capacity of GD chelates6. They are small molecules that leave the vascular space quickly, with a half-life in plasma of around 15-30 minutes. They do not cross the blood-brain barrier or the cell membrane, and as such, after leaving the vascular space, they are distributed around the interstitial space. They are eliminated, without being metabolised, through glomerular filtration. In patients with normal renal function, 98% of Gd is eliminated in urine in the first 24 hours13, and it is not eliminated from or reabsorbed into the renal tubule14. Pharmacokinetic studies have demonstrated its elimination by glomerular filtration, extending the contrast’s half-life by more than 30 hours but without side effects of nephrotoxicity. In renal failure patients, peritoneal clearance of GBCM was 3.8ml/minute/1.73m2 with a T1/2 of 52.7 hours, which is not surprising, given the slow clearance of peritoneal dialysis techniques. 75% of doses administered were eliminated by peritoneal dialysis after 5 days and as such, peritoneal dialysis is not an effective technique for eliminating contrast. After two haemodialysis sessions, 95% of the gadolinium dose administered was eliminated but there were no tests of its efficacy in the removing the risk of NSF. However, we recommend that patients on dialysis undergo haemodialysis less than two hours after administration and another haemodialysis session the next day. It is not routinely recommended in non-dialysis patients6. Dose and administration rangeAs a gadolinium atom modifies the relaxation times of many neighbouring hydrogen nuclei, the contrast dose used is low, significantly lower than the quantity of iodine administered for computerised tomography studies15. The most used commercial preparations have a concentration of 0.5 molar (0.5M), and as such, the standard administration dose is 0.1mmol/kg of weight, equivalent to 0.2ml/kg of contrast4. High doses and increases in the accumulated dose increase the risk of NSF6. NEPHROGENIC SYSTEMIC FIBROSISNSF is an acquired fibrosing disorder that has been observed in patients with severely impaired renal function. Although the term “nephrogenic systemic fibrosis” was adopted in 2005, it was recognised for the first time in 1997 and reported in the year 2000 by Cowper as a scleromyxedema-like illness in dialysis patients1. In our country, Rodríquez Jornet et al. published the first case in 2009, with a detailed pathological review of the patient, and the macroscopic and microscopic images are available at: http://www.revistanefrologia.com/modules.php?name=articulos&idarticulo=129&idlangart=ES16. Table 2 displays the chronology and evolution of the term. EpidemiologyNSF affects most cases of patients with impaired renal function, particularly those with an estimated glomerular filtration rate of less than 30ml/min/1.73m2 independently of the origin of renal damage (acute, chronic or haemodialysis patients)2,3, who are administered GBCM. According to Zou et al., the two most affected groups are patients with chronic renal failure (CRF) on dialysis (85% of cases) and those with acute renal failure17. Another patient group that may be affected are those with liver failure who have acute hepatorenal syndrome18,19. It is well-known that not all risk patients exposed to GBCM have a disease6.NSF is more common in middle-aged patients (50-60 years of age)20, although it may affect children and the elderly21,22. There are no differences according to race or sex, or any relationship with the cause or duration of CRF20.Although various authors have reported different prevalences in accordance with the population selected, it is currently estimated that there is a mean incidence of 0%-18% in the risk population23. There is a clear relationship between the dose of GBCM used and the risk of NSF, with there being a NSF incidence close to 0 after an exposure to a standard dose15,24. Differences were also reported in the incidence of NSF according to the characteristics of the molecule, with a greater number of cases of NSF having been recorded after exposure to non-ionic linear compounds. As we have mentioned before, it seems that there is a greater risk of incidence in the peritoneal dialysis patient group25.Thanks to the knowledge of risk factors and the better use of GBCM, the number of cases of NSF has decreased significantly26. Since 2008, there have been no cases of any CM being reported without these CM being replaced27. Many hospitals have continued to use the same GBCM but have changed the patterns of use. AetiopathogenesisAlthough the exact pathogenesis of NSF continues to be unknown, the only solid association identified in all patients with NSF is renal failure, both in its chronic and acute forms, and its presence is a sine qua non condition for the diagnosis of the disease28. However, only a small percentage of the risk population exposed to GBCM develops NSF, and cases of NSF have also been reported without exposure to GBCM29.Given that exposure to GBCM does not explain all cases of NSF, other coadjuvant risk factors have been studied that may contribute to its development, many of them associated with situations of renal failure. Pro-inflammatory factors: vessel injury, surgery, thrombosis, procoagulant stages, severe infection, chronic hepatitis C, chronic liver disease and liver transplantation, hyperparathyroidism and hypothyroidism. Biochemical factors: acidosis, intravenous iron, erythropoietin, calcium and phosphorus30. Pathophysiological mechanismsThe two forms, free Gd ions and the chelate-Gd complex may cause the release of cytokines, stimulating skin macrophages (Gd-free ions) or peripheral blood monocytes (chelate-Gd complexes). All of these processes (macrophage activation, pro-inflammatory cytokine release, differentiation of fibrocytes in blood, activation of fibroblasts, TGF-β pathways, metallothionein, FGF-23 and Klotho protein) stimulate fibroblasts30, a response that creates collagen deposits and fibrosis by increasing transforming growth factor beta 1 levels31. The presence of renal failure contributes to the release of free GD3 by increasing transmetalation in a uraemic environment and decreasing the glomerular filtration rate32. A complete diagram with pathophysiological mechanisms published by Chopra et al. is available at http://www.hindawi.com/journals/ijn/2012/912189/fig1/30.  DiagnosisIt presents clinically as a thickening and hardening of the skin, associated with pain, muscle weakness, bone pain and joint contractures, which causes severe disability3. Over time there may be loss of flexibility, limited mobility and joint contractures2,34. Lesions may appear in the form of plaques (58%) with irregular edges and papules (32%), nodules (17%), macules, vesicles, blisters, bullae and ulcers2,21,35,36. It typically affects the legs, but may be found anywhere apart from the face in most cases35. These skin lesions progress over time to fibrotic skin surrounded by wrinkles, also known as “orange peel”37. Most lesions are hyperpigmented and erythematous (39%), but their colour can vary (purple, brown, yellow, pink, orange-red, grey-brown)35,38. Sometimes these symptoms can be confused and wrongly treated as cellulitis6. Kroshinsky et al. published the case of a 46-year-old woman with CRF, oedema in her legs and skin changes, who was examined and a differential diagnosis was carried out, with macroscopic and microscopic images of the dermis being created39. At the time this condition was first reported, scientists thought that it was just a skin disorder, but it is nowadays well-known that it affects joints, the muscular system, the testicles, the kidney, the heart and the dura mater31,40,41. Another sign of interest is that it has similar symptoms to conjunctivitis in 75% of cases6.The onset of symptoms is variable; it generally occurs between two weeks and two months after exposure to GBCM. However, delayed onset has also been reported, years after exposure17.The histological diagnosis is based on a skin biopsy where skin fibrosis is observed, with thickened collagen bundles and a variable quantity of elastic fibres and mucin. The mediating cell is the circulating fibrocyte (CD34 and positive procollagen I in the immunohistochemistry stain)28,42. In most cases, the inflammatory cells are not present and on some occasions, perivascular mononuclear infiltrate has been observed43. Sanyal et al. carried out a histological review of a clinical case with an electron microscope and energy dispersive x-ray fluorescence44.With regard to its association with GBCM, the first publications are from 200645,46, with the presence of gadolinium in tissues being demonstrated only one year later47,48. Under normal conditions, GBCM are eliminated by glomerular filtration in 1-2 days. Prognosis The natural outcome of NSF is not fully known. It has been reported that in up to 5% of cases, it may have a fulminant course20. A third will have a mild course without functional limitation17. There is increased mortality after 24 months of skin manifestations of NSF49. The true mortality rate is unknown and is difficult to determine, given the high prevalence of other comorbidities34. TreatmentThere is no evidence of effective treatment and only in transplant patients has an improvement or a detention in the progression of renal disease been achieved in the case of acute renal failure50.As mentioned above, GBCM molecular weight allows glomerular filtration6 and given these characteristics, there is the possibility of elimination with haemodialysis51. Several authors have carried out studies that confirm the elimination of various types of GBCM with three haemodialysis sessions of three hours each. Based on these results, the European Society of Radiology recommends carrying out nine hours of haemodialysis over three sessions. However, gadofosveset is an agent that is difficult to eliminate by haemodialysis due to a large proportion of it being bound to serum albumin6. Broome et al. presented a series with three patients who developed NSF despite undergoing the previously indicated haemodialysis sessions52. To present, no studies have been carried out on continuous haemofiltration or continuous venovenous haemodiafiltration.Most treatments proposed are still being researched and they are currently yielding suboptimal results (oral steroids, extracorporeal photopheresis, plasmapheresis, thalidomide, cyclophosphamide, pentoxifylline, intravenous immunoglobulin, interferon alpha and vitamin D, ultraviolet radiation and etanercept)20. Recently, combined treatments with imatinib and extracorporeal photopheresis have been attempted53,54. The efficacy of treatment with alefacept was also confirmed in three patients with NSF55. The improvement in renal function (transplantation and resolution of acute renal failure) may slow down and even reverse the process20. However, in reality, no treatment has shown to be effective; therefore, prevention is important. PREVENTION OF NEPHROGENIC SYSTEMIC FIBROSISIdentification of patients with chronic kidney diseaseThe classification of chronic kidney disease (CKD) followed the initial publication of the National Kidney Foundation through the Kidney Disease Outcomes Quality Initiative (K-DOQI) guidelines56. The definition of CKD by K-DOQI is as follows:Renal damage for at least three months, defined by structural or functional abnormalities of the kidney or without a decrease in the GFR and shown by pathological changes or renal damage markers (changes in the composition of blood or urine or changes in images of the kidney).GFR <60ml/min/1.73m2 for more than three months, with or without renal damage.It is common in consultations for renal function to be studied simply by measuring serum creatinine (SCr). However, and although it is true that SCr is a good follow-up parameter of the evolution of filtration, it is not always equivalent to glomerular filtration. SCr also depends on factors other than the GFR, such as tubular elimination and the generation and extrarenal elimination of creatinine, which explains the wide range for SCr in healthy individuals. Some studies57 show a high percentage of males and particularly of females who have reductions in the GFR with normal SCr. Even with creatinine ranges between 1.3 and 2.5mg/dl, there are significant percentages of very severe renal failure (GFR below 30ml/min/1.73m2). Therefore, the real prevalence of individuals with renal failure appears to be higher than that which can be determined by studying SCr. The results of these observations are important. This “hidden” renal failure may easily worsen due to the large amount of medications, particularly in glomerular haemodynamics, such as non-steroidal anti-inflammatory drugs, angiotensin-converting-enzyme inhibitors and other types of drugs. Likewise, patients often undergo x-ray examinations when there is an inadequate evaluation of renal function, based only on plasma creatinine.The international organisation KDIGO (Kidney Disease Global Outcomes; http://www.kdigo.org/) recommends using prediction equations to calculate the GFR based on SCr. In adults, the formulas most used are those of the Modification of Diet in Renal Disease (MDRD) study and that of Cockcroft and Gault58. There are certain circumstances in which the first is not validated (Table 3) and in order to estimate the GFR, 24-hour urine should be collected or studies of creatinine clearance in 24-hour urine, iothalamate, iohexol or insulin should be carried out. In any case, the estimation of GFR using the MDRD formula is more accurate that SCr, and considering these limitations, the doctor may obtain valid information about renal function. Recently, KDIGO recommended a new formula for calculating renal function, called CKD-EPI (Chronic Kidney Disease Epidemiology Collaboration), which is more accurate than MDRD for values close to 60ml/min59. Likewise, it updated the CKD classification by incorporating the CGA concept: C: cause of CKD, G: GFR incorporating groups 3a and 3b, and A: albuminuria with three subgroups: A1 (<30mg/g of creatinine), A2 (30-300) and A3 (>300)60 (Table 4).There are occasionally no data on renal function. In patients who have unknown renal function and who require an x-ray examination with gadolinium, a series of parameters should be considered, such as renal failure risk factors, which will mean that the examination must be delayed until their exact renal function is known (Table 5). The study of risk factors must be part of the routine before using GBCM in any hospital. IMMEDIATE ADVERSE REACTIONS TO GADOLINIUM-BASED CONTRAST MEDIAGBCM are very safe drugs, with a low immediate adverse reaction (IAR) rate of 0.07%-2.4%61-63, mostly of a mild nature, mainly nausea or headaches at the time of injection.Although all GBCM show quite a similar IAR incidence64, there are differences in their occurrence that cannot seem to be explained by their physicochemical characteristics65,66 (Table 6).Among IAR to GBCM, we must highlight allergic reactions, due to their relevance, which are defined as a type of adverse reaction measured immunologically by antibodies or lymphocytes, characterised by being specific and recurrent if the patient is exposed to the drug again67. Two types of allergic reaction to x-ray contrast media are distinguished depending on the moment of presentation: immediate and non-immediate or delayed68. Immediate allergic reactions are measured by immunoglobin E; if a systemic allergic reaction develops, there is anaphylaxis. This is caused by the release of histamines and other mediators, causing symptoms that may put the life of the patients at risk: laryngeal oedema, angioedema, upper airway obstruction, urticarial, nausea, vomiting, low blood pressure and/or shock.The occurrence of allergic reactions to GBCM is unpredictable, although it is known that its incidence increases in asthmatic patients and in those with food allergies and/or medication allergies58,69.With regards to how to act against an allergic reaction to a GBCM, Figure 1 displays an algorithm, which schematically shows how to manage these emergency situations in the x-ray diagnosis department. LEARN FROM EVIDENCEClinical use and abuseSince the introduction of GBCM in MRI, its applications have been increasing daily, and it is now used in all organs of the body. During the first few years, a false sense of security was created, which led to an overenthusiastic use of GBCM, which were often used as replacements for iodinated contrasts in computerised tomography or conventional angiography studies in patients who were allergic to iodinated contrasts or in those with renal failure and even in MRI, at doses much higher than those recommended.This use of GBCM, before NSF was reported, was carried out without any type of control in terms of dose or administration times and without taking any precautions in relation to the renal function of patients.The reporting of this delayed and potentially serious adverse reaction marked a turning point that forced x-ray departments to establish new guidelines aimed at protecting patients. Although the initial information may have been confusing, some evidence was clear and shed light with regard to the measures to adopt to prevent disease: it was only reported in patients with severe renal failure (GFR<30), its incidence was related to the administration of high doses of gadolinium and it was more common in patients with pro-inflammatory symptoms. Clinical limitations in the use of gadolinium-based contrast media The main limitation with regard to the use of GBCM in MRI is the difficulty of knowing the GFR of patients, particularly outpatients. In this regard, collaboration between the x-ray department, which would have to routinely record renal failure risk factors (Table 4) before carrying out the GBCM study, and the doctor who requests the test, who must provide information about the patient’s renal function and assess the risk/benefit of the test requested for the patient. If any of the risk factors of renal failure are confirmed or the GFR of the patient cannot be excluded or assessed, it would be preferable to postpone it until MDRD or CKD-EPI are determined in another test.Since gadolinium has been considered an agent the potentially causes NSF, restrictive guidelines have been designed for its administration (Table 7), with the most important aspects being the possession of recent GFR data and the adjustment of doses used in accordance with the latter (Table 8).In 2010, the U.S. Food and Drug Administration (FDA) established general precautions on the use of GBCM and limited Magnevist®, Omniscan® and Optimark® GBCM in patients with acute renal failure and high-risk severe CRF43. Two years after the recommendations carried out by the FDA, a 71% decrease was observed in MRI in patients with MDRD 30ml/min/1.73m2 and a 99% increase was observed in requests for SCr a month before carrying out MRI70. A year before, the European Medicines Agency also contraindicated the use of the aforementioned GBCM in patients with severe renal failure, infants and those awaiting liver transplantation43. According to Bennet et al., in Denmark since 2007 and in the United States since 2009, no new cases of NSF have been published71.The possibility of this adverse reaction occurring should not limit clinical action. It is essential to find a balance between the guarantee of patient safety and the carrying out of the tests necessary for correct clinical management. As such, the need for a test and its effectiveness will be discussed clinically, and other diagnostic options will be taken into account, as well as alternative contrasts. In short, the risk/benefit will be weighed up. CONCLUSIONSGBCM are a group of drugs with differentiated physiochemical characteristics that are increasingly being used in diagnosis by MRI.Due to the fact that they were initially used without taking patients’ renal function into account, and without an exact knowledge of the toxic doses permitted, a series of adverse effects appeared, and in particular, the predominantly dermatological multiple organ fibrosing disorder subsequently known as NSF, which discredited its use.The reporting of this delayed and potentially severe adverse reaction marked a turning point, since it made it compulsory to establish consensuses to protect patients by assessing the GFR and risk factors. All of this along with dose adjustment have decreased the number of adverse reactions significantly and in the last five years there have hardly been any published cases with the use of gadolinium.As for IAR, all GBCM have a low and similar incidence, although there are some differences between them, with gadodiamide having the lowest incidence63,64,67. These reactions, although they are generally mild, can occasionally be severe and even fatal.Patient protection is key when GBCM are used in x-rays. The identification and selection of patients at risk, the assessment of the risk and benefit and informing the patient about the adverse effects are essential.In most cases, it is necessary to assess the patient, make a multidisciplinary decision, and in particular, treat every case individually. Conflicts of interestThe content of this review is based on an update of Working Session presentations sponsored by GE Healthcare entitled What happened to NSF? The current situation, which took place at the XXXI SERAM Conference (Granada, 2012). The publication of this review was carried out independently of the Working Session sponsor.<a href="grande/12375_19904_59997_en_12375_f1.jpg" class="elsevierStyleCrossRefs"><img src="12375_19904_59997_en_12375_f1.jpg" alt="Classification of the different gadolinium-based contrasts according to their distribution "></img></a>Table 1. Classification of the different gadolinium-based contrasts according to their distribution <a href="grande/12375_16025_59998_en_t2_copy1.jpg" class="elsevierStyleCrossRefs"><img src="12375_16025_59998_en_t2_copy1.jpg" alt="Chronology and evolution of the term &"></img></a>Table 2. Chronology and evolution of the term &<a href="grande/12375_16025_59999_en_t3_copy1.jpg" class="elsevierStyleCrossRefs"><img src="12375_16025_59999_en_t3_copy1.jpg" alt="Circumstances in which the MDRD (Modification of Diet in Renal Disease) equation is not valid for calculating the glomerular filtration rate "></img></a>Table 3. Circumstances in which the MDRD (Modification of Diet in Renal Disease) equation is not valid for calculating the glomerular filtration rate <a href="grande/12375_16025_60000_en_t4_copy1.jpg" class="elsevierStyleCrossRefs"><img src="12375_16025_60000_en_t4_copy1.jpg" alt="Classification of chronic kidney disease (57)"></img></a>Table 4. Classification of chronic kidney disease (57)<a href="grande/12375_16025_60001_en_t5_copy1.jpg" class="elsevierStyleCrossRefs"><img src="12375_16025_60001_en_t5_copy1.jpg" alt="Chronic kidney disease risk factors "></img></a>Table 5. Chronic kidney disease risk factors <a href="grande/12375_16025_60002_en_t6_copy1.jpg" class="elsevierStyleCrossRefs"><img src="12375_16025_60002_en_t6_copy1.jpg" alt="Percentage of immediate adverse reactions to gadolinium-based contrast media "></img></a>Table 6. Percentage of immediate adverse reactions to gadolinium-based contrast media <a href="grande/12375_16025_60003_en_t7_copy1.jpg" class="elsevierStyleCrossRefs"><img src="12375_16025_60003_en_t7_copy1.jpg" alt="Measures to avoid nephrogenic systemic fibrosis development "></img></a>Table 7. Measures to avoid nephrogenic systemic fibrosis development <a href="grande/12375_16025_60004_en_t8_copy1.jpg" class="elsevierStyleCrossRefs"><img src="12375_16025_60004_en_t8_copy1.jpg" alt="Administration of gadolinium adjusted to renal function "></img></a>Table 8. Administration of gadolinium adjusted to renal function <a href="grande/12375_16025_60005_en_f1_copy2.jpg" class="elsevierStyleCrossRefs"><img src="12375_16025_60005_en_f1_copy2.jpg" alt="Protocol for treating adverse reactions to gadolinium."></img></a>Figure 1. Protocol for treating adverse reactions to gadolinium." "pdfFichero" => "P1-E572-S4645-A12375-EN.pdf" "tienePdf" => true "PalabrasClave" => array:2 [ "es" => array:4 [ 0 => array:4 [ "clase" => "keyword" "titulo" => "Palabras clave" "identificador" => "xpalclavsec437743" "palabras" => array:1 [ 0 => "Reacciones adversas" ] ] 1 => array:4 [ "clase" => "keyword" "titulo" => "Palabras clave" "identificador" => "xpalclavsec437745" "palabras" => array:1 [ 0 => "Resonancia magnética" ] ] 2 => array:4 [ "clase" => "keyword" "titulo" => "Palabras clave" "identificador" => "xpalclavsec437747" "palabras" => array:1 [ 0 => "Gadolinio" ] ] 3 => array:4 [ "clase" => "keyword" "titulo" => "Palabras clave" "identificador" => "xpalclavsec437749" "palabras" => array:1 [ 0 => "Fibrosis sistémica nefrogénica" ] ] ] "en" => array:4 [ 0 => array:4 [ "clase" => "keyword" "titulo" => "Keywords" "identificador" => "xpalclavsec437744" "palabras" => array:1 [ 0 => "Adverse reactions" ] ] 1 => array:4 [ "clase" => "keyword" "titulo" => "Keywords" "identificador" => "xpalclavsec437746" "palabras" => array:1 [ 0 => "MRI" ] ] 2 => array:4 [ "clase" => "keyword" "titulo" => "Keywords" "identificador" => "xpalclavsec437748" "palabras" => array:1 [ 0 => "Gadolinium" ] ] 3 => array:4 [ "clase" => "keyword" "titulo" => "Keywords" "identificador" => "xpalclavsec437750" "palabras" => array:1 [ 0 => "Nephrogenic systemic fibrosis" ] ] ] ] "tieneResumen" => true "resumen" => array:2 [ "es" => array:1 [ "resumen" => "La fibrosis sistémica nefrogénica es un trastorno fibrosante que afecta a pacientes con deterioro de la función renal y se asocia a la administración de medios de contraste basados en el gadolinio, empleados en la resonancia magnética. A pesar de tratarse de un grupo de fármacos que se consideraban seguros, la notificación de esta reacción adversa, potencialmente grave, supuso un punto de inflexión en las pautas de administración de estos medios de contraste. Se han intentado establecer parámetros de seguridad a fin de identificar a los pacientes con factores de riesgo por presentar insuficiencia renal. La estrecha farmacovigilancia y el rigor en la observación de las normativas actuales, con especial atención al valor del filtrado glomerular, han reducido los casos publicados relacionados con el uso de medios de contraste basados en el gadolinio. En un encuentro entre radiólogos y nefrólogos revisamos los aspectos más relevantes en la actualidad y las recomendaciones para su prevención." ] "en" => array:1 [ "resumen" => "Nephrogenic systemic fibrosis is a fibrosing disorder that affects patients with impaired renal function and is associated with the administration of gadolinium-based contrast media used in MRI. Despite being in a group of drugs that were considered safe, report about this potentially serious adverse reaction was a turning point in the administration guidelines of these contrast media. There has been an attempt to establish safety parameters to identify patients with risk factors of renal failure. The close pharmacovigilance and strict observation of current regulations, with special attention being paid to the value of glomerular filtration, have reduced the published cases involving the use of gadolinium-based contrast media. In a meeting between radiologists and nephrologists we reviewed the most relevant aspects currently and recommendations for its prevention." ] ] "multimedia" => array:9 [ 0 => array:8 [ "identificador" => "fig1" "etiqueta" => "Fig. 1" "tipo" => "MULTIMEDIAFIGURA" "mostrarFloat" => true "mostrarDisplay" => false "copyright" => "Elsevier España" "figura" => array:1 [ 0 => array:4 [ "imagen" => "12375_19904_59997_en_12375_f1.jpg" "Alto" => 671 "Ancho" => 874 "Tamanyo" => 396611 ] ] "descripcion" => array:1 [ "en" => "Classification of the different gadolinium-based contrasts according to their distribution" ] ] 1 => array:8 [ "identificador" => "fig2" "etiqueta" => "Tab. 2" "tipo" => "MULTIMEDIAFIGURA" "mostrarFloat" => true "mostrarDisplay" => false "copyright" => "Elsevier España" "figura" => array:1 [ 0 => array:4 [ "imagen" => "12375_16025_59998_en_t2_copy1.jpg" "Alto" => 1524 "Ancho" => 1048 "Tamanyo" => 488306 ] ] "descripcion" => array:1 [ "en" => "Chronology and evolution of the term &" ] ] 2 => array:8 [ "identificador" => "fig3" "etiqueta" => "Tab. 3" "tipo" => "MULTIMEDIAFIGURA" "mostrarFloat" => true "mostrarDisplay" => false "copyright" => "Elsevier España" "figura" => array:1 [ 0 => array:4 [ "imagen" => "12375_16025_59999_en_t3_copy1.jpg" "Alto" => 694 "Ancho" => 1065 "Tamanyo" => 187431 ] ] "descripcion" => array:1 [ "en" => "Circumstances in which the MDRD (Modification of Diet in Renal Disease) equation is not valid for calculating the glomerular filtration rate" ] ] 3 => array:8 [ "identificador" => "fig4" "etiqueta" => "Tab. 4" "tipo" => "MULTIMEDIAFIGURA" "mostrarFloat" => true "mostrarDisplay" => false "copyright" => "Elsevier España" "figura" => array:1 [ 0 => array:4 [ "imagen" => "12375_16025_60000_en_t4_copy1.jpg" "Alto" => 538 "Ancho" => 2172 "Tamanyo" => 276337 ] ] "descripcion" => array:1 [ "en" => "Classification of chronic kidney disease (57)" ] ] 4 => array:8 [ "identificador" => "fig5" "etiqueta" => "Tab. 5" "tipo" => "MULTIMEDIAFIGURA" "mostrarFloat" => true "mostrarDisplay" => false "copyright" => "Elsevier España" "figura" => array:1 [ 0 => array:4 [ "imagen" => "12375_16025_60001_en_t5_copy1.jpg" "Alto" => 647 "Ancho" => 1050 "Tamanyo" => 161461 ] ] "descripcion" => array:1 [ "en" => "Chronic kidney disease risk factors" ] ] 5 => array:8 [ "identificador" => "fig6" "etiqueta" => "Tab. 6" "tipo" => "MULTIMEDIAFIGURA" "mostrarFloat" => true "mostrarDisplay" => false "copyright" => "Elsevier España" "figura" => array:1 [ 0 => array:4 [ "imagen" => "12375_16025_60002_en_t6_copy1.jpg" "Alto" => 803 "Ancho" => 2158 "Tamanyo" => 433837 ] ] "descripcion" => array:1 [ "en" => "Percentage of immediate adverse reactions to gadolinium-based contrast media" ] ] 6 => array:8 [ "identificador" => "fig7" "etiqueta" => "Tab. 7" "tipo" => "MULTIMEDIAFIGURA" "mostrarFloat" => true "mostrarDisplay" => false "copyright" => "Elsevier España" "figura" => array:1 [ 0 => array:4 [ "imagen" => "12375_16025_60003_en_t7_copy1.jpg" "Alto" => 862 "Ancho" => 1069 "Tamanyo" => 341023 ] ] "descripcion" => array:1 [ "en" => "Measures to avoid nephrogenic systemic fibrosis development" ] ] 7 => array:8 [ "identificador" => "fig8" "etiqueta" => "Tab. 8" "tipo" => "MULTIMEDIAFIGURA" "mostrarFloat" => true "mostrarDisplay" => false "copyright" => "Elsevier España" "figura" => array:1 [ 0 => array:4 [ "imagen" => "12375_16025_60004_en_t8_copy1.jpg" "Alto" => 735 "Ancho" => 1088 "Tamanyo" => 246242 ] ] "descripcion" => array:1 [ "en" => "Administration of gadolinium adjusted to renal function" ] ] 8 => array:8 [ "identificador" => "fig9" "etiqueta" => "Fig. 1" "tipo" => "MULTIMEDIAFIGURA" "mostrarFloat" => true "mostrarDisplay" => false "copyright" => "Elsevier España" "figura" => array:1 [ 0 => array:4 [ "imagen" => "12375_16025_60005_en_f1_copy2.jpg" "Alto" => 1618 "Ancho" => 2112 "Tamanyo" => 884931 ] ] "descripcion" => array:1 [ "en" => "Protocol for treating adverse reactions to gadolinium." ] ] ] "bibliografia" => array:2 [ "titulo" => "Bibliography" "seccion" => array:1 [ 0 => array:1 [ "bibliografiaReferencia" => array:82 [ 0 => array:3 [ "identificador" => "bib1" "etiqueta" => "1" "referencia" => array:1 [ 0 => array:3 [ "referenciaCompleta" => "Cowper SE, Robin HS, Steinberg SM, Su LD, Gupta S, LeBoit PE. 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Función renal, fibrosis sistémica nefrogénica y otras reacciones adversas asociadas a los medios de contraste basados en el gadolinio

Ana Cangaa, Maria Kislikovab, María Martínez-Gálvezc, Mercedes Ariasd, Patricia Fraga-Rivase, Cecilio Poyatosf, Ángel L.M. de Franciscog, Ángel L.M. de Franciscob

a Servicio de Radiodiagnóstico, Hospital Universitario Marqués de Valdecilla, Santander, Cantabria,

b Servicio de Nefrología, Hospital Universitario Marqués de Valdecilla, Santander, Cantabria,

c Servicio de Radiodiagnóstico, Hospital José María Morales Meseguer, Murcia,

d Unidad de Diagnóstico por Imagen Galaria. Empresa Pública de Servicios Sanitarios, Complejo Hospitalario Universitario de Vigo,

e Servicio de Radiodiagnóstico, Hospital del Henares. Unidad Central de Radiodiagnóstico, Madrid,

f Servicio de Radiodiagnóstico., Hospital Universitario Dr. Peset Valencia,

g Servicio de Nefrología, Hospital Universitario Marqués de Valdecilla, Santander, Cantabria, Spain,

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are used in magnetic resonance imaging &#40;MRI&#41; studies due to their magnetic ability to change the position of the protons of water molecules in tissues&#44; which is a change that improves the study&#8217;s diagnostic capacity&#46; These contrast media act by shorting the T1 and T2 relaxation time of the tissues to which they are distributed&#44; which fundamentally leads to an increased signal in T1-weighted sequences&#46; However&#44; if the GBCM concentration is high&#44; T2 shortening is predominant&#44; which causes a decrease in the signal&#46; Nine agents have currently been approved and are available in Europe&#59; their characteristics are summarised in Table 1&#46;</p><p class="elsevierStylePara"><span class="elsevierStyleBold">&#160;</span></p><p class="elsevierStylePara"><span class="elsevierStyleBold">Structure and pharmacokinetics</span></p><p class="elsevierStylePara">Gadolinium &#40;Gd&#41; is a heavy metal with a high paramagnetic capacity and which is not soluble in water&#46; In its free form &#40;Gd3&#41; it is very toxic&#44; and as such&#44; it is necessary to chelate it with different organic ligands&#44; creating gadolinium chelates<span class="elsevierStyleSup">4</span>&#46; There is a certain tendency for the ion to separate from the ligand in a process called chelation blocking<span class="elsevierStyleSup">5</span>&#46; If this process continues&#44; there is transmetalation and this causes NSF<span class="elsevierStyleSup">6</span>&#46; Transmetalation is a chemical reaction whereby a secondary free metal with affinity for the chelate allows gadolinium release &#40;Gd3&#41;&#46; In renal failure patients&#44; it decreases the renal elimination of GBCM&#59; its half-life is extended&#44; which increases the possibility of Gd3 dissociating from the chelate&#46; This facilitates the recruitment of circulating fibrocytes&#44; triggering the fibrosing reaction<span class="elsevierStyleSup">7&#44;8</span>&#46; The structure of gadolinium chelates may be linear or macrocyclic&#44; with the latter being that which shows higher thermodynamic stability constants&#46; Being hydrophilic compounds&#44; they can be classified<span class="elsevierStyleSup">9</span> as ionic and non-ionic&#44; with the latter having lower osmolarity for the same concentration &#40;Table 1&#41;&#46; Of all the agents&#44; non-ionic linear agents are the least stable and they increase the risk of transmetalation&#46; As such&#44; they are associated with a higher risk of NSF<span class="elsevierStyleSup">10&#44;11</span>&#46;</p><p class="elsevierStylePara">In terms of the distribution after their intravenous administration &#40;Table 1&#41;&#44; GBCM are classified into three types&#58; non-specific extracellular&#44; mixed &#40;hepatospecific extracellular and intracellular distribution with a variable percentage of biliary elimination&#41; and intravascular &#40;they remain in the intravascular space for longer&#41;&#46; The vast majority of GBCM used in daily practice are from the first group<span class="elsevierStyleSup">12</span>&#46;</p><p class="elsevierStylePara">GD chelates have a molecular weight that ranges between 500 and 1&#44;000Da&#44; they are not bound to plasma proteins and are not lipophilic&#44; which means that after their intravenous administration&#44; there is a distribution and balance within the extracellular space&#46; All of these characteristics help to create the good glomerular filtration capacity of GD chelates<span class="elsevierStyleSup">6</span>&#46; They are small molecules that leave the vascular space quickly&#44; with a half-life in plasma of around 15-30 minutes&#46; They do not cross the blood-brain barrier or the cell membrane&#44; and as such&#44; after leaving the vascular space&#44; they are distributed around the interstitial space&#46; They are eliminated&#44; without being metabolised&#44; through glomerular filtration&#46; In patients with normal renal function&#44; 98&#37; of Gd is eliminated in urine in the first 24 hours<span class="elsevierStyleSup">13</span>&#44; and it is not eliminated from or reabsorbed into the renal tubule<span class="elsevierStyleSup">14</span>&#46; Pharmacokinetic studies have demonstrated its elimination by glomerular filtration&#44; extending the contrast&#8217;s half-life by more than 30 hours but without side effects of nephrotoxicity&#46; In renal failure patients&#44; peritoneal clearance of GBCM was 3&#46;8ml&#47;minute&#47;1&#46;73m<span class="elsevierStyleSup">2</span> with a T1&#47;2 of 52&#46;7 hours&#44; which is not surprising&#44; given the slow clearance of peritoneal dialysis techniques&#46; 75&#37; of doses administered were eliminated by peritoneal dialysis after 5 days and as such&#44; peritoneal dialysis is not an effective technique for eliminating contrast&#46; After two haemodialysis sessions&#44; 95&#37; of the gadolinium dose administered was eliminated but there were no tests of its efficacy in the removing the risk of NSF&#46; However&#44; we recommend that patients on dialysis undergo haemodialysis less than two hours after administration and another haemodialysis session the next day&#46; It is not routinely recommended in non-dialysis patients<span class="elsevierStyleSup">6</span>&#46;</p><p class="elsevierStylePara"><span class="elsevierStyleBold">&#160;</span></p><p class="elsevierStylePara"><span class="elsevierStyleBold">Dose and administration range</span></p><p class="elsevierStylePara">As a gadolinium atom modifies the relaxation times of many neighbouring hydrogen nuclei&#44; the contrast dose used is low&#44; significantly lower than the quantity of iodine administered for computerised tomography studies<span class="elsevierStyleSup">15</span>&#46; The most used commercial preparations have a concentration of 0&#46;5 molar &#40;0&#46;5M&#41;&#44; and as such&#44; the standard administration dose is 0&#46;1mmol&#47;kg of weight&#44; equivalent to 0&#46;2ml&#47;kg of contrast<span class="elsevierStyleSup">4</span>&#46; High doses and increases in the accumulated dose increase the risk of NSF<span class="elsevierStyleSup">6</span>&#46;</p><p class="elsevierStylePara"><span class="elsevierStyleBold">&#160;</span></p><p class="elsevierStylePara"><span class="elsevierStyleBold">NEPHROGENIC SYSTEMIC FIBROSIS</span></p><p class="elsevierStylePara">NSF is an acquired fibrosing disorder that has been observed in patients with severely impaired renal function&#46; Although the term &#8220;nephrogenic systemic fibrosis&#8221; was adopted in 2005&#44; it was recognised for the first time in 1997 and reported in the year 2000 by Cowper as a scleromyxedema-like illness in dialysis patients<span class="elsevierStyleSup">1</span>&#46; In our country&#44; Rodr&#237;quez Jornet et al&#46; published the first case in 2009&#44; with a detailed pathological review of the patient&#44; and the macroscopic and microscopic images are available at&#58; http&#58;&#47;&#47;www&#46;revistanefrologia&#46;com&#47;modules&#46;php&#63;name&#61;articulos&#38;idarticulo&#61;129&#38;idlangart&#61;ES<span class="elsevierStyleSup">16</span>&#46; Table 2 displays the chronology and evolution of the term&#46;</p><p class="elsevierStylePara"><span class="elsevierStyleBold">&#160;</span></p><p class="elsevierStylePara"><span class="elsevierStyleBold">Epidemiology</span></p><p class="elsevierStylePara">NSF affects most cases of patients with impaired renal function&#44; particularly those with an estimated glomerular filtration rate of less than 30ml&#47;min&#47;1&#46;73m<span class="elsevierStyleSup">2</span> independently of the origin of renal damage &#40;acute&#44; chronic or haemodialysis patients&#41;<span class="elsevierStyleSup">2&#44;3</span>&#44; who are administered GBCM&#46; According to Zou et al&#46;&#44; the two most affected groups are patients with chronic renal failure &#40;CRF&#41; on dialysis &#40;85&#37; of cases&#41; and those with acute renal failure<span class="elsevierStyleSup">17</span>&#46; Another patient group that may be affected are those with liver failure who have acute hepatorenal syndrome<span class="elsevierStyleSup">18&#44;19</span>&#46; It is well-known that not all risk patients exposed to GBCM have a disease<span class="elsevierStyleSup">6</span>&#46;</p><p class="elsevierStylePara">NSF is more common in middle-aged patients &#40;50-60 years of age&#41;<span class="elsevierStyleSup">20</span>&#44; although it may affect children and the elderly<span class="elsevierStyleSup">21&#44;22</span>&#46; There are no differences according to race or sex&#44; or any relationship with the cause or duration of CRF<span class="elsevierStyleSup">20</span>&#46;</p><p class="elsevierStylePara">Although various authors have reported different prevalences in accordance with the population selected&#44; it is currently estimated that there is a mean incidence of 0&#37;-18&#37; in the risk population<span class="elsevierStyleSup">23</span>&#46; There is a clear relationship between the dose of GBCM used and the risk of NSF&#44; with there being a NSF incidence close to 0 after an exposure to a standard dose<span class="elsevierStyleSup">15&#44;24</span>&#46; Differences were also reported in the incidence of NSF according to the characteristics of the molecule&#44; with a greater number of cases of NSF having been recorded after exposure to non-ionic linear compounds&#46; As we have mentioned before&#44; it seems that there is a greater risk of incidence in the peritoneal dialysis patient group<span class="elsevierStyleSup">25</span>&#46;</p><p class="elsevierStylePara">Thanks to the knowledge of risk factors and the better use of GBCM&#44; the number of cases of NSF has decreased significantly<span class="elsevierStyleSup">26</span>&#46; Since 2008&#44; there have been no cases of any CM being reported without these CM being replaced<span class="elsevierStyleSup">27</span>&#46; Many hospitals have continued to use the same GBCM but have changed the patterns of use&#46;</p><p class="elsevierStylePara"><span class="elsevierStyleBold">&#160;</span></p><p class="elsevierStylePara"><span class="elsevierStyleBold">Aetiopathogenesis</span></p><p class="elsevierStylePara">Although the exact pathogenesis of NSF continues to be unknown&#44; the only solid association identified in all patients with NSF is renal failure&#44; both in its chronic and acute forms&#44; and its presence is a sine qua non condition for the diagnosis of the disease<span class="elsevierStyleSup">28</span>&#46; However&#44; only a small percentage of the risk population exposed to GBCM develops NSF&#44; and cases of NSF have also been reported without exposure to GBCM<span class="elsevierStyleSup">29</span>&#46;</p><p class="elsevierStylePara">Given that exposure to GBCM does not explain all cases of NSF&#44; other coadjuvant risk factors have been studied that may contribute to its development&#44; many of them associated with situations of renal failure&#46; Pro-inflammatory factors&#58; vessel injury&#44; surgery&#44; thrombosis&#44; procoagulant stages&#44; severe infection&#44; chronic hepatitis C&#44; chronic liver disease and liver transplantation&#44; hyperparathyroidism and hypothyroidism&#46; Biochemical factors&#58; acidosis&#44; intravenous iron&#44; erythropoietin&#44; calcium and phosphorus<span class="elsevierStyleSup">30</span>&#46;</p><p class="elsevierStylePara"><span class="elsevierStyleBold">&#160;</span></p><p class="elsevierStylePara"><span class="elsevierStyleBold">Pathophysiological mechanisms</span></p><p class="elsevierStylePara">The two forms&#44; free Gd ions and the chelate-Gd complex may cause the release of cytokines&#44; stimulating skin macrophages &#40;Gd-free ions&#41; or peripheral blood monocytes &#40;chelate-Gd complexes&#41;&#46; All of these processes &#40;macrophage activation&#44; pro-inflammatory cytokine release&#44; differentiation of fibrocytes in blood&#44; activation of fibroblasts&#44; TGF-&#946; pathways&#44; metallothionein&#44; FGF-23 and Klotho protein&#41; stimulate fibroblasts<span class="elsevierStyleSup">30</span>&#44; a response that creates collagen deposits and fibrosis by increasing transforming growth factor beta 1 levels<span class="elsevierStyleSup">31</span>&#46; The presence of renal failure contributes to the release of free GD3 by increasing transmetalation in a uraemic environment and decreasing the glomerular filtration rate<span class="elsevierStyleSup">32</span>&#46; A complete diagram with pathophysiological mechanisms published by Chopra et al&#46; is available at http&#58;&#47;&#47;www&#46;hindawi&#46;com&#47;journals&#47;ijn&#47;2012&#47;912189&#47;fig1&#47;<span class="elsevierStyleSup">30</span>&#46;&#160;</p><p class="elsevierStylePara"><span class="elsevierStyleBold">&#160;</span></p><p class="elsevierStylePara"><span class="elsevierStyleBold">Diagnosis</span></p><p class="elsevierStylePara">It presents<span class="elsevierStyleBold"> </span><span class="elsevierStyleBold">clinically</span> as a thickening and hardening of the skin&#44; associated with pain&#44; muscle weakness&#44; bone pain and joint contractures&#44; which causes severe disability<span class="elsevierStyleSup">3</span>&#46; Over time there may be loss of flexibility&#44; limited mobility and joint contractures<span class="elsevierStyleSup">2&#44;34</span>&#46; Lesions may appear in the form of plaques &#40;58&#37;&#41; with irregular edges and papules &#40;32&#37;&#41;&#44; nodules &#40;17&#37;&#41;&#44; macules&#44; vesicles&#44; blisters&#44; bullae and ulcers<span class="elsevierStyleSup">2&#44;21&#44;35&#44;36</span>&#46; It typically affects the legs&#44; but may be found anywhere apart from the face in most cases<span class="elsevierStyleSup">35</span>&#46; These skin lesions progress over time to fibrotic skin surrounded by wrinkles&#44; also known as &#8220;orange peel&#8221;<span class="elsevierStyleSup">37</span>&#46; Most lesions are hyperpigmented and erythematous &#40;39&#37;&#41;&#44; but their colour can vary &#40;purple&#44; brown&#44; yellow&#44; pink&#44; orange-red&#44; grey-brown&#41;<span class="elsevierStyleSup">35&#44;38</span>&#46; Sometimes these symptoms can be confused and wrongly treated as cellulitis<span class="elsevierStyleSup">6</span>&#46; Kroshinsky et al&#46; published the case of a 46-year-old woman with CRF&#44; oedema in her legs and skin changes&#44; who was examined and a differential diagnosis was carried out&#44; with macroscopic and microscopic images of the dermis being created<span class="elsevierStyleSup">39</span>&#46; At the time this condition was first reported&#44; scientists thought that it was just a skin disorder&#44; but it is nowadays well-known that it affects joints&#44; the muscular system&#44; the testicles&#44; the kidney&#44; the heart and the dura mater<span class="elsevierStyleSup">31&#44;40&#44;41</span>&#46; Another sign of interest is that it has similar symptoms to conjunctivitis in 75&#37; of cases<span class="elsevierStyleSup">6</span>&#46;</p><p class="elsevierStylePara">The <span class="elsevierStyleBold">onset</span> of symptoms is variable&#59; it generally occurs between two weeks and two months after exposure to GBCM&#46; However&#44; delayed onset has also been reported&#44; years after exposure<span class="elsevierStyleSup">17</span>&#46;</p><p class="elsevierStylePara">The <span class="elsevierStyleBold">histological diagnosis</span> is based on a skin biopsy where skin fibrosis is observed&#44; with thickened collagen bundles and a variable quantity of elastic fibres and mucin&#46; The mediating cell is the circulating fibrocyte &#40;CD34 and positive procollagen I in the immunohistochemistry stain&#41;<span class="elsevierStyleSup">28&#44;42</span>&#46; In most cases&#44; the inflammatory cells are not present and on some occasions&#44; perivascular mononuclear infiltrate has been observed<span class="elsevierStyleSup">43</span>&#46; Sanyal et al&#46; carried out a histological review of a clinical case with an electron microscope and energy dispersive x-ray fluorescence<span class="elsevierStyleSup">44</span><span class="elsevierStyleInf">&#46;</span></p><p class="elsevierStylePara">With regard to its association with GBCM&#44; the first publications are from 2006<span class="elsevierStyleSup">45&#44;46</span>&#44; with the presence of gadolinium in tissues being demonstrated only one year later<span class="elsevierStyleSup">47&#44;48</span>&#46; Under normal conditions&#44; GBCM are eliminated by glomerular filtration in 1-2 days&#46;</p><p class="elsevierStylePara"><span class="elsevierStyleBold">&#160;</span></p><p class="elsevierStylePara"><span class="elsevierStyleBold">Prognosis</span><span class="elsevierStyleBold">&#160;</span></p><p class="elsevierStylePara">The natural outcome of NSF is not fully known&#46; It has been reported that in up to 5&#37; of cases&#44; it may have a fulminant course<span class="elsevierStyleSup">20</span>&#46; A third will have a mild course without functional limitation<span class="elsevierStyleSup">17</span>&#46; There is increased mortality after 24 months of skin manifestations of NSF<span class="elsevierStyleSup">49</span>&#46; The true mortality rate is unknown and is difficult to determine&#44; given the high prevalence of other comorbidities<span class="elsevierStyleSup">34</span>&#46;</p><p class="elsevierStylePara"><span class="elsevierStyleBold">&#160;</span></p><p class="elsevierStylePara"><span class="elsevierStyleBold">Treatment</span></p><p class="elsevierStylePara">There is no evidence of effective treatment and only in transplant patients has an improvement or a detention in the progression of renal disease been achieved in the case of acute renal failure<span class="elsevierStyleSup">50</span>&#46;</p><p class="elsevierStylePara">As mentioned above&#44; GBCM molecular weight allows glomerular filtration<span class="elsevierStyleSup">6 </span>and given these characteristics&#44; there is the possibility of elimination with haemodialysis<span class="elsevierStyleSup">51</span>&#46; Several authors have carried out studies that confirm the elimination of various types of GBCM with three haemodialysis sessions of three hours each&#46; Based on these results&#44; the European Society of Radiology recommends carrying out nine hours of haemodialysis over three sessions&#46; However&#44; gadofosveset is an agent that is difficult to eliminate by haemodialysis due to a large proportion of it being bound to serum albumin<span class="elsevierStyleSup">6</span>&#46; Broome et al&#46; presented a series with three patients who developed NSF despite undergoing the previously indicated haemodialysis sessions<span class="elsevierStyleSup">52</span>&#46; To present&#44; no studies have been carried out on continuous haemofiltration or continuous venovenous haemodiafiltration&#46;</p><p class="elsevierStylePara">Most treatments proposed are still being researched and they are currently yielding suboptimal results &#40;oral steroids&#44; extracorporeal photopheresis&#44; plasmapheresis&#44; thalidomide&#44; cyclophosphamide&#44; pentoxifylline&#44; intravenous immunoglobulin&#44; interferon alpha and vitamin D&#44; ultraviolet radiation and etanercept&#41;<span class="elsevierStyleSup">20</span>&#46; Recently&#44; combined treatments with imatinib and extracorporeal photopheresis have been attempted<span class="elsevierStyleSup">53&#44;54</span>&#46; The efficacy of treatment with alefacept was also confirmed in three patients with NSF<span class="elsevierStyleSup">55</span>&#46; The improvement in renal function &#40;transplantation and resolution of acute renal failure&#41; may slow down and even reverse the process<span class="elsevierStyleSup">20</span>&#46; However&#44; in reality&#44; no treatment has shown to be effective&#59; therefore&#44; prevention is important&#46;</p><p class="elsevierStylePara"><span class="elsevierStyleBold">&#160;</span></p><p class="elsevierStylePara"><span class="elsevierStyleBold">PREVENTION OF NEPHROGENIC SYSTEMIC FIBROSIS</span></p><p class="elsevierStylePara"><span class="elsevierStyleBold">Identification of patients with chronic kidney disease</span></p><p class="elsevierStylePara">The classification of chronic kidney disease &#40;CKD&#41; followed the initial publication of the National Kidney Foundation through the Kidney Disease Outcomes Quality Initiative &#40;K-DOQI&#41; guidelines<span class="elsevierStyleSup">56</span>&#46; The definition of CKD by K-DOQI is as follows&#58;</p><p class="elsevierStylePara">Renal damage for at least three months&#44; defined by structural or functional abnormalities of the kidney or without a decrease in the GFR and shown by pathological changes or renal damage markers &#40;changes in the composition of blood or urine or changes in images of the kidney&#41;&#46;</p><p class="elsevierStylePara">GFR&#160;&#60;60ml&#47;min&#47;1&#46;73m<span class="elsevierStyleSup">2</span> for more than three months&#44; with or without renal damage&#46;</p><p class="elsevierStylePara">It is common in consultations for renal function to be studied simply by measuring serum creatinine &#40;SCr&#41;&#46; However&#44; and although it is true that SCr is a good follow-up parameter of the evolution of filtration&#44; it is not always equivalent to glomerular filtration&#46; SCr also depends on factors other than the GFR&#44; such as tubular elimination and the generation and extrarenal elimination of creatinine&#44; which explains the wide range for SCr in healthy individuals&#46; Some studies<span class="elsevierStyleSup">57 </span>show a high percentage of males and particularly of females who have reductions in the GFR with normal SCr&#46; Even with creatinine ranges between 1&#46;3 and 2&#46;5mg&#47;dl&#44; there are significant percentages of very severe renal failure &#40;GFR below 30ml&#47;min&#47;1&#46;73m<span class="elsevierStyleSup">2</span>&#41;&#46; Therefore&#44; the real prevalence of individuals with renal failure appears to be higher than that which can be determined by studying SCr&#46; The results of these observations are important&#46; This &#8220;hidden&#8221; renal failure may easily worsen due to the large amount of medications&#44; particularly in glomerular haemodynamics&#44; such as non-steroidal anti-inflammatory drugs&#44; angiotensin-converting-enzyme inhibitors and other types of drugs&#46; Likewise&#44; patients often undergo x-ray examinations when there is an inadequate evaluation of renal function&#44; based only on plasma creatinine&#46;</p><p class="elsevierStylePara">The international organisation KDIGO &#40;Kidney Disease Global Outcomes&#59; http&#58;&#47;&#47;www&#46;kdigo&#46;org&#47;&#41; recommends using prediction equations to calculate the GFR based on SCr&#46; In adults&#44; the formulas most used are those of the Modification of Diet in Renal Disease &#40;MDRD&#41; study and that of Cockcroft and Gault<span class="elsevierStyleSup">58</span>&#46; There are certain circumstances in which the first is not validated &#40;Table 3&#41; and in order to estimate the GFR&#44; 24-hour urine should be collected or studies of creatinine clearance in 24-hour urine&#44; iothalamate&#44; iohexol or insulin should be carried out&#46; In any case&#44; the estimation of GFR using the MDRD formula is more accurate that SCr&#44; and considering these limitations&#44; the doctor may obtain valid information about renal function&#46; Recently&#44; KDIGO recommended a new formula for calculating renal function&#44; called CKD-EPI &#40;Chronic Kidney Disease Epidemiology Collaboration&#41;&#44; which is more accurate than MDRD for values close to 60ml&#47;min<span class="elsevierStyleSup">59</span>&#46; Likewise&#44; it updated the CKD classification by incorporating the CGA concept&#58; C&#58; cause of CKD&#44; G&#58; GFR incorporating groups 3a and 3b&#44; and A&#58; albuminuria with three subgroups&#58; A1 &#40;&#60;30mg&#47;g of creatinine&#41;&#44; A2 &#40;30-300&#41; and A3 &#40;&#62;300&#41;<span class="elsevierStyleSup">60</span> &#40;Table 4&#41;&#46;</p><p class="elsevierStylePara">There are occasionally no data on renal function&#46; In patients who have unknown renal function and who require an x-ray examination with gadolinium&#44; a series of parameters should be considered&#44; such as renal failure risk factors&#44; which will mean that the examination must be delayed until their exact renal function is known &#40;Table 5&#41;&#46; The study of risk factors must be part of the routine before using GBCM in any hospital&#46;</p><p class="elsevierStylePara"><span class="elsevierStyleBold">&#160;</span></p><p class="elsevierStylePara"><span class="elsevierStyleBold">IMMEDIATE ADVERSE REACTIONS TO GADOLINIUM-BASED CONTRAST MEDIA</span></p><p class="elsevierStylePara"><span class="elsevierStyleBold">GBCM are very safe drugs&#44; with a low immediate adverse reaction &#40;IAR&#41; rate of 0&#46;07&#37;-2&#46;4&#37;<span class="elsevierStyleSup">61-63</span>&#44; mostly of a mild nature&#44; mainly nausea or headaches at the time of injection&#46;</span></p><p class="elsevierStylePara">Although all GBCM show quite a similar IAR incidence<span class="elsevierStyleSup">64</span>&#44; there are differences in their occurrence that cannot seem to be explained by their physicochemical characteristics<span class="elsevierStyleSup">65&#44;66 </span>&#40;Table 6&#41;&#46;</p><p class="elsevierStylePara">Among IAR to GBCM&#44; we must highlight allergic reactions&#44; due to their relevance&#44; which are defined as a type of adverse reaction measured immunologically by antibodies or lymphocytes&#44; characterised by being specific and recurrent if the patient is exposed to the drug again<span class="elsevierStyleSup">67</span>&#46; Two types of allergic reaction to x-ray contrast media are distinguished depending on the moment of presentation&#58; immediate and non-immediate or delayed<span class="elsevierStyleSup">68</span>&#46; Immediate allergic reactions are measured by immunoglobin E&#59; if a systemic allergic reaction develops&#44; there is anaphylaxis&#46; This is caused by the release of histamines and other mediators&#44; causing symptoms that may put the life of the patients at risk&#58; laryngeal oedema&#44; angioedema&#44; upper airway obstruction&#44; urticarial&#44; nausea&#44; vomiting&#44; low blood pressure and&#47;or shock&#46;</p><p class="elsevierStylePara">The occurrence of allergic reactions to GBCM is unpredictable&#44; although it is known that its incidence increases in asthmatic patients and in those with food allergies and&#47;or medication allergies<span class="elsevierStyleSup">58&#44;69</span>&#46;</p><p class="elsevierStylePara">With regards to how to act against an allergic reaction to a GBCM&#44; Figure 1 displays an algorithm&#44; which schematically shows how to manage these emergency situations in the x-ray diagnosis department&#46;</p><p class="elsevierStylePara"><span class="elsevierStyleBold">&#160;</span></p><p class="elsevierStylePara"><span class="elsevierStyleBold">LEARN FROM EVIDENCE</span></p><p class="elsevierStylePara"><span class="elsevierStyleBold">Clinical use and abuse</span></p><p class="elsevierStylePara">Since the introduction of GBCM in MRI&#44; its applications have been increasing daily&#44; and it is now used in all organs of the body&#46; During the first few years&#44; a false sense of security was created&#44; which led to an overenthusiastic use of GBCM&#44; which were often used as replacements for iodinated contrasts in computerised tomography or conventional angiography studies in patients who were allergic to iodinated contrasts or in those with renal failure and even in MRI&#44; at doses much higher than those recommended&#46;</p><p class="elsevierStylePara">This use of GBCM&#44; before NSF was reported&#44; was carried out without any type of control in terms of dose or administration times and without taking any precautions in relation to the renal function of patients&#46;</p><p class="elsevierStylePara">The reporting of this delayed and potentially serious adverse reaction marked a turning point that forced x-ray departments to establish new guidelines aimed at protecting patients&#46; Although the initial information may have been confusing&#44; some evidence was clear and shed light with regard to the measures to adopt to prevent disease&#58; it was only reported in patients with severe renal failure &#40;GFR&#60;30&#41;&#44; its incidence was related to the administration of high doses of gadolinium and it was more common in patients with pro-inflammatory symptoms&#46;</p><p class="elsevierStylePara"><span class="elsevierStyleBold">&#160;</span></p><p class="elsevierStylePara"><span class="elsevierStyleBold">Clinical limitations in the use of gadolinium-based contrast media </span></p><p class="elsevierStylePara">The main limitation with regard to the use of GBCM in MRI is the difficulty of knowing the GFR of patients&#44; particularly outpatients&#46; In this regard&#44; collaboration between the x-ray department&#44; which would have to routinely record renal failure risk factors &#40;Table 4&#41; before carrying out the GBCM study&#44; and the doctor who requests the test&#44; who must provide information about the patient&#8217;s renal function and assess the risk&#47;benefit of the test requested for the patient&#46; If any of the risk factors of renal failure are confirmed or the GFR of the patient cannot be excluded or assessed&#44; it would be preferable to postpone it until MDRD or CKD-EPI are determined in another test&#46;</p><p class="elsevierStylePara">Since gadolinium has been considered an agent the potentially causes NSF&#44; restrictive guidelines have been designed for its administration &#40;Table 7&#41;&#44; with the most important aspects being the possession of recent GFR data and the adjustment of doses used in accordance with the latter &#40;Table 8&#41;&#46;</p><p class="elsevierStylePara">In 2010&#44; the U&#46;S&#46; Food and Drug Administration &#40;FDA&#41; established general precautions on the use of GBCM and limited Magnevist<span class="elsevierStyleSup">&#174;</span>&#44; Omniscan<span class="elsevierStyleSup">&#174;</span> and Optimark<span class="elsevierStyleSup">&#174; </span>GBCM in patients with acute renal failure and high-risk severe CRF<span class="elsevierStyleSup">43</span>&#46; Two years after the recommendations carried out by the FDA&#44; a 71&#37; decrease was observed in MRI in patients with MDRD 30ml&#47;min&#47;1&#46;73m<span class="elsevierStyleSup">2 </span>and a 99&#37; increase was observed in requests for SCr a month before carrying out MRI<span class="elsevierStyleSup">70</span>&#46; A year before&#44; the European Medicines Agency also contraindicated the use of the aforementioned GBCM in patients with severe renal failure&#44; infants and those awaiting liver transplantation<span class="elsevierStyleSup">43</span>&#46; According to Bennet et al&#46;&#44; in Denmark since 2007 and in the United States since 2009&#44; no new cases of NSF have been published<span class="elsevierStyleSup">71</span>&#46;</p><p class="elsevierStylePara">The possibility of this adverse reaction occurring should not limit clinical action&#46; It is essential to find a balance between the guarantee of patient safety and the carrying out of the tests necessary for correct clinical management&#46; As such&#44; the need for a test and its effectiveness will be discussed clinically&#44; and other diagnostic options will be taken into account&#44; as well as alternative contrasts&#46; In short&#44; the risk&#47;benefit will be weighed up&#46;</p><p class="elsevierStylePara"><span class="elsevierStyleBold">&#160;</span></p><p class="elsevierStylePara"><span class="elsevierStyleBold">CONCLUSIONS</span></p><p class="elsevierStylePara">GBCM are a group of drugs with differentiated physiochemical characteristics that are increasingly being used in diagnosis by MRI&#46;</p><p class="elsevierStylePara">Due to the fact that they were initially used without taking patients&#8217; renal function into account&#44; and without an exact knowledge of the toxic doses permitted&#44; a series of adverse effects appeared&#44; and in particular&#44; the predominantly dermatological multiple organ fibrosing disorder subsequently known as NSF&#44; which discredited its use&#46;</p><p class="elsevierStylePara">The reporting of this delayed and potentially severe adverse reaction marked a turning point&#44; since it made it compulsory to establish consensuses to protect patients by assessing the GFR and risk factors&#46; All of this along with dose adjustment have decreased the number of adverse reactions significantly and in the last five years there have hardly been any published cases with the use of gadolinium&#46;</p><p class="elsevierStylePara">As for IAR&#44; all GBCM have a low and similar incidence&#44; although there are some differences between them&#44; with gadodiamide having the lowest incidence<span class="elsevierStyleSup">63&#44;64&#44;67</span>&#46; These reactions&#44; although they are generally mild&#44; can occasionally be severe and even fatal&#46;</p><p class="elsevierStylePara">Patient protection is key when GBCM are used in x-rays&#46; The identification and selection of patients at risk&#44; the assessment of the risk and benefit and informing the patient about the adverse effects are essential&#46;</p><p class="elsevierStylePara">In most cases&#44; it is necessary to assess the patient&#44; make a multidisciplinary decision&#44; and in particular&#44; treat every case individually&#46;</p><p class="elsevierStylePara"><span class="elsevierStyleBold">&#160;</span></p><p class="elsevierStylePara"><span class="elsevierStyleBold">Conflicts of interest</span></p><p class="elsevierStylePara">The content of this review is based on an update of Working Session presentations sponsored by GE Healthcare entitled <span class="elsevierStyleBold">What happened to NSF&#63; The current situation</span>&#44; which took place at the XXXI SERAM Conference &#40;Granada&#44; 2012&#41;&#46; The publication of this review was carried out independently of the Working Session sponsor&#46;</p><p class="elsevierStylePara"><a href="grande&#47;12375&#95;19904&#95;59997&#95;en&#95;12375&#95;f1&#46;jpg" class="elsevierStyleCrossRefs"><img src="12375_19904_59997_en_12375_f1.jpg" alt="Classification of the different gadolinium-based contrasts according to their distribution "></img></a></p><p class="elsevierStylePara">Table 1&#46; Classification of the different gadolinium-based contrasts according to their distribution </p><p class="elsevierStylePara"><a href="grande&#47;12375&#95;16025&#95;59998&#95;en&#95;t2&#95;copy1&#46;jpg" class="elsevierStyleCrossRefs"><img src="12375_16025_59998_en_t2_copy1.jpg" alt="Chronology and evolution of the term &#38;"></img></a></p><p class="elsevierStylePara">Table 2&#46; Chronology and evolution of the term &#38;</p><p class="elsevierStylePara"><a href="grande&#47;12375&#95;16025&#95;59999&#95;en&#95;t3&#95;copy1&#46;jpg" class="elsevierStyleCrossRefs"><img src="12375_16025_59999_en_t3_copy1.jpg" alt="Circumstances in which the MDRD &#40;Modification of Diet in Renal Disease&#41; equation is not valid for calculating the glomerular filtration rate "></img></a></p><p class="elsevierStylePara">Table 3&#46; Circumstances in which the MDRD &#40;Modification of Diet in Renal Disease&#41; equation is not valid for calculating the glomerular filtration rate </p><p class="elsevierStylePara"><a href="grande&#47;12375&#95;16025&#95;60000&#95;en&#95;t4&#95;copy1&#46;jpg" class="elsevierStyleCrossRefs"><img src="12375_16025_60000_en_t4_copy1.jpg" alt="Classification of chronic kidney disease &#40;57&#41;"></img></a></p><p class="elsevierStylePara">Table 4&#46; Classification of chronic kidney disease &#40;57&#41;</p><p class="elsevierStylePara"><a href="grande&#47;12375&#95;16025&#95;60001&#95;en&#95;t5&#95;copy1&#46;jpg" class="elsevierStyleCrossRefs"><img src="12375_16025_60001_en_t5_copy1.jpg" alt="Chronic kidney disease risk factors "></img></a></p><p class="elsevierStylePara">Table 5&#46; Chronic kidney disease risk factors </p><p class="elsevierStylePara"><a href="grande&#47;12375&#95;16025&#95;60002&#95;en&#95;t6&#95;copy1&#46;jpg" class="elsevierStyleCrossRefs"><img src="12375_16025_60002_en_t6_copy1.jpg" alt="Percentage of immediate adverse reactions to gadolinium-based contrast media "></img></a></p><p class="elsevierStylePara">Table 6&#46; Percentage of immediate adverse reactions to gadolinium-based contrast media </p><p class="elsevierStylePara"><a href="grande&#47;12375&#95;16025&#95;60003&#95;en&#95;t7&#95;copy1&#46;jpg" class="elsevierStyleCrossRefs"><img src="12375_16025_60003_en_t7_copy1.jpg" alt="Measures to avoid nephrogenic systemic fibrosis development "></img></a></p><p class="elsevierStylePara">Table 7&#46; Measures to avoid nephrogenic systemic fibrosis development </p><p class="elsevierStylePara"><a href="grande&#47;12375&#95;16025&#95;60004&#95;en&#95;t8&#95;copy1&#46;jpg" class="elsevierStyleCrossRefs"><img src="12375_16025_60004_en_t8_copy1.jpg" alt="Administration of gadolinium adjusted to renal function "></img></a></p><p class="elsevierStylePara">Table 8&#46; Administration of gadolinium adjusted to renal function </p><p class="elsevierStylePara"><a href="grande&#47;12375&#95;16025&#95;60005&#95;en&#95;f1&#95;copy2&#46;jpg" class="elsevierStyleCrossRefs"><img src="12375_16025_60005_en_f1_copy2.jpg" alt="Protocol for treating adverse reactions to gadolinium&#46;"></img></a></p><p class="elsevierStylePara">Figure 1&#46; Protocol for treating adverse reactions to gadolinium&#46;</p>"
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        "resumen" => "<p class="elsevierStylePara">La fibrosis sist&#233;mica nefrog&#233;nica es un trastorno fibrosante que afecta a pacientes con deterioro de la funci&#243;n renal y se asocia a la administraci&#243;n de medios de contraste basados en el gadolinio&#44; empleados en la resonancia magn&#233;tica&#46; A pesar de tratarse de un grupo de f&#225;rmacos que se consideraban seguros&#44; la notificaci&#243;n de esta reacci&#243;n adversa&#44; potencialmente grave&#44; supuso un punto de inflexi&#243;n en las pautas de administraci&#243;n de estos medios de contraste&#46; Se han intentado establecer par&#225;metros de seguridad a fin de identificar a los pacientes con factores de riesgo por presentar insuficiencia renal&#46; La estrecha farmacovigilancia y el rigor en la observaci&#243;n de las normativas actuales&#44; con especial atenci&#243;n al valor del filtrado glomerular&#44; han reducido los casos publicados relacionados con el uso de medios de contraste basados en el gadolinio&#46; En un encuentro entre radi&#243;logos y nefr&#243;logos revisamos los aspectos m&#225;s relevantes en la actualidad y las recomendaciones para su prevenci&#243;n&#46;</p>"
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        "resumen" => "<p class="elsevierStylePara">Nephrogenic systemic fibrosis is a fibrosing disorder that affects patients with impaired renal function and is associated with the administration of gadolinium-based contrast media used in MRI&#46; Despite being in a group of drugs that were considered safe&#44; report about this potentially serious adverse reaction was a turning point in the administration guidelines of these contrast media&#46; There has been an attempt to establish safety parameters to identify patients with risk factors of renal failure&#46; The close pharmacovigilance and strict observation of current regulations&#44; with special attention being paid to the value of glomerular filtration&#44; have reduced the published cases involving the use of gadolinium-based contrast media&#46; In a meeting between radiologists and nephrologists we reviewed the most relevant aspects currently and recommendations for its prevention&#46;</p>"
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Article information

ISSN: 20132514
Original language: English

DOI:10.3265/Nefrologia.pre2014.Apr.12375

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Year/Month	Html	Pdf	Total

2024 November	7	0	7
2024 October	111	55	166
2024 September	135	86	221
2024 August	105	87	192
2024 July	104	47	151
2024 June	151	63	214
2024 May	272	59	331
2024 April	87	68	155
2024 March	117	33	150
2024 February	91	57	148
2024 January	79	50	129
2023 December	85	35	120
2023 November	116	69	185
2023 October	141	117	258
2023 September	111	130	241
2023 August	83	39	122
2023 July	95	77	172
2023 June	84	55	139
2023 May	85	60	145
2023 April	66	48	114
2023 March	89	42	131
2023 February	99	37	136
2023 January	74	42	116
2022 December	105	48	153
2022 November	99	67	166
2022 October	97	89	186
2022 September	111	61	172
2022 August	96	55	151
2022 July	85	73	158
2022 June	68	62	130
2022 May	111	50	161
2022 April	67	51	118
2022 March	99	53	152
2022 February	118	58	176
2022 January	93	53	146
2021 December	108	56	164
2021 November	88	61	149
2021 October	65	73	138
2021 September	80	63	143
2021 August	78	62	140
2021 July	70	49	119
2021 June	66	44	110
2021 May	81	66	147
2021 April	219	101	320
2021 March	90	69	159
2021 February	128	52	180
2021 January	84	29	113
2020 December	54	28	82
2020 November	83	25	108
2020 October	63	28	91
2020 September	65	30	95
2020 August	77	28	105
2020 July	72	18	90
2020 June	76	37	113
2020 May	89	19	108
2020 April	55	27	82
2020 March	86	22	108
2020 February	86	30	116
2020 January	103	29	132
2019 December	117	34	151
2019 November	74	12	86
2019 October	74	12	86
2019 September	108	15	123
2019 August	88	25	113
2019 July	90	32	122
2019 June	91	35	126
2019 May	214	20	234
2019 April	166	38	204
2019 March	91	44	135
2019 February	76	37	113
2019 January	61	26	87
2018 December	274	48	322
2018 November	275	43	318
2018 October	228	34	262
2018 September	486	30	516
2018 August	232	29	261
2018 July	195	31	226
2018 June	185	29	214
2018 May	252	19	271
2018 April	232	19	251
2018 March	228	13	241
2018 February	154	12	166
2018 January	169	13	182
2017 December	201	15	216
2017 November	176	17	193
2017 October	170	30	200
2017 September	151	12	163
2017 August	142	25	167
2017 July	184	17	201
2017 June	217	16	233
2017 May	307	23	330
2017 April	172	27	199
2017 March	222	28	250
2017 February	332	18	350
2017 January	156	21	177
2016 December	180	23	203
2016 November	281	34	315
2016 October	384	39	423
2016 September	742	49	791
2016 August	900	42	942
2016 July	495	23	518
2016 June	311	0	311
2016 May	313	0	313
2016 April	357	0	357
2016 March	289	0	289
2016 February	310	0	310
2016 January	298	0	298
2015 December	264	0	264
2015 November	270	0	270
2015 October	273	0	273
2015 September	238	0	238
2015 August	216	0	216
2015 July	295	0	295
2015 June	170	0	170
2015 May	225	0	225
2015 April	52	0	52

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