Inflammatory response caused by larvae and adults of Gnathostoma (Nematoda: Gnathostomatidae) in vertebrates of Mexico, including humans
Respuesta inflamatoria ocasionada por larvas y adultos de Gnathostoma (Nematoda: Gnathostomatidae) en vertebrados de México, incluyendo al hombre
Luis Jorge García-Márquez1, Virginia León-Règagnon2, Rafael Lamothe-Argumedo3, David Osorio-Sarabia3, Luis García-Prieto3
1 Centro Universitario de Investigación y Desarrollo Agropecuario (CUIDA), Universidad de Colima. Av. Universidad #333, Col. de las Víboras, 28040 Colima, Colima, México.
2 Estación de Biología Chamela, Instituto de Biología, Universidad Nacional Autónoma de México. Apartado postal 21, 48980 San Patricio, Jalisco, México.
3 Laboratorio de Helmintología, Instituto de Biología, Universidad Nacional Autónoma de México. Apartado postal 70-153, 04510 México, D. F., México.
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Av. Universidad #333, Col. de las Víboras, 28040 Colima, Colima, México." "etiqueta" => "1" "identificador" => "aff0005" ] 1 => array:3 [ "entidad" => "Estación de Biología Chamela, Instituto de Biología, Universidad Nacional Autónoma de México. Apartado postal 21, 48980 San Patricio, Jalisco, México." "etiqueta" => "2" "identificador" => "aff0010" ] 2 => array:3 [ "entidad" => "Laboratorio de Helmintología, Instituto de Biología, Universidad Nacional Autónoma de México. Apartado postal 70-153, 04510 México, D. F., México." "etiqueta" => "3" "identificador" => "aff0015" ] ] ] ] "titulosAlternativos" => array:1 [ "en" => array:1 [ "titulo" => "Respuesta inflamatoria ocasionada por larvas y adultos de <span class="elsevierStyleItalic">Gnathostoma</span> (Nematoda: Gnathostomatidae) en vertebrados de México, incluyendo al hombre" ] ] "resumenGrafico" => array:2 [ "original" => 0 "multimedia" => array:7 [ "identificador" => "fig0005" "etiqueta" => "Figure 1" "tipo" => "MULTIMEDIAFIGURA" "mostrarFloat" => true "mostrarDisplay" => false "figura" => array:1 [ 0 => array:4 [ "imagen" => "gr1.jpeg" "Alto" => 885 "Ancho" => 1406 "Tamanyo" => 244804 ] ] "descripcion" => array:1 [ "es" => "<p id="spar0005" class="elsevierStyleSimplePara elsevierViewall">Skeletal muscle (me) of fish (<span class="elsevierStyleItalic">Petenia splendida</span>) with parasitic cyst (qp) and larva (A<span class="elsevierStyleInf">3</span>L) of <span class="elsevierStyleItalic">Gnathostoma</span> sp., encapsulated by connective tissue (category I lesion). Hematoxylin -eosin staining. Scale bar 100<span class="elsevierStyleHsp" style=""></span>μm.</p>" ] ] ] "textoCompleto" => "<span class="elsevierStyleSections"><span id="sec0005" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0025">Introduction</span><p id="par0005" class="elsevierStylePara elsevierViewall"><span class="elsevierStyleItalic">Gnathostoma</span> is represented in Mexico by 3 species: <span class="elsevierStyleItalic">Gnathostoma binucleatum</span> Almeyda-Artigas, 1991, <span class="elsevierStyleItalic">Gnathostoma lamothei</span><a class="elsevierStyleCrossRef" href="#bib0025">Bertoni-Ruiz, García-Prieto, Osorio-Sarabia and León-Règagnon, 2005</a>, and <span class="elsevierStyleItalic">Gnathostoma turgidum</span> Stossich, 1902; its geographic distribution comprises 15 of the 32 states of the Mexican territory, and it parasitizes 80 host species (<a class="elsevierStyleCrossRef" href="#bib0125">Pérez-Álvarez et al., 2008</a>; <a class="elsevierStyleCrossRef" href="#bib0055">García-Márquez et al., 2009</a>). Additionally, more than 8 000 cutaneous and 11 ocular human cases have been recorded in this country (<a class="elsevierStyleCrossRef" href="#bib0075">Lamothe-Argumedo, 2003</a>, <a class="elsevierStyleCrossRef" href="#bib0080">2006</a>), with <span class="elsevierStyleItalic">G. binucleatum</span> being the only species confirmed as an ethiological agent in Mexican human infections (<a class="elsevierStyleCrossRef" href="#bib0090">León-Règagnon et al., 2002</a>).<a name="p430"></a></p><p id="par0010" class="elsevierStylePara elsevierViewall">Histopathology caused by adult worms of this genus has been described in several regions of the world for several host species including dogs (<a class="elsevierStyleCrossRef" href="#bib0110">Nayar et al., 1978</a>), cats (<a class="elsevierStyleCrossRef" href="#bib0030">Beveridge et al., 1998</a>), weasels (<a class="elsevierStyleCrossRef" href="#bib0015">Ashizawa et al., 1979</a>), and pigs and boars (<a class="elsevierStyleCrossRef" href="#bib0100">Mei et al., 2001</a>), among others. In contrast, pathogenic changes by advanced third stage larvae (A<span class="elsevierStyleInf">3</span>L) of <span class="elsevierStyleItalic">Gnathostoma</span> have only been studied in fish-eating birds (<a class="elsevierStyleCrossRef" href="#bib0050">García-Márquez et al., 2001</a>). In humans, histological lesions have been described in skin (<a class="elsevierStyleCrossRef" href="#bib0115">Ollague and Ollague, 1987</a>), brain (<a class="elsevierStyleCrossRef" href="#bib0140">Schmutzhard et al., 1988</a>), eyes (<a class="elsevierStyleCrossRef" href="#bib0020">Barua et al., 2007</a>), and intestine (<a class="elsevierStyleCrossRef" href="#bib0145">Seguchi et al., 1995</a>). The main objective of this study is to describe and compare the histological lesions caused by A<span class="elsevierStyleInf">3</span>L and adults of <span class="elsevierStyleItalic">Gnathostoma</span> sp., in several vertebrate host species including humans.</p></span><span id="sec0010" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0030">Materials and methods</span><p id="par0015" class="elsevierStylePara elsevierViewall">Nine species of wild vertebrates (2 fish, 1 amphibian, 1 reptile, 3 birds, and 2 mammals, all in adult stage) were obtained from 9 localities from Mexico between June 2004 and September 2005 (<a class="elsevierStyleCrossRef" href="#tbl0005">Table 1</a>). One larva was obtained from a skin biopsy conducted on a human adult patient in the General Hospital from Tepic (Secretaría de Salud del Estado de Nayarit) in 2000. Fish were collected with a seine net, amphibians were collected manually, and reptiles, birds, and mammals were shot by local hunters. All organisms were collected under the scientific collection permit FAUT-0056 issued to VLR. Skeletal muscles of all vertebrates except the mammals were ground individually, compressed between 2 glass plates, and examined with the aid of a magnifying glass to search for A<span class="elsevierStyleInf">3</span>L of <span class="elsevierStyleItalic">Gnathostoma</span>. The digestive tract and liver of mammals were dissected within 4<span class="elsevierStyleHsp" style=""></span>hr after capture, and reviewed under the microscope. Histologic lesions were evaluated based on 1 larva (alive or degenerating) or 1 live adult in host tissue. The positive tissues were fixed in 10% formaldehyde buffered solution (pH<span class="elsevierStyleHsp" style=""></span>=<span class="elsevierStyleHsp" style=""></span>7.2) during 24<span class="elsevierStyleHsp" style=""></span>hr, and processed following conventional histologic techniques (<a class="elsevierStyleCrossRef" href="#bib0130">Prophet et al., 1992</a>). Five cross sections 6<span class="elsevierStyleHsp" style=""></span>μm thick were made for each host species, and 10 microscopic fields were analyzed for each section following <a class="elsevierStyleCrossRef" href="#bib0155">Vivar-Díaz (2010)</a>. Observations were made with a Carl Zeiss Primo star 07745 microscope (10x and 40x). Classification of the lesions follows the criteria proposed by <a class="elsevierStyleCrossRef" href="#bib0150">Vázquez-Núñez et al. (2004)</a> (<a class="elsevierStyleCrossRef" href="#tbl0010">Table 2</a>). Voucher specimens of representative histological sections were deposited at the Colección Nacional de Helmintos (CNHE), Instituto de Biología, UNAM, Mexico City (CNHE 8739-8743).</p><elsevierMultimedia ident="tbl0005"></elsevierMultimedia><elsevierMultimedia ident="tbl0010"></elsevierMultimedia></span><span id="sec0015" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0035">Results</span><p id="par0020" class="elsevierStylePara elsevierViewall">The presence of live larvae encysted in skeletal muscle of fishes, amphibians, and reptiles caused histological lesions ranging from mild hyperplasia of fibrous connective tissue around the parasite (lesions category I) to moderate hyperplasia of this tissue with infiltration of macrophages and heterophils in the interstitial zone, at levels below 50% (category II) (<a class="elsevierStyleCrossRef" href="#fig0005">Fig. 1</a>). In birds, inflammatory response in muscle tissue included moderate to severe hyperplasia of fibrous connective tissue around the parasite, as well as infiltration of macrophages, heterophils (eosinophils), lymphocytes and mononuclear cells, at levels above 50% causing degeneration and necrosis of muscle fibers with vasculitis (categories II, III) (<a class="elsevierStyleCrossRef" href="#fig0010">Fig. 2</a>). In the most severe cases, granulomatous lesions were recorded, with<a name="p431"></a> degeneration of the parasite, severe hyperplasia of fibrous connective tissue, and infiltration of epithelioid cells, giant cells, fibroblasts, and occasionally heterophils (eosinophils) (category IV). Inflammatory reaction in human skin was characterized by a moderate to severe hyperplasia of fibrous connective tissue surrounding the parasite, infiltration of macrophages, heterophils (eosinophils), lymphocytes and mononuclear cells, at levels above 50%, as well as degeneration and necrosis of muscle fibers with vasculitis. At the epidermic level, necrosis, acanthosis and hyperkeratosis were present, while in the dermis, infiltration of lymphocytes, eosinophils, macrophages, and plasmatic cells was recorded, producing an eosinophilic migratory panniculits (categories III and IV), without encysting of the A<span class="elsevierStyleInf">3</span>L of <span class="elsevierStyleItalic">Gnathostoma</span> spp. (<a class="elsevierStyleCrossRef" href="#fig0015">Fig. 3</a>).</p><elsevierMultimedia ident="fig0005"></elsevierMultimedia><elsevierMultimedia ident="fig0010"></elsevierMultimedia><elsevierMultimedia ident="fig0015"></elsevierMultimedia><p id="par0025" class="elsevierStylePara elsevierViewall">Adults collected in the stomachs of opossums and raccoons caused lesions of categories III and IV; these specimens also exhibited congestion, hemorrhages, and mineralization (<a class="elsevierStyleCrossRef" href="#fig0020">Figs. 4</a>, <a class="elsevierStyleCrossRef" href="#fig0025">5</a>).</p><elsevierMultimedia ident="fig0020"></elsevierMultimedia><elsevierMultimedia ident="fig0025"></elsevierMultimedia></span><span id="sec0020" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0040">Discussion</span><p id="par0030" class="elsevierStylePara elsevierViewall">In this study, we analyzed and compared the inflammatory reaction caused by larvae and adults of the<a name="p432"></a> 3 species of <span class="elsevierStyleItalic">Gnathostoma</span> distributed in Mexico, i.e., <span class="elsevierStyleItalic">G. binucleatum</span> (adult in <span class="elsevierStyleItalic">Leopardus pardalis), G. lamothei</span> (adult in <span class="elsevierStyleItalic">Procyon lotor hernandezi</span>), and <span class="elsevierStyleItalic">G. turgidum</span> (adults in <span class="elsevierStyleItalic">Didelphis</span> spp., and <span class="elsevierStyleItalic">Philander opossum</span>). The specific identity of larvae found in fish, amphibians, reptiles, and birds could not be determined due to lack of morphometric traits in histological cross sections.</p><p id="par0035" class="elsevierStylePara elsevierViewall">The inflammatory reaction and lesions caused by A<span class="elsevierStyleInf">3</span>L and adults of <span class="elsevierStyleItalic">Gnathostoma</span> spp., in all of the 10 vertebrate host species studied, including 1 human, are a complex response to the presence of the parasite, resulting in very different tissue alterations (categories I-IV, see <a class="elsevierStyleCrossRef" href="#tbl0010">Table 2</a>). The A<span class="elsevierStyleInf">3</span>L of <span class="elsevierStyleItalic">Gnathostoma</span> sp. found in fish, amphibians, and reptiles causes a minimal response in these 3 hosts groups, because of the encystment of the A<span class="elsevierStyleInf">3</span>L in the skeletal muscle; this suggests an acute infection without tissue reaction by the host, allowing parasite survival and thus, continuation of its life cycle (<a class="elsevierStyleCrossRef" href="#bib0070">Lamothe-Argumedo, 1997</a>). In the bird species studied, the more frequent lesion categories correspond to II, III and IV, which agree with the findings of <a class="elsevierStyleCrossRef" href="#bib0050">García-Márquez et al. (2001)</a> in the same group of hosts. This inflammatory reaction is due to the number of larvae involved in the infection and to the role of birds as paratenic hosts of <span class="elsevierStyleItalic">Gnathostoma</span> larvae, accumulating a large number of nematodes through time (<a class="elsevierStyleCrossRef" href="#bib0085">León-Règagnon et al., 2005</a>).</p><p id="par0040" class="elsevierStylePara elsevierViewall">The initial inflammatory and immunological response caused by the parasite is acute; it is characterized by cellular infiltration of eosinophils and neutrophils (heterophils in birds, fishes, and reptiles) with phagocytic action and release of cytosine, leukotrienes, prostaglandins, etc. The release of chemical substances activates the cellular and humoral (IgE antibodies) immunological response. Finally, the chronic condition of the infection is distinguished by a granulomatous lesion (<a class="elsevierStyleCrossRef" href="#bib0105">Mitchell et al., 2006</a>).</p><p id="par0045" class="elsevierStylePara elsevierViewall">The human inflammatory reaction to the presence of A<span class="elsevierStyleInf">3</span>L of <span class="elsevierStyleItalic">G. binucleatum</span> in the skin is an eosinophilic granulomatose panniculitis; this is caused by the erratic migration of the larvae through the dermis; similar results have been reported in human biopsies in Mexico (<a class="elsevierStyleCrossRef" href="#bib0095">Magaña et al., 2004</a>) and Ecuador (<a class="elsevierStyleCrossRef" href="#bib0115">Ollague and Ollague, 1987</a>), and by other <span class="elsevierStyleItalic">Gnathostoma</span> species in several Asian countries (e.g., <a class="elsevierStyleCrossRef" href="#bib0060">Grobusch et al., 2000</a>). In some cases, larvae can migrate to other organs such as brain, eyes, and liver, causing meningitis (<a class="elsevierStyleCrossRef" href="#bib0140">Schmutzhard et al., 1988</a>), retinopathies (<a class="elsevierStyleCrossRef" href="#bib0135">Rao et al., 1999</a>), and eosinophilic hepatitis (<a class="elsevierStyleCrossRef" href="#bib0145">Seguchi et al., 1995</a>), respectively.</p><p id="par0050" class="elsevierStylePara elsevierViewall">The presence of adults of <span class="elsevierStyleItalic">G. turgidum</span> and <span class="elsevierStyleItalic">G. lamothei</span> infecting the stomach of opossum and raccoon, respectively, led to a granulomatous eosinophilic gastritis, (Categories III-IV); this condition was caused by the parasite migration to the stomach fundic region, to form an intraluminal nodule on the mucosa. This pathology has been observed in several definitive hosts such as domestic and feral cats (<a class="elsevierStyleCrossRef" href="#bib0100">Mei et al., 2001</a>; <a class="elsevierStyleCrossRef" href="#bib0030">Beveridge et al., 1998</a>), domestic dogs (<a class="elsevierStyleCrossRef" href="#bib0010">Álvarez-Guerrero et al., 2012</a>), raccoons (<a class="elsevierStyleCrossRef" href="#bib0005">Almeyda-Artigas et al., 1994</a>), Asiatic lions (<a class="elsevierStyleCrossRef" href="#bib0120">Patel et al., 2000</a>), domestic swine (<a class="elsevierStyleCrossRef" href="#bib0100">Mei et al., 2001</a>), wild boar<a name="p433"></a> (<a class="elsevierStyleCrossRef" href="#bib0065">Ishiwata et al., 1998</a>), raccoons (<a class="elsevierStyleCrossRef" href="#bib0025">Bertoni-Ruiz et al., 2005</a>), and opossums (<a class="elsevierStyleCrossRef" href="#bib0045">García-Márquez, 2005</a>).</p><p id="par0055" class="elsevierStylePara elsevierViewall">The histological damage produced by these nematodes is the result of 2 main parasitic mechanisms: <span class="elsevierStyleItalic">1)</span> migration through tissues of A<span class="elsevierStyleInf">3</span>L; <span class="elsevierStyleItalic">2)</span> enzymatic release which causes tissue degeneration, necrosis, and granulomas. The parasitized host reacts with a cellular immune response with production of cytokines such as interleukin (IL)-<a name="p434"></a>type IL-4, IL-5, IL-10, and IL-13, as well as the colony stimulating granulocyte and monocyte factor (GM-CSF), which activate and stimulate the proliferation of cells, such as eosinophils, macrophages, monocytes, lymphocytes, plasmatic cells, epithelioid cells, giant cells, and fibroblasts (<a class="elsevierStyleCrossRef" href="#bib0035">Cox and Liew, 1992</a>). This condition promotes a tissue response and granuloma formation, originating a chronic infection due to the host immune response against the parasite or their secretions or excretions (<a class="elsevierStyleCrossRef" href="#bib0035">Cox and Liew, 1992</a>; <a class="elsevierStyleCrossRef" href="#bib0040">Díaz-Camacho et al., 1998</a>).</p><p id="par0060" class="elsevierStylePara elsevierViewall">Host-parasite interaction determines the type of inflammatory reaction; the characterization of the different levels (categories) of this response, proposed by <a class="elsevierStyleCrossRef" href="#bib0150">Vázquez-Núñez et al. (2004)</a>, is a useful guide to analyze microscopic features of the lesions caused by parasites as <span class="elsevierStyleItalic">Gnathostoma</span> spp. and provides a basic understanding of the general principles of the pathogenesis and pathology of gnathostomiasis.</p></span></span>" "textoCompletoSecciones" => array:1 [ "secciones" => array:10 [ 0 => array:2 [ "identificador" => "xres406698" "titulo" => "Abstract" ] 1 => array:2 [ "identificador" => "xpalclavsec382918" "titulo" => "Key words" ] 2 => array:2 [ "identificador" => "xres406697" "titulo" => "Resumen" ] 3 => array:2 [ "identificador" => "xpalclavsec382917" "titulo" => "Palabras clave" ] 4 => array:2 [ "identificador" => "sec0005" "titulo" => "Introduction" ] 5 => array:2 [ "identificador" => "sec0010" "titulo" => "Materials and methods" ] 6 => array:2 [ "identificador" => "sec0015" "titulo" => "Results" ] 7 => array:2 [ "identificador" => "sec0020" "titulo" => "Discussion" ] 8 => array:2 [ "identificador" => "xack119039" "titulo" => "Acknowledgements" ] 9 => array:1 [ "titulo" => "Literature cited" ] ] ] "pdfFichero" => "main.pdf" "tienePdf" => true "fechaRecibido" => "2013-01-28" "fechaAceptado" => "2013-12-01" "PalabrasClave" => array:2 [ "es" => array:1 [ 0 => array:4 [ "clase" => "keyword" "titulo" => "Key words" "identificador" => "xpalclavsec382918" "palabras" => array:3 [ 0 => "gnathostomiasis" 1 => "histopathology" 2 => "zoonoses" ] ] ] "en" => array:1 [ 0 => array:4 [ "clase" => "keyword" "titulo" => "Palabras clave" "identificador" => "xpalclavsec382917" "palabras" => array:3 [ 0 => "gnatostomiasis" 1 => "histopatología" 2 => "zoonosis" ] ] ] ] "tieneResumen" => true "resumen" => array:2 [ "es" => array:2 [ "titulo" => "Abstract" "resumen" => "<p id="spar0040" class="elsevierStyleSimplePara elsevierViewall">The aim of this study was to describe and compare the inflammatory reaction caused by <span class="elsevierStyleItalic">Gnathostoma</span> spp., in various tissues of wild vertebrates and humans in Mexico. Parasitized tissues were collected from 10 species of vertebrates from 8 states. Samples were fixed in 10% formalin, pH 7.2 and processed with standard histological techniques. The lesions were classified into 4 categories. The advanced third stage larvae in fish, amphibians, and reptiles were associated with inflammatory reaction categories I and II (no injury, discrete or minimum); birds presented lesions classified in categories II, III, and IV (injuries minimal to discrete, moderate to severe; granulomatous); 1 human sample had lesions classified in categories III and IV (injuries moderate to severe; granulomatous). Adult parasites in mammals generated responses in categories III and IV. Inflammatory reactions observed in the different studied vertebrates suggest a complex host response to the presence of the parasite, causing variable tissue changes. The tissue reactions provide basic knowledge on the general principles of the pathogenesis and pathology of gnathostomiasis.</p>" ] "en" => array:2 [ "titulo" => "Resumen" "resumen" => "<p id="spar0045" class="elsevierStyleSimplePara elsevierViewall">El objetivo de este estudio fue describir y comparar la reacción inflamatoria que causa <span class="elsevierStyleItalic">Gnathostoma</span> spp., en los tejidos de diversos vertebrados silvestres y el humano en México. Se recolectaron tejidos parasitados de 10 especies de vertebrados, de 8 estados de la República Mexicana. Las muestras se fijaron en formalina al 10%, pH 7.2 y se procesaron con la técnica histológica de rutina. Las lesiones se clasificaron en 4 categorías; las larvas de tercer estadio avanzado en los peces, anfibios y reptiles causaron una reacción inflamatoria de las categorías I y II (sin lesión, o lesión mínima a discreta); en las aves, se registraron las categorías II, III y IV (lesión mínima a discreta, moderada a intensa y granulomatosa) y en el humano, categorías III y IV (lesión moderada a intensa y granulomatosa). Los parásitos adultos en los mamíferos generaron respuestas de las categorías III y IV. Las reacciones inflamatorias que causan a los diferentes vertebrados estudiados sugieren una respuesta compleja debido a la presencia del parásito y a la respuesta de los hospederos, causando alteraciones tisulares muy variables. Las reacciones tisulares proporcionan conocimientos básicos sobre los principios generales de la patogenia y patología de la gnatostomiasis.</p>" ] ] "multimedia" => array:7 [ 0 => array:7 [ "identificador" => "fig0005" "etiqueta" => "Figure 1" "tipo" => "MULTIMEDIAFIGURA" "mostrarFloat" => true "mostrarDisplay" => false "figura" => array:1 [ 0 => array:4 [ "imagen" => "gr1.jpeg" "Alto" => 885 "Ancho" => 1406 "Tamanyo" => 244804 ] ] "descripcion" => array:1 [ "es" => "<p id="spar0005" class="elsevierStyleSimplePara elsevierViewall">Skeletal muscle (me) of fish (<span class="elsevierStyleItalic">Petenia splendida</span>) with parasitic cyst (qp) and larva (A<span class="elsevierStyleInf">3</span>L) of <span class="elsevierStyleItalic">Gnathostoma</span> sp., encapsulated by connective tissue (category I lesion). Hematoxylin -eosin staining. Scale bar 100<span class="elsevierStyleHsp" style=""></span>μm.</p>" ] ] 1 => array:7 [ "identificador" => "fig0010" "etiqueta" => "Figure 2" "tipo" => "MULTIMEDIAFIGURA" "mostrarFloat" => true "mostrarDisplay" => false "figura" => array:1 [ 0 => array:4 [ "imagen" => "gr2.jpeg" "Alto" => 784 "Ancho" => 1406 "Tamanyo" => 266002 ] ] "descripcion" => array:1 [ "es" => "<p id="spar0010" class="elsevierStyleSimplePara elsevierViewall">A), skeletal muscle (me) of bird (<span class="elsevierStyleItalic">Ardea alba</span>) with unencysted larva (A<span class="elsevierStyleInf">3</span>L) of <span class="elsevierStyleItalic">Gnathostoma</span> sp., exhibiting moderate to severe mixed inflammatory infiltration (Ci); B-C), inflammatory cells, mainly eosinophils, neutrophils and macrophages, muscledegeneration and necrosis (me) (categories II-III lesions). Hematoxylin -eosin staining. Scale bar 100<span class="elsevierStyleHsp" style=""></span>μm.</p>" ] ] 2 => array:7 [ "identificador" => "fig0015" "etiqueta" => "Figure 3" "tipo" => "MULTIMEDIAFIGURA" "mostrarFloat" => true "mostrarDisplay" => false "figura" => array:1 [ 0 => array:4 [ "imagen" => "gr3.jpeg" "Alto" => 803 "Ancho" => 1274 "Tamanyo" => 291106 ] ] "descripcion" => array:1 [ "es" => "<p id="spar0015" class="elsevierStyleSimplePara elsevierViewall">A), human skin with unencysted larva (A<span class="elsevierStyleInf">3</span>L) of <span class="elsevierStyleItalic">Gnathostoma</span> sp. in the dermis, exhibiting severe to granulomatous mixed inflammatory infiltration (Ci); B), inflammatory cells eosinophils (Eo) macrophages and lymphocytes; C), Giantcell (Cg) forming granuloma (Categories III-IV lesions). Masson's trichrome staining. Scale bar 100<span class="elsevierStyleHsp" style=""></span>μm.</p>" ] ] 3 => array:7 [ "identificador" => "fig0020" "etiqueta" => "Figure 4" "tipo" => "MULTIMEDIAFIGURA" "mostrarFloat" => true "mostrarDisplay" => false "figura" => array:1 [ 0 => array:4 [ "imagen" => "gr4.jpeg" "Alto" => 1018 "Ancho" => 1274 "Tamanyo" => 208363 ] ] "descripcion" => array:1 [ "es" => "<p id="spar0020" class="elsevierStyleSimplePara elsevierViewall"><span class="elsevierStyleItalic">Gnathostoma turgidum</span> embedded in the gastric mucosa of <span class="elsevierStyleItalic">Didelphis virginiana</span>. The worm is indicated by an arrow.</p>" ] ] 4 => array:7 [ "identificador" => "fig0025" "etiqueta" => "Figure 5" "tipo" => "MULTIMEDIAFIGURA" "mostrarFloat" => true "mostrarDisplay" => false "figura" => array:1 [ 0 => array:4 [ "imagen" => "gr5.jpeg" "Alto" => 935 "Ancho" => 1404 "Tamanyo" => 251709 ] ] "descripcion" => array:1 [ "es" => "<p id="spar0025" class="elsevierStyleSimplePara elsevierViewall">Gastric mucosa of <span class="elsevierStyleItalic">Didelphis virginiana</span>. A), adult female of <span class="elsevierStyleItalic">Gnathostoma turgidum</span> on the submucosa with inflammatory infiltration; B), foreign body giant cells; C), proliferation of fibrous connective tissue on the submucosa; D), necrosis and dystrophic mineralization with fibroplasia (categories III-IV lesions). Hematoxylin -eosin staining. Scale bar 100<span class="elsevierStyleHsp" style=""></span>μm.</p>" ] ] 5 => array:7 [ "identificador" => "tbl0005" "etiqueta" => "Table 1" "tipo" => "MULTIMEDIATABLA" "mostrarFloat" => true "mostrarDisplay" => false "tabla" => array:2 [ "tablatextoimagen" => array:1 [ 0 => array:2 [ "tabla" => array:1 [ 0 => """ <table border="0" frame="\n \t\t\t\t\tvoid\n \t\t\t\t" class=""><thead title="thead"><tr title="table-row"><td class="td" title="\n \t\t\t\t\ttable-head\n \t\t\t\t " align="left" valign="middle" style="border-bottom: 2px solid black"><span class="elsevierStyleItalic">Host species</span> \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="\n \t\t\t\t\ttable-head\n \t\t\t\t " align="center" valign="middle" style="border-bottom: 2px solid black"><span class="elsevierStyleItalic">Stage</span> \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="\n \t\t\t\t\ttable-head\n \t\t\t\t " align="center" valign="middle" style="border-bottom: 2px solid black"><span class="elsevierStyleItalic">Distribution</span> \t\t\t\t\t\t\n \t\t\t\t</td></tr></thead><tbody title="tbody"><tr title="table-row"><td class="td" title="\n \t\t\t\t\ttable-entry\n \t\t\t\t " align="left" valign="middle">Fish \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="center" valign="middle"> \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="center" valign="middle"> \t\t\t\t\t\t\n \t\t\t\t</td></tr><tr title="table-row"><td class="td" title="\n \t\t\t\t\ttable-entry\n \t\t\t\t " align="left" valign="middle"><span class="elsevierStyleItalic">Petenia splendida</span><a class="elsevierStyleCrossRef" href="#tblfn0005"><span class="elsevierStyleSup">a</span></a> \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="center" valign="middle">L<span class="elsevierStyleInf">3</span>A \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="center" valign="middle">Oaxaca: Presa Temascal (18°13'00” N, 96°25'00” W) \t\t\t\t\t\t\n \t\t\t\t</td></tr><tr title="table-row"><td class="td" title="\n \t\t\t\t\ttable-entry\n \t\t\t\t " align="left" valign="middle"><span class="elsevierStyleItalic">Gobiomorus dormitor</span><a class="elsevierStyleCrossRef" href="#tblfn0005"><span class="elsevierStyleSup">a</span></a> \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="center" valign="middle">L<span class="elsevierStyleInf">3</span>A \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="center" valign="middle">Tabasco: Pantanos de Centla (18°28'19” N, 92°39'15” W) \t\t\t\t\t\t\n \t\t\t\t</td></tr><tr title="table-row"><td class="td" title="\n \t\t\t\t\ttable-entry\n \t\t\t\t " align="left" valign="middle">Amphibians \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="center" valign="middle"> \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="center" valign="middle"> \t\t\t\t\t\t\n \t\t\t\t</td></tr><tr title="table-row"><td class="td" title="\n \t\t\t\t\ttable-entry\n \t\t\t\t " align="left" valign="middle"><span class="elsevierStyleItalic">Lithobates forreri</span><a class="elsevierStyleCrossRef" href="#tblfn0005"><span class="elsevierStyleSup">a</span></a> \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="center" valign="middle">L<span class="elsevierStyleInf">3</span>A \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="center" valign="middle">Chiapas: Laguna Catazajá (17°46'03” N, 92°02'00” W) \t\t\t\t\t\t\n \t\t\t\t</td></tr><tr title="table-row"><td class="td" title="\n \t\t\t\t\ttable-entry\n \t\t\t\t " align="left" valign="middle">Reptiles \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="center" valign="middle"> \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="center" valign="middle"> \t\t\t\t\t\t\n \t\t\t\t</td></tr><tr title="table-row"><td class="td" title="\n \t\t\t\t\ttable-entry\n \t\t\t\t " align="left" valign="middle"><span class="elsevierStyleItalic">Crocodylus acutus</span><a class="elsevierStyleCrossRef" href="#tblfn0005"><span class="elsevierStyleSup">a</span></a> \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="center" valign="middle">L<span class="elsevierStyleInf">3</span>A \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="center" valign="middle">Colima: Laguna de Amela (18°50'07” N, 103°45'55” W) \t\t\t\t\t\t\n \t\t\t\t</td></tr><tr title="table-row"><td class="td" title="\n \t\t\t\t\ttable-entry\n \t\t\t\t " align="left" valign="middle">Birds \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="center" valign="middle"> \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="center" valign="middle"> \t\t\t\t\t\t\n \t\t\t\t</td></tr><tr title="table-row"><td class="td" title="\n \t\t\t\t\ttable-entry\n \t\t\t\t " align="left" valign="middle"><span class="elsevierStyleItalic">Ardea alba</span><a class="elsevierStyleCrossRef" href="#tblfn0005"><span class="elsevierStyleSup">a</span></a> \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="center" valign="middle">L<span class="elsevierStyleInf">3</span>A \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="center" valign="middle">Sinaloa: Laguna Alhuate (24°31'01” N, 107°20'10” W) \t\t\t\t\t\t\n \t\t\t\t</td></tr><tr title="table-row"><td class="td" title="\n \t\t\t\t\ttable-entry\n \t\t\t\t " align="left" valign="middle"><span class="elsevierStyleItalic">Pelecanus erythrorhynchus</span><a class="elsevierStyleCrossRef" href="#tblfn0005"><span class="elsevierStyleSup">a</span></a> \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="center" valign="middle">L<span class="elsevierStyleInf">3</span>A \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="center" valign="middle">Sinaloa: Laguna Alhuate (24°31'01” N, 107°20'10” W) \t\t\t\t\t\t\n \t\t\t\t</td></tr><tr title="table-row"><td class="td" title="\n \t\t\t\t\ttable-entry\n \t\t\t\t " align="left" valign="middle"><span class="elsevierStyleItalic">Phalacrocorax brasilianus</span><a class="elsevierStyleCrossRef" href="#tblfn0005"><span class="elsevierStyleSup">a</span></a> \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="center" valign="middle">L<span class="elsevierStyleInf">3</span>A \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="center" valign="middle">Guerrero: Laguna de Tres Palos (16°47'47” N, 99°44'30” W) \t\t\t\t\t\t\n \t\t\t\t</td></tr><tr title="table-row"><td class="td" title="\n \t\t\t\t\ttable-entry\n \t\t\t\t " align="left" valign="middle">Mammals \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="center" valign="middle"> \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="center" valign="middle"> \t\t\t\t\t\t\n \t\t\t\t</td></tr><tr title="table-row"><td class="td" title="\n \t\t\t\t\ttable-entry\n \t\t\t\t " align="left" valign="middle"><span class="elsevierStyleItalic">Homo sapiens</span><a class="elsevierStyleCrossRef" href="#tblfn0010"><span class="elsevierStyleSup">b</span></a> \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="center" valign="middle">L<span class="elsevierStyleInf">3</span>A \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="center" valign="middle">Nayarit: Tepic (21°30'13” N, 104°53'40” W) \t\t\t\t\t\t\n \t\t\t\t</td></tr><tr title="table-row"><td class="td" title="\n \t\t\t\t\ttable-entry\n \t\t\t\t " align="left" valign="middle"><span class="elsevierStyleItalic">Didelphis virginiana</span><a class="elsevierStyleCrossRef" href="#tblfn0015"><span class="elsevierStyleSup">c</span></a> \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="center" valign="middle">Adult \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="center" valign="middle">Veracruz: Tlacotalpan (18°38'29” N, 95°41'26” W) \t\t\t\t\t\t\n \t\t\t\t</td></tr><tr title="table-row"><td class="td" title="\n \t\t\t\t\ttable-entry\n \t\t\t\t " align="left" valign="middle"><span class="elsevierStyleItalic">Procyon lotor</span><a class="elsevierStyleCrossRef" href="#tblfn0015"><span class="elsevierStyleSup">c</span></a> \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="center" valign="middle">Adult \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="center" valign="middle">Veracruz: Tlacotalpan (18°38'29” N, 95°41'26” W) \t\t\t\t\t\t\n \t\t\t\t</td></tr></tbody></table> """ ] "imagenFichero" => array:1 [ 0 => "xTab633725.png" ] ] ] "notaPie" => array:3 [ 0 => array:3 [ "identificador" => "tblfn0005" "etiqueta" => "a)" "nota" => "<p class="elsevierStyleNotepara" id="npar0005">Skeletal muscle;</p>" ] 1 => array:3 [ "identificador" => "tblfn0010" "etiqueta" => "b)" "nota" => "<p class="elsevierStyleNotepara" id="npar0010">dermis;</p>" ] 2 => array:3 [ "identificador" => "tblfn0015" "etiqueta" => "c)" "nota" => "<p class="elsevierStyleNotepara" id="npar0015">stomach.</p>" ] ] ] "descripcion" => array:1 [ "es" => "<p id="spar0030" class="elsevierStyleSimplePara elsevierViewall">Hosts infected with <span class="elsevierStyleItalic">Gnathostoma</span> spp. included in this study</p>" ] ] 6 => array:7 [ "identificador" => "tbl0010" "etiqueta" => "Table 2" "tipo" => "MULTIMEDIATABLA" "mostrarFloat" => true "mostrarDisplay" => false "tabla" => array:2 [ "tablatextoimagen" => array:1 [ 0 => array:2 [ "tabla" => array:1 [ 0 => """ <table border="0" frame="\n \t\t\t\t\tvoid\n \t\t\t\t" class=""><thead title="thead"><tr title="table-row"><td class="td" title="\n \t\t\t\t\ttable-head\n \t\t\t\t " align="left" valign="middle" style="border-bottom: 2px solid black"><span class="elsevierStyleItalic">Category</span> \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="\n \t\t\t\t\ttable-head\n \t\t\t\t " align="center" valign="middle" style="border-bottom: 2px solid black"><span class="elsevierStyleItalic">Description</span> \t\t\t\t\t\t\n \t\t\t\t</td></tr></thead><tbody title="tbody"><tr title="table-row"><td class="td" title="\n \t\t\t\t\ttable-entry\n \t\t\t\t " align="left" valign="middle">I<a class="elsevierStyleCrossRef" href="#tblfn0020">*</a> \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="center" valign="middle">Mild hyperplasia of fibrous connective tissue around the parasite. \t\t\t\t\t\t\n \t\t\t\t</td></tr><tr title="table-row"><td class="td" title="\n \t\t\t\t\ttable-entry\n \t\t\t\t " align="left" valign="middle">II<a class="elsevierStyleCrossRef" href="#tblfn0020">*</a> \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="center" valign="middle">Moderate hyperplasia of fibrous connective tissue around the parasite; infiltration of macrophages and heterophils, mainly at levels below 50%. \t\t\t\t\t\t\n \t\t\t\t</td></tr><tr title="table-row"><td class="td" title="\n \t\t\t\t\ttable-entry\n \t\t\t\t " align="left" valign="middle">III<a class="elsevierStyleCrossRef" href="#tblfn0025">**</a> \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="center" valign="middle">Moderate to severe hyperplasia of fibrous connective tissue around the parasite; infiltration macrophages, heterophils (eosinophils), lymphocytes and mononuclear cells, at levels above 50%. Degeneration and necrosis of muscle fibers with vasculitis. \t\t\t\t\t\t\n \t\t\t\t</td></tr><tr title="table-row"><td class="td" title="\n \t\t\t\t\ttable-entry\n \t\t\t\t " align="left" valign="middle">IV<a class="elsevierStyleCrossRef" href="#tblfn0025">**</a> \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="center" valign="middle">Granulomatous lesion; severe hyperplasia of fibrous connective tissue; infiltration of epithelioid cells, giant cells, fibroblasts, and occasionally heterophils (eosinophils). \t\t\t\t\t\t\n \t\t\t\t</td></tr></tbody></table> """ ] "imagenFichero" => array:1 [ 0 => "xTab633724.png" ] ] ] "notaPie" => array:2 [ 0 => array:3 [ "identificador" => "tblfn0020" "etiqueta" => "*" "nota" => "<p class="elsevierStyleNotepara" id="npar0020">Categories described for live larvae exclusively;</p>" ] 1 => array:3 [ "identificador" => "tblfn0025" "etiqueta" => "**" "nota" => "<p class="elsevierStyleNotepara" id="npar0025">categories described for degenerating larvae and live adults. Mild lesion: histopathological changes present in less than 25% of the ocular field (acute infection); moderate lesion: histopathological changes present in 25–50% of the ocular field (sub-acute infection); severe lesion: histopathological changes present in 50–100% of the ocular field (chronic infection).</p>" ] ] ] "descripcion" => array:1 [ "es" => "<p id="spar0035" class="elsevierStyleSimplePara elsevierViewall">Histologic category of lesions found in vertebrates infected by <span class="elsevierStyleItalic">Gnathostoma</span> spp. Evaluation was based in all cases on 1 larva or 1 adult in host tissue</p>" ] ] ] "bibliografia" => array:2 [ "titulo" => "Literature cited" "seccion" => array:1 [ 0 => array:2 [ "identificador" => "bibs0005" "bibliografiaReferencia" => array:31 [ 0 => array:3 [ "identificador" => "bib0005" "etiqueta" => "Almeyda-Artigas et al., 1994" "referencia" => array:1 [ 0 => array:2 [ "contribucion" => array:1 [ 0 => array:2 [ "titulo" => "First record of <span class="elsevierStyleItalic">Gnathostoma procyonis</span>, Chandler, 1942 in Mexico and note on larval <span class="elsevierStyleItalic">G. binucleatum</span> Almeyda-Artigas, 1991" "autores" => array:1 [ 0 => array:2 [ "etal" => false "autores" => array:5 [ 0 => "R.J. 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Special thanks to Luis Antonio Morales Arreola for technical assistance and Dr. Messina-Robles, from the Departmento de Dermatología, Hospital General de Tepic, Secretaría de Salud de Nayarit, for the donation of parasitized human tissue.</p>" "vista" => "all" ] ] ] "idiomaDefecto" => "es" "url" => "/18703453/0000008500000002/v1_201501071639/S1870345314707705/v1_201501071639/es/main.assets" "Apartado" => null "PDF" => "https://static.elsevier.es/multimedia/18703453/0000008500000002/v1_201501071639/S1870345314707705/v1_201501071639/es/main.pdf?idApp=UINPBA00004N&text.app=https://www.elsevier.es/" "EPUB" => "https://multimedia.elsevier.es/PublicationsMultimediaV1/item/epub/S1870345314707705?idApp=UINPBA00004N" ]
| año/Mes | Html | Total | |
|---|---|---|---|
| 2024 Noviembre | 18 | 0 | 18 |
| 2024 Octubre | 81 | 6 | 87 |
| 2024 Septiembre | 55 | 2 | 57 |
| 2024 Agosto | 43 | 1 | 44 |
| 2024 Julio | 41 | 5 | 46 |
| 2024 Junio | 47 | 2 | 49 |
| 2024 Mayo | 22 | 3 | 25 |
| 2024 Abril | 26 | 6 | 32 |
| 2024 Marzo | 44 | 8 | 52 |
| 2024 Febrero | 82 | 5 | 87 |
| 2024 Enero | 74 | 0 | 74 |
| 2023 Diciembre | 90 | 12 | 102 |
| 2023 Noviembre | 98 | 9 | 107 |
| 2023 Octubre | 155 | 8 | 163 |
| 2023 Septiembre | 73 | 1 | 74 |
| 2023 Agosto | 79 | 4 | 83 |
| 2023 Julio | 123 | 4 | 127 |
| 2023 Junio | 106 | 5 | 111 |
| 2023 Mayo | 147 | 2 | 149 |
| 2023 Abril | 54 | 6 | 60 |
| 2023 Marzo | 90 | 2 | 92 |
| 2023 Febrero | 87 | 0 | 87 |
| 2023 Enero | 125 | 7 | 132 |
| 2022 Diciembre | 70 | 5 | 75 |
| 2022 Noviembre | 84 | 4 | 88 |
| 2022 Octubre | 85 | 12 | 97 |
| 2022 Septiembre | 62 | 12 | 74 |
| 2022 Agosto | 72 | 11 | 83 |
| 2022 Julio | 43 | 7 | 50 |
| 2022 Junio | 49 | 8 | 57 |
| 2022 Mayo | 67 | 10 | 77 |
| 2022 Abril | 53 | 10 | 63 |
| 2022 Marzo | 103 | 7 | 110 |
| 2022 Febrero | 66 | 3 | 69 |
| 2022 Enero | 87 | 15 | 102 |
| 2021 Diciembre | 67 | 13 | 80 |
| 2021 Noviembre | 61 | 5 | 66 |
| 2021 Octubre | 84 | 15 | 99 |
| 2021 Septiembre | 81 | 13 | 94 |
| 2021 Agosto | 88 | 12 | 100 |
| 2021 Julio | 51 | 7 | 58 |
| 2021 Junio | 48 | 8 | 56 |
| 2021 Mayo | 54 | 6 | 60 |
| 2021 Abril | 145 | 48 | 193 |
| 2021 Marzo | 77 | 10 | 87 |
| 2021 Febrero | 48 | 21 | 69 |
| 2021 Enero | 62 | 19 | 81 |
| 2020 Diciembre | 79 | 24 | 103 |
| 2020 Noviembre | 78 | 20 | 98 |
| 2020 Octubre | 56 | 20 | 76 |
| 2020 Septiembre | 37 | 5 | 42 |
| 2020 Agosto | 56 | 2 | 58 |
| 2020 Julio | 31 | 6 | 37 |
| 2020 Junio | 46 | 6 | 52 |
| 2020 Mayo | 54 | 7 | 61 |
| 2020 Abril | 50 | 10 | 60 |
| 2020 Marzo | 66 | 4 | 70 |
| 2020 Febrero | 48 | 8 | 56 |
| 2020 Enero | 49 | 9 | 58 |
| 2019 Diciembre | 61 | 6 | 67 |
| 2019 Noviembre | 59 | 1 | 60 |
| 2019 Octubre | 36 | 5 | 41 |
| 2019 Septiembre | 43 | 2 | 45 |
| 2019 Agosto | 25 | 0 | 25 |
| 2019 Julio | 45 | 17 | 62 |
| 2019 Junio | 90 | 14 | 104 |
| 2019 Mayo | 190 | 17 | 207 |
| 2019 Abril | 72 | 5 | 77 |
| 2019 Marzo | 12 | 6 | 18 |
| 2019 Febrero | 20 | 7 | 27 |
| 2019 Enero | 17 | 6 | 23 |
| 2018 Diciembre | 9 | 5 | 14 |
| 2018 Noviembre | 16 | 3 | 19 |
| 2018 Octubre | 34 | 23 | 57 |
| 2018 Septiembre | 9 | 5 | 14 |
| 2018 Agosto | 17 | 10 | 27 |
| 2018 Julio | 14 | 9 | 23 |
| 2018 Junio | 14 | 10 | 24 |
| 2018 Mayo | 5 | 17 | 22 |
| 2018 Abril | 22 | 4 | 26 |
| 2018 Marzo | 14 | 2 | 16 |
| 2018 Febrero | 8 | 6 | 14 |
| 2018 Enero | 6 | 6 | 12 |
| 2017 Diciembre | 6 | 3 | 9 |
| 2017 Noviembre | 10 | 12 | 22 |
| 2017 Octubre | 14 | 5 | 19 |
| 2017 Septiembre | 14 | 15 | 29 |
| 2017 Agosto | 7 | 17 | 24 |
| 2017 Julio | 14 | 6 | 20 |
| 2017 Junio | 24 | 56 | 80 |
| 2017 Mayo | 25 | 31 | 56 |
| 2017 Abril | 13 | 13 | 26 |
| 2017 Marzo | 20 | 31 | 51 |
| 2017 Febrero | 21 | 11 | 32 |
| 2017 Enero | 15 | 7 | 22 |
| 2016 Diciembre | 23 | 24 | 47 |
| 2016 Noviembre | 22 | 28 | 50 |
| 2016 Octubre | 37 | 56 | 93 |
| 2016 Septiembre | 71 | 11 | 82 |
| 2016 Agosto | 45 | 7 | 52 |
| 2016 Julio | 18 | 18 | 36 |
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