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Basic Research
Comparison of Intraperitoneal Honey and Sodium Hyaluronate-Carboxymethylcellulose (Seprafilm™) for the Prevention of Postoperative Intra-Abdominal Adhesions
Arif EmreI, Murat AkinI,
Corresponding author
makin@gazi.edu.tr

Tel.: 903122025719
, Ipek IsikgonulII, Osman YukselI, Ahmet Ziya AnadolI, Cagatay CifterI
I Department of General Surgery, Gazi University Medical School - Ankara, Turkey
II Department of Pathology, Gazi University Medical School - Ankara, Turkey
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    "textoCompleto" => "<span class="elsevierStyleSections"><span id="cesec10" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="cestitle60">INTRODUCTION</span><p id="para10" class="elsevierStylePara elsevierViewall">Postoperative intra-abdominal adhesion &#40;PIAA&#41; formation has long been considered an unavoidable consequence of laparotomy&#46; Despite improvements in surgical techniques and instruments&#44; PIAA formation is still a major source of morbidity and mortality&#46; The incidence of adhesion formation has been reported to be 93 to 100&#37; in patients who have undergone abdominal surgery&#46;<a class="elsevierStyleCrossRef" href="#bib1">1</a> PIAAs after laparotomy can induce small-bowel obstruction&#44; infarction&#44; fistula formation&#44; chronic pelvic pain&#44; secondary female infertility and technical difficulty in cases of re-operation&#59; they also generate a significant economic burden from the need for increased medical services&#46;<a class="elsevierStyleCrossRef" href="#bib2">2</a>&#44; <a class="elsevierStyleCrossRef" href="#bib3">3</a></p><p id="para20" class="elsevierStylePara elsevierViewall">The search for an effective anti-adhesion device has been continuing for decades&#46; Many methods&#44; drugs and materials have been evaluated to prevent PIAAs&#46; The long list of failed materials includes corticosteroids&#44; antihistamine&#44; dextran&#44; saline&#44; anti-cytokine agents&#44; recombinant tissue plasminogen activators&#44; aprotinin&#44; octreotide and heparin&#46;<a class="elsevierStyleCrossRef" href="#bib2">2</a>&#44;<a class="elsevierStyleCrossRef" href="#bib4">4</a> Thus far&#44; no ideal method has been found for the prevention of PIAA formation&#46; Intra-abdominal administration of some anti-adhesive barriers&#44; such as a bioresorbable membrane consisting of sodium hyaluronate and carboxymethylcellulose &#40;Seprafilm&#8482;&#41; &#40;Genzyme Corporation&#44; Cambridge&#44; MA&#41;&#44; may reduce postoperative adhesions&#44; as demonstrated by some animal models and clinical studies&#46;<a class="elsevierStyleCrossRef" href="#bib2">2</a>&#44;<a class="elsevierStyleCrossRef" href="#bib5">5</a>&#44;<a class="elsevierStyleCrossRef" href="#bib6">6</a></p><p id="para30" class="elsevierStylePara elsevierViewall">Honey has been used in burn victims and as a method of wound treatment for more than 2000 years&#46; Honey is the foodstuff produced by honeybees from the nectar of flowers or secretions from other parts of the plant&#46; It is rich in flavonoid components&#44; such as luteolin&#44; quercetin&#44; apigenin&#44; fisetin&#44; kaempferol&#44; isorhamnetin&#44; acacetin&#44; tamarixetin&#44; chrysin and galangin&#44; and&#44; thus&#44; exhibits antioxidant activity&#46; Honey inhibits the growth of both gram-positive and gram-negative bacteria and provides anti-bacterial&#44; anti-inflammatory&#44; immuno-stimulatory&#44; anti-ulcer and wound- and burn-healing effects&#46;<a class="elsevierStyleCrossRef" href="#bib7">7</a> Certain physical properties of honey&#44; such as its hygroscopicity&#44; low pH and hypertonicity&#44; are supposedly responsible for its wound-healing effects&#46;<a class="elsevierStyleCrossRef" href="#bib7">7</a>&#44;<a class="elsevierStyleCrossRef" href="#bib8">8</a></p><p id="para40" class="elsevierStylePara elsevierViewall">The purpose of this study was to compare honey with a standard bioresorbable membrane &#40;Seprafilm&#8482;&#41; to prevent the formation of PIAAs in rats&#46;</p></span><span id="cesec20" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="cestitle70">MATERIALS AND METHODS</span><p id="para50" class="elsevierStylePara elsevierViewall">This study was performed in the Animal Research Laboratory of Gazi University&#46; Approval from the Research Committee of Gazi University was obtained before the study&#46; A total of 30 female Wistar Albino rats&#44; each weighing between 280&#8211;390 g&#44; were used after overnight fasting&#46;</p><p id="para60" class="elsevierStylePara elsevierViewall">The animals were divided into three groups&#44; each containing ten rats&#46; Group 1 &#40;control group&#41; represented the cecal abrasion group&#44; with no intraperitoneal administration of any substance&#46; Group 2 &#40;honey group&#41; underwent cecal abrasion and intraperitoneal honey administration &#40;Mechihoney&#44; Europa lmt&#46;&#44; RICHLANDS QLD&#44; AUSTRALIA&#41;&#46; Group 3 &#40;Seprafilm&#8482; group&#41; underwent cecal abrasion and intraperitoneal Seprafilm&#8482; application&#46; For anesthesia&#44; the animals received 50 mg&#47;kg of ketamine hydrochloride &#40;Ketalar&#44; 50 mg&#47;mL&#59; Parke-Davis&#44; Istanbul&#41; intramuscularly and 5 mg&#47;kg of xylazine &#40;Xylazine-20 Injection&#44; Butler Company&#44; Columbus&#44; OH&#41;&#46;</p><p id="para70" class="elsevierStylePara elsevierViewall">After shaving and disinfection of the skin&#44; a 3-cm midline incision was made&#46; The terminal ileum and cecum were mobilized and placed on wet gauze&#46; Both sides of a 5- to 10-cm segment of terminal ileum and cecum were scraped until serosal petechiae appeared on the intestinal surfaces&#46; The arteries of the scraped segments were then clamped for one minute to induce transient ischemia &#40;scraping model&#44; Figure <a class="elsevierStyleCrossRef" href="#fig1">1A</a>&#44; <a class="elsevierStyleCrossRef" href="#fig1">1B</a>&#41;&#46;<a class="elsevierStyleCrossRef" href="#bib8">8</a> In the control group&#44; only this scraping model was performed&#44; while in the honey group&#44; the scraped areas were coated with 4 g of honey&#46; In the Seprafilm&#8482; group&#44; a 20x30-mm sheet of material was applied directly to the abraded cecum before closure&#46; The abdominal incision was closed in two layers with simple&#44; continuous sutures of silk 3&#47;0&#46;</p><elsevierMultimedia ident="fig1"></elsevierMultimedia><p id="para80" class="elsevierStylePara elsevierViewall">All rats were allowed to resume their diets until the 10<span class="elsevierStyleSup">th</span> postoperative day&#44; at which point they were sacrificed with ether&#46; The peritoneal cavities were entered via a reversed U-shaped incision in the anterior abdominal wall&#44; which was retracted caudally to provide maximal exposure&#46; Adhesions were examined macroscopically by two independent investigators &#40;MA&#44; HB&#41; and graded blindly according to the Blauer and Collins scale &#40;Table <a class="elsevierStyleCrossRef" href="#tbl1">1</a>&#41;&#46;<a class="elsevierStyleCrossRef" href="#bib9">9</a> Tissues containing adhesions were excised en bloc and the samples were fixed in a 10&#37; formaldehyde solution&#46; Samples were routinely processed by dehydration and paraffin embedding&#44; and 5-&#956;m cross-sections were prepared using a microtome&#46; The samples were examined under a light microscope after hemotoxylin-eosin staining and were evaluated blindly by the same pathologist &#40;IIG&#41; to determine the general structure and the amount of fibroblastic activity and fibrosis present &#40;Table <a class="elsevierStyleCrossRef" href="#tbl2">2</a>&#41;&#46; Thus&#44; the fibrotic score of each rat was calculated according to the criteria mentioned&#46;<a class="elsevierStyleCrossRef" href="#bib1">1</a></p><elsevierMultimedia ident="tbl1"></elsevierMultimedia><elsevierMultimedia ident="tbl2"></elsevierMultimedia><span id="cesec30" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="cestitle80">Statistics</span><p id="para90" class="elsevierStylePara elsevierViewall">The Kruskal-Wallis test was used to test for differences in the grades of adhesions observed in the three groups&#46; A Mann-Whitney U statistic analysis was used as a non-parametric test to determine differences in adhesion grading&#46; A P-value &#8804;0&#46;05 was considered significant&#44; and a P-value &#60;0&#46;001 was considered highly significant&#46;</p></span></span><span id="cesec40" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="cestitle90">RESULTS</span><p id="para100" class="elsevierStylePara elsevierViewall">A total of 30 rats were randomly assigned to the control group &#40;n &#61; 10&#41;&#44; the honey group &#40;n &#61; 10&#41; or the Seprafilm&#8482; group &#40;n &#61; 10&#41;&#46; Five rats &#40;one in the control group&#44; two in the honey group and two in the Seprafilm&#8482; group&#41; died before re-laparotomy&#46; These rats were replaced and the adhesion operation was redone for corresponding groups and included in the study&#46; The intra-abdominal adhesions and histopathological fibrosis scores are summarized in table <a class="elsevierStyleCrossRef" href="#tbl3">3</a>&#46; Of the ten rats in the control group&#44; five developed grade 4 adhesions&#44; three developed grade 3 adhesions &#40;Figure <a class="elsevierStyleCrossRef" href="#fig1">1C</a>&#41;&#44; and two developed grade 2 adhesions&#46; In the Seprafilm&#8482; group&#44; six developed grade 1 adhesions&#44; and four developed grade 0 adhesions&#46; In the honey group&#44; five developed grade 1 adhesions &#40;Figure <a class="elsevierStyleCrossRef" href="#fig1">1D</a>&#41;&#44; and five developed grade 2 adhesions&#46; Upon histological examination&#44; tissue from rats in the control group demonstrated lymphocytes&#44; plasma cells&#44; polymorphonuclear leucocytes and areas of fibrosis containing fibroblasts &#40;Figure <a class="elsevierStyleCrossRef" href="#fig2">2</a>&#41;&#46; The rats in the honey and Seprafilm&#8482; groups demonstrated decreased infiltration of inflammatory cells&#44; fibroblasts and areas of fibrosis &#40;Figure <a class="elsevierStyleCrossRef" href="#fig3">3</a>&#41;&#46;</p><elsevierMultimedia ident="tbl3"></elsevierMultimedia><elsevierMultimedia ident="fig2"></elsevierMultimedia><elsevierMultimedia ident="fig3"></elsevierMultimedia><p id="para110" class="elsevierStylePara elsevierViewall">The control group had higher adhesion scores between the abdominal wall and the organs &#40;Figure <a class="elsevierStyleCrossRef" href="#fig1">1C</a>&#41;&#46; The honey and Seprafilm&#8482; groups had fewer adhesive attachments to the intra-abdominal structures &#40;Figure <a class="elsevierStyleCrossRef" href="#fig1">1D</a>&#41;&#46; Compared to the control group&#44; both the honey &#40;p&#61;0&#46;001&#41; and Seprafilm&#8482; &#40;p&#61;0&#46;001&#41; groups exhibited a lower incidence of adhesion formation&#46; Comparison of the Seprafilm&#8482; and honey groups showed that adhesion formation was less severe in the Seprafilm&#8482; group &#40;p&#61;0&#46;003&#41;&#46; The Seprafilm&#8482; group exhibited decreased fibrosis scores compared to the control group &#40;p&#61;0&#46;016&#41;&#46; The fibrosis scores in the honey group were also lower than the control group&#44; but this difference was not significant &#40;p&#61;0&#46;063&#41;&#46; Importantly&#44; there was no significant difference between the fibrosis scores of the honey and Seprafilm&#8482; groups &#40;p&#61; 0&#46;688&#41;&#46;</p></span><span id="cesec50" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="cestitle100">DISCUSSION</span><p id="para120" class="elsevierStylePara elsevierViewall">PIAAs account for 40&#37; of all cases of intestinal obstruction&#44; with 60&#8211;70&#37; of those involving the small bowel&#46; Of the patients who require abdominal re-operation&#44; 30&#8211;40&#37; have postoperative adhesion-related intestinal obstruction&#46; Enterocutaneous fistulas&#44; intra-abdominal abscesses and ureteral obstructions can also develop as a result of PIAAs&#46; In addition to causing substantial abdominal and pelvic pain&#44; PIAAs are the leading cause of secondary infertility in women&#46;<a class="elsevierStyleCrossRef" href="#bib10">10</a>&#44; <a class="elsevierStyleCrossRef" href="#bib11">11</a> Therefore&#44; PIAA formations not only represent a significant expenditure for the healthcare system&#44; but they can also result in loss of work force capacity and impaired quality of life&#46; In addition&#44; PIAAs are a major source of morbidity following laparotomy and are the most common cause of high financial burdens&#46; Total costs related to adhesions have been estimated at 1&#46;2 billion U&#46;S&#46; dollars per year&#46;<a class="elsevierStyleCrossRef" href="#bib12">12</a>&#44;<a class="elsevierStyleCrossRef" href="#bib13">13</a> Moreover&#44; complications from adhesions after gynecological surgery were estimated to result in 226&#46;8 million U&#46;S&#46; dollars in health care costs in 2006&#46;<a class="elsevierStyleCrossRef" href="#bib14">14</a></p><p id="para130" class="elsevierStylePara elsevierViewall">Adhesion formation is a complicated process&#46; Although the pathophysiology of adhesion formation is widely understood&#44; an absolute solution to this problem does not yet exist&#46; Adhesions can result from mechanical peritoneal damage&#44; tissue ischemia or the presence of foreign materials&#46; Additionally&#44; two areas of injury must be in contact with each other&#46; Both fibrinogenesis and fibrinolysis are activated&#44; and a distortion of the dynamic balance between these two processes leads to adhesion formation&#46;<a class="elsevierStyleCrossRef" href="#bib13">13</a>&#44;<a class="elsevierStyleCrossRef" href="#bib15">15</a></p><p id="para140" class="elsevierStylePara elsevierViewall">There are many experimental models for provoking peritoneal adhesions&#46; The scraping model is very effective in engendering peritoneal adhesions because it involves two stages of damage&#44; direct mechanical intestinal wall damage from gauze scraping and ischemic damage from vascular clamping &#40;Figure <a class="elsevierStyleCrossRef" href="#fig1">1A</a>&#44; <a class="elsevierStyleCrossRef" href="#fig1">1B</a>&#41;&#46;<a class="elsevierStyleCrossRef" href="#bib8">8</a> As this model mimics abdominal surgery&#44; we chose to use it in this study&#46;</p><p id="para150" class="elsevierStylePara elsevierViewall">PIAAs at the peritoneum most commonly form within seven to ten days and become persistent after fourteen days&#46; Therefore&#44; this stage is critical in preventing adhesion formation&#44; and efforts to combat adhesion formation concentrate mostly on this phase&#46; We chose to wait ten days before performing re-laparotomy because other studies have shown the adhesion scores peak at this time&#46;<a class="elsevierStyleCrossRef" href="#bib1">1</a>&#44;<a class="elsevierStyleCrossRef" href="#bib16">16</a></p><p id="para160" class="elsevierStylePara elsevierViewall">During the past decade&#44; a variety of commercially available substances and materials have been used in attempts to reduce PIAAs&#46;<a class="elsevierStyleCrossRef" href="#bib14">14</a> All of these materials have unique compositions and characteristics&#44; with limitations and advantages regarding their use in the clinical setting&#46; Ideally&#44; such a barrier should be anti-adhesive&#44; highly biocompatible&#44; resorbable&#44; adherent to the traumatized surface&#44; effective on an oozing surface&#44; applicable through the laparoscope and relatively inexpensive&#46; As yet&#44; such an ideal barrier does not exist&#46;<a class="elsevierStyleCrossRef" href="#bib14">14</a></p><p id="para170" class="elsevierStylePara elsevierViewall">The mechanical separation of peritoneal surfaces represents a strategy for blocking peritoneal adhesion formation&#46; This approach is particularly attractive&#44; especially if the device can be easily applied by the surgeon and if the material is biodegradable and does not cause systemic effects&#46; A bioresorbable membrane consisting of sodium hyaluronate and carboxymethylcellulose &#40;Seprafilm&#8482;&#41; is one such material used to prevent surgical adhesions&#46; Within 24 hours of application&#44; the Seprafilm&#8482; turns into a gel&#44; which remains in place to separate adhesiogenic tissues during the first few days after surgery when adhesions are most likely to develop&#46; The material is cleared from the body within four weeks&#46;<a class="elsevierStyleCrossRef" href="#bib2">2</a>&#44;<a class="elsevierStyleCrossRef" href="#bib4">4</a>&#44;<a class="elsevierStyleCrossRef" href="#bib12">12</a></p><p id="para180" class="elsevierStylePara elsevierViewall">Prospective&#44; randomized trials have demonstrated that Seprafilm&#8482; significantly reduces the incidence&#44; severity and extent of adhesions following two-stage restorative proctocolectomy and uterine myomectomy&#46; It has also been demonstrated to decrease the incidence of small-bowel obstruction after intestinal resection&#46;<a class="elsevierStyleCrossRef" href="#bib10">10</a>&#44;<a class="elsevierStyleCrossRef" href="#bib12">12</a>&#44;<a class="elsevierStyleCrossRef" href="#bib17">17</a>&#44;<a class="elsevierStyleCrossRef" href="#bib18">18</a> This benefit was confirmed in our study&#44; where Seprafilm&#8482; was shown to significantly reduce postoperative adhesion formation compared to the control group&#46; However&#44; the therapeutic and physiological effects of Seprafilm&#8482; may be limited to the site of application&#46; The fact that the membrane is thin&#44; crisp and filmy may make it difficult to use&#46; This may be particularly true during difficult abdominal wound closures or cases involving a small incision&#46;<a class="elsevierStyleCrossRef" href="#bib2">2</a></p><p id="para190" class="elsevierStylePara elsevierViewall">Natural honey has been used to treat burns and decubitis wounds since ancient times&#46; Honey is becoming increasingly popular as a modern wound-dressing material&#44; and studies have been published demonstrating its effectiveness&#46; When honey is applied to wounds&#44; it has been found to reduce inflammation&#44; swelling and pain&#44; eliminating the need for surgical removal&#44; and induces a rapid clearance of infections&#46; In the literature&#44; it has been reported that honey carries no toxic effects&#46; Honey is also considered sterile and inhibits the growth of both gram-positive and gram-negative bacteria&#46; It has antifungal&#44; cytostatic&#44; anti-inflammatory&#44; antitumoral and antimetastatic effects and promotes wound healing&#46;<a class="elsevierStyleCrossRef" href="#bib8">8</a>&#44;<a class="elsevierStyleCrossRef" href="#bib19">19</a> However&#44; studies regarding its effects on preventing PIAAs are limited&#46;</p><p id="para200" class="elsevierStylePara elsevierViewall">The mechanisms underlying the effects of honey on wound healing are not entirely clear&#46; However&#44; several different characteristics of honey may have effects on various steps of the wound-healing process&#46; Aysan&#44; et al&#46; suggested that one or more of the ingredients of honey&#44; including cafeic acid&#44; benzoic acid&#44; phenolic acid&#44; flavanoid glycons&#44; inhibin and catalase&#44; may be responsible for its effect&#46; Inhibin and catalase have also been shown to promote the proliferation of epithelial cells&#46; Another possible mechanism by which honey can promote wound healing is by increasing fibroblastic activity&#46; Honey is hygroscopic&#44; hypertonic and has a low pH&#46; Hygroscopic substances decrease edema and constitute a fluid barrier to inhibit deepening of the wound&#46; Hypertonicity contributes to antibacterial and antifungal properties&#46; Thus&#44; a hypertonic environment with a low pH and low moisture may promote the wound-healing process by degrading native collagen within the wound&#46;<a class="elsevierStyleCrossRef" href="#bib8">8</a>&#44; <a class="elsevierStyleCrossRef" href="#bib20">20</a></p><p id="para210" class="elsevierStylePara elsevierViewall">In the present study&#44; we utilized a rat model to compare two types of anti-adhesive devices&#58; an anti-adhesive sheet barrier membrane and honey&#46; We found both materials&#44; if applied just prior to laparotomy closure&#44; significantly reduced the formation of PIAAs&#46; Although the mechanism of action is not clear&#44; intraperitoneal administration of honey can reduce PIAAs&#46; Our study indicates that honey may be used as an anti-adhesive barrier and can produce results similar to those of various types of commercially available materials&#46;</p></span></span>"
    "textoCompletoSecciones" => array:1 [
      "secciones" => array:6 [
        0 => array:2 [
          "identificador" => "xpalclavsec1584633"
          "titulo" => "KEYWORDS"
        ]
        1 => array:2 [
          "identificador" => "cesec10"
          "titulo" => "INTRODUCTION"
        ]
        2 => array:3 [
          "identificador" => "cesec20"
          "titulo" => "MATERIALS AND METHODS"
          "secciones" => array:1 [
            0 => array:2 [
              "identificador" => "cesec30"
              "titulo" => "Statistics"
            ]
          ]
        ]
        3 => array:2 [
          "identificador" => "cesec40"
          "titulo" => "RESULTS"
        ]
        4 => array:2 [
          "identificador" => "cesec50"
          "titulo" => "DISCUSSION"
        ]
        5 => array:1 [
          "titulo" => "REFERENCES"
        ]
      ]
    ]
    "pdfFichero" => "main.pdf"
    "tienePdf" => true
    "fechaRecibido" => "2008-10-26"
    "fechaAceptado" => "2008-12-29"
    "PalabrasClave" => array:1 [
      "en" => array:1 [
        0 => array:4 [
          "clase" => "keyword"
          "titulo" => "KEYWORDS"
          "identificador" => "xpalclavsec1584633"
          "palabras" => array:5 [
            0 => "Postoperative intra-abdominal adhesions"
            1 => "Seprafilm"
            2 => "Honey"
            3 => "Rat"
            4 => "Cecal abrasion"
          ]
        ]
      ]
    ]
    "tieneResumen" => true
    "resumen" => array:1 [
      "en" => array:2 [
        "resumen" => "<span id="ceabs10" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="cestitle10">BACKGROUND&#58;</span><p id="spara70" class="elsevierStyleSimplePara elsevierViewall">Abdominal surgery can lead to postoperative intra-abdominal adhesions &#40;PIAAs&#41; with significant morbidity and mortality&#46; This study compares the use of honey with a standard bioresorbable membrane &#40;Seprafilm&#8482;&#41; to prevent the formation of PIAAs in rats&#46;</p></span> <span id="ceabs20" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="cestitle20">METHODS&#58;</span><p id="spara80" class="elsevierStyleSimplePara elsevierViewall">Thirty rats underwent laparotomy&#44; and PIAAs were induced by scraping the cecum&#46; The animals were divided into three groups&#44; each containing ten rats&#46; Group 1 &#40;control&#41; represented the cecal abrasion group&#44; with no intraperitoneal administration of any substance&#46; Group 2 &#40;honey group&#41; underwent cecal abrasion and intraperitoneal administration of honey&#46; Group 3 &#40;Seprafilm&#8482; group&#41; underwent cecal abrasion and intraperitoneal Seprafilm&#8482; application&#46;</p></span> <span id="ceabs30" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="cestitle30">RESULTS&#58;</span><p id="spara90" class="elsevierStyleSimplePara elsevierViewall">Group 1 exhibited higher adhesion scores for adhesions between the abdominal wall and the organs&#46; Groups 2 and 3 had decreased adhesive attachments to the intra-abdominal structures&#46; Compared to group 1&#44; the incidence of adhesion formation was lower in both group 2 &#40;p&#61;0&#46;001&#41; and group 3 &#40;p&#61;0&#46;001&#41;&#46; The incidence of fibrosis was also lower in group 2 &#40;p&#61;0&#46;016&#41; and group 3 &#40;p&#61;0&#46;063&#41; compared to group 1&#46; There was no significant difference between the histopathological fibrosis scores for the rats in group 2 and those in group 3 &#40;p&#61; 0&#46;688&#41;&#46;</p></span> <span id="ceabs40" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="cestitle40">CONCLUSION&#58;</span><p id="spara100" class="elsevierStyleSimplePara elsevierViewall">This study suggests that both honey and Seprafilm&#8482; decrease the incidence of PIAAs in the rat cecal abrasion model&#46; Although the mechanism of action is not clear&#44; intraperitoneal administration of honey reduced PIAAs&#46; The outcome of this study demonstrates that honey is as effective as Seprafilm&#8482; in preventing PIAAs&#46;</p></span>"
        "secciones" => array:4 [
          0 => array:2 [
            "identificador" => "ceabs10"
            "titulo" => "BACKGROUND&#58;"
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          1 => array:2 [
            "identificador" => "ceabs20"
            "titulo" => "METHODS&#58;"
          ]
          2 => array:2 [
            "identificador" => "ceabs30"
            "titulo" => "RESULTS&#58;"
          ]
          3 => array:2 [
            "identificador" => "ceabs40"
            "titulo" => "CONCLUSION&#58;"
          ]
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      0 => array:7 [
        "identificador" => "fig1"
        "etiqueta" => "Figure 1 -"
        "tipo" => "MULTIMEDIAFIGURA"
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          0 => array:4 [
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          "en" => "<p id="spara10" class="elsevierStyleSimplePara elsevierViewall"><span class="elsevierStyleBold">A-B&#58;</span> Scraping model&#46; <span class="elsevierStyleBold">C&#58;</span> Grade 3 adhesion in a control group animal&#44; with extensive and thick adhesive bands and adhesions between the organs and the abdominal wall&#46; <span class="elsevierStyleBold">D&#58;</span> Grade 1 adhesions in Seprafilm&#8482; group and honey group animals with thin&#44; easily removable adhesive bands between the organs and the abdominal wall&#46;</p>"
        ]
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      1 => array:7 [
        "identificador" => "fig2"
        "etiqueta" => "Figure 2 -"
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        "figura" => array:1 [
          0 => array:4 [
            "imagen" => "gr2.jpeg"
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          "en" => "<p id="spara20" class="elsevierStyleSimplePara elsevierViewall">In the control group&#44; the infiltration of inflammatory cells and areas of fibrosis consisting of fibroblasts are seen in the histopathological examination &#40;H&#47;E staining&#41;</p>"
        ]
      ]
      2 => array:7 [
        "identificador" => "fig3"
        "etiqueta" => "Figure 3 -"
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          "en" => "<p id="spara30" class="elsevierStyleSimplePara elsevierViewall">In the Seprafilm&#8482; group and the honey group fewer inflammatory cells and decreased fibrosis are seen &#40;H&#47;E staining&#41;</p>"
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      ]
      3 => array:7 [
        "identificador" => "tbl1"
        "etiqueta" => "Table 1 -"
        "tipo" => "MULTIMEDIATABLA"
        "mostrarFloat" => true
        "mostrarDisplay" => false
        "tabla" => array:1 [
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                0 => """
                  <table border="0" frame="\n
                  \t\t\t\t\tvoid\n
                  \t\t\t\t" class=""><thead title="thead"><tr title="table-row"><th class="td" title="\n
                  \t\t\t\t\ttable-head\n
                  \t\t\t\t  " align="left" valign="middle" scope="col">Grade&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t\t\t</th><th class="td" title="\n
                  \t\t\t\t\ttable-head\n
                  \t\t\t\t  " align="left" valign="middle" scope="col">Description of adhesions&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t\t\t</th></tr></thead><tbody title="tbody"><tr title="table-row"><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="left" valign="top">0&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="left" valign="top">No adhesion&nbsp;\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="top">1&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="left" valign="top">Thin adhesive bands&#44; easily removable&nbsp;\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="top">2&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="left" valign="top">Thick adhesive bands limited to one area&nbsp;\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="top">3&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="left" valign="top">Extensive and thick adhesive bands&nbsp;\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="top">4&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="left" valign="top">Extensive and thick adhesive bands and adhesions between viscera and&#47;or abdominal wall&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td></tr></tbody></table>
                  """
              ]
            ]
          ]
        ]
        "descripcion" => array:1 [
          "en" => "<p id="spara40" class="elsevierStyleSimplePara elsevierViewall">Blauer and Collins scale for macroscopic assessment of adhesion formation<a class="elsevierStyleCrossRef" href="#bib9">9</a></p>"
        ]
      ]
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        "identificador" => "tbl2"
        "etiqueta" => "Table 2 -"
        "tipo" => "MULTIMEDIATABLA"
        "mostrarFloat" => true
        "mostrarDisplay" => false
        "tabla" => array:1 [
          "tablatextoimagen" => array:1 [
            0 => array:1 [
              "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"><th class="td" title="\n
                  \t\t\t\t\ttable-head\n
                  \t\t\t\t  " align="left" valign="middle" scope="col">Grade&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t\t\t</th><th class="td" title="\n
                  \t\t\t\t\ttable-head\n
                  \t\t\t\t  " align="left" valign="middle" scope="col">Histopathological signs&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t\t\t</th></tr></thead><tbody title="tbody"><tr title="table-row"><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="left" valign="top">0&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="left" valign="top">No fibrosis&nbsp;\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="top">1&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="left" valign="top">Thin bunches of a cellular fibrosis&nbsp;\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="top">2&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="left" valign="top">Wide areas of fibrosis with reduced vascularization&nbsp;\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="top">3&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="left" valign="top">Areas of fibrosis formed by thick bunch of collagen&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td></tr></tbody></table>
                  """
              ]
            ]
          ]
        ]
        "descripcion" => array:1 [
          "en" => "<p id="spara50" class="elsevierStyleSimplePara elsevierViewall">Scale for microscopic assessment of fibrosis<a class="elsevierStyleCrossRef" href="#bib1">1</a></p>"
        ]
      ]
      5 => array:7 [
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        "etiqueta" => "Table 3 -"
        "tipo" => "MULTIMEDIATABLA"
        "mostrarFloat" => true
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        "tabla" => array:3 [
          "leyenda" => "<p id="tfn1" class="elsevierStyleSimplePara elsevierViewall">SD&#58; standard deviation&#46;</p>"
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                0 => """
                  <table border="0" frame="\n
                  \t\t\t\t\tvoid\n
                  \t\t\t\t" class=""><thead title="thead"><tr title="table-row"><th class="td" title="\n
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                  \t\t\t\t  " align="center" valign="middle" scope="col">&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t\t\t</th><th class="td" title="\n
                  \t\t\t\t\ttable-head\n
                  \t\t\t\t  " align="center" valign="middle" scope="col">Adhesion score&nbsp;\t\t\t\t\t\t\n
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                  \t\t\t\t\ttable-head\n
                  \t\t\t\t  " align="center" valign="middle" scope="col">Fibrosis score&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t\t\t</th></tr></thead><tbody title="tbody"><tr title="table-row"><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="left" valign="top">Control group &#40;SD &#177;&#41;&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="center" valign="top">3&#46;3 &#40;2&#8211;4&#41;&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="center" valign="top">1&#46;9 &#40;0&#8211;3&#41;&nbsp;\t\t\t\t\t\t\n
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es en pt

¿Es usted profesional sanitario apto para prescribir o dispensar medicamentos?

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