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Comparison of ventriculotomy closure with and without a coelomic fat patch in Japanese quail (Coturnix coturnix japonica).

Removal of foreign bodies from the ventriculus in birds may necessitate ventriculotomy. Complications with this intervention include leakage and adhesion formation. To investigate if the use of a coelomic fat patch and a tension-relieving suture in addition to a simple interrupted pattern would improve the healing process after ventriculotomy, 2 groups of 9 Japanese quail (Coturnix coturnix japonica) underwent ventriculotomy. In group 1, only simple-interrupted and tension-relieving sutures were used for closure of the ventriculotomy. In group 2, a coelomic fat patch from the surrounding adipose tissue was applied to the incision site in addition to the sutures. All quail recovered normally and were considered clinically healthy after surgery. Three birds from each group were euthanatized at days 7, 14, and 21 after surgery. On histologic examination, the suture techniques used for closure of the ventriculotomy led to minimal inflammation of the surrounding tissues in both groups. Serosal inflammation was significantly greater in group 2 birds that had the adipose patch at closure compared with group 1 birds. Therefore, the use of a coelomic fat patch to cover the site of ventriculotomy did not result in an improved healing process and its use is not recommended in quail.

Key words: soft tissue surgery, ventriculotomy, coelomic fat patch, gastrointestinal, avian, Japanese quail, Coturnix coturnix japonica

Introduction

Gastrointestinal foreign objects, especially those containing heavy metals, are a common clinical presentation in pet birds. (1) Foreign bodies may be removed by hastening of gastrointestinal passage, proventricular and ventricular endoscopic retrieval, retrograde flushing, or use of magnets. If these methods fail, surgery (ventriculotomy) may be necessary to treat this condition effectively.

At present, several descriptions and single case reports exist regarding ventriculotomy in different avian species. However, with the exception of one study in Japanese quail (Coturnix coturnix japonica), to our knowledge there are no scientifically-based standards for the surgical approach and closure of the avian ventriculus. (2-12) Surgery of the ventriculus has been associated with a high incidence of postoperative complications as well. Complications include leakage at the site of incision, localized infection, and coelomitis. (11) These complications and a lack of surgical guidelines often are reasons why veterinarians avoid gastrointestinal surgery in avian species, thereby missing the potential opportunity to diagnose and treat a disease rapidly. (12)

Difficulties in surgical closure of the ventriculus are caused partially by the specific anatomic and functional peculiarities of the ventriculus in birds. The tendinous part of the ventriculus is not recommended as an incision site because of the high tension on this area. Furthermore, birds lack an omentum, which could be used as a patch to cover the incision as is done in mammals. As an alternative patch, a porcine collagen patch has been evaluated for enhancing ventriculotomy healing in Japanese quail. (12) Results revealed that the porcine collagen patch did not enhance wound healing and may have contributed to leakage at the incision site because of a xenograft rejection response, characterized by predominantly T lymphocytes in the ventricular serosal aggregates adjacent to the collagen patch in all studied quail. Furthermore, regardless of the technique used, different degrees of adhesions were present between the surgical site and fat, abdominal muscles, and viscera in all quail, and accessory lymphoid aggregates in the liver with mild to moderate hepatitis were present in most quail of both treatment groups.

Based on these findings, we wanted to investigate if an autologous patch would result in improved healing after ventriculotomy. The methods in our study were based on the methods used by Ferrell et a1 (12) except that, besides the fat patch, a tension-relieving suture was added in the closure of the ventriculus. We used coelomic fat as a patch in quail, as this is available readily in the coelomic cavity of several bird species. Fat is used as a graft in human reconstructive surgery and as a filler or biologic dressing in neurosurgery. (13,14)

Therefore, the purpose of our study was to assess the impact of an autologous fat patch in addition to a tension-relieving and a simple-interrupted suture in wound healing after ventriculotomy in Japanese quail.

Material and Methods

We used 18 Japanese quail (2 males, 16 females; 10 weeks of age) in this study. The birds were kept in two indoor aviaries (200 x 200 x 150 cm) with a concrete floor. The floor was covered additionally with 10-15 cm of sawdust and branches, which provided natural places to hide, a nest, and a dust bath. The temperature of the aviaries was 16-18[degrees]C (60.8-64.4[degrees]F) with 12 hours of artificial light (100-watt bulbs). Each aviary contained 1 male and 8 female birds. Birds were fed a commercial grain mix for quail with supplemental vegetables (lettuce) and, once weekly, insects (crickets) in feed bowls placed on the floor. Birds were obtained from a commercial breeder 4 weeks before the start of the study. The study was approved by the Animal Care and Use Committee of the Canton of Zurich.

The health of the quail was assessed by body weight measurement and results of physical examination, complete blood cell count, plasma biochemical analysis, fecal investigation for endoparasites by flotation, and bacterial culture for Salmonella species (all using standard techniques). Quail were assigned randomly to 2 groups (n = 9 each), each containing 1 male and 8 female birds. All randomization was performed using a freeware program (available in the public domain at http://www.randomizer.org).

Three hours before surgery, food was withheld. Then, 15 minutes before general anesthesia with isoflurane, butorphanol (2 mg/kg IM; Morphasol-4, Dr. E. Graeub AG, Bern, Switzerland), carprofen (4 mg/kg SC; Rimadyl, Pfizer AG, Zurich, Switzerland), and enrofloxacin (15 mg/kg IM; Baytril Bayer, Berlin, Germany) were given. Enrofloxacin and carprofen were administered daily at the same dosage for 7 days after the surgery.

Anesthesia was induced by face mask with 5% isoflurane, and the birds were intubated and maintained on 1.5% isoflurane. A 24-gauge intravenous catheter was placed in the jugular vein and lactated Ringer's solution (20 mL/kg/h IV) was administered during surgery. The birds were positioned in a dorsal recumbency. After surgical preparation of the site with a 4% chlorhexidine solution, the position of the ventriculus was determined by palpating the coelomic cavity. A 15-mm incision was made in the coelomic midline, starting 5 mm caudal to the sternum. A second incision was made perpendicular to the first incision, running parallel to the last left ribs, creating an inverted "L." The underlying musculature of the body wall was elevated by using Bishop-Harmon tissue forceps, and sharp Metzenbaum scissors were used to incise into the coelomic cavity, entering the posthepatic septum. The ventriculus was visible dorsocranially with surrounding adipose tissue (Fig 1). A stay suture was placed in the lateral thick muscle (Musculus crassus caudodorsalis) with 3/0 poliglecaprone 25 (Monocryl, Ethicon, Johnson & Johnson Medical, Raritan, NJ, USA) on a taper needle, and the ventriculus was lifted closer to the surgical wound. Minimal hemorrhage occurred from disrupting the superficial vessels during this manipulation. The caudal thin muscle (Musculus tenuis caudoventralis) was visualized easily because of its typical elliptic structure and slightly lighter color. A second stay suture was placed on the M. crassus cranioventralis. The ventriculus was isolated as well as possible from the surrounding coelomic cavity by using moist gauze sponges. A full thickness stab incision into the M. tenuis caudoventralis was made by using a #15 scalpel blade (Fig 2), (15) and the incision was enlarged bluntly up to 5-8 mm with small Metzenbaum scissors. The koilin layer of the ventriculus was observed readily and a tip of a sterile cotton swab (5 mm) was inserted easily in the formed opening (to simulate an invasive procedure).

In group 1 birds, the ventriculotomy was closed by using a tension-relieving suture and an appositional simple interrupted suture pattern. The tension-relieving suture as described by Schulz (16) was placed first by using 3/0 poliglecaprone 25 on a taper needle, incorporating the koilin layer, mucosa and submucosa, muscle, and serosa. This was followed by an appositional simple interrupted suture pattern with 4/0 poliglecaprone 25 on a taper needle, through the full thickness of M. tenuis caudoventralis (Fig 3), except for the koilin layer. The coelomic wall and skin were closed by using 4/0 poliglecaprone 25 in a simple continuous suture pattern.

In group 2 birds, after closing the ventriculotomy as described for group 1 birds, a patch of adipose tissue of approximately 5-8 mm thickness was lifted from the surrounding adipose tissue. The patch was placed directly on top of the ventriculotomy site with two simple interrupted sutures with 4/0 poliglecaprone 25 (Fig 4). The coelomic wall and skin were closed as described above.

For anesthetic recovery, quail were kept in a separate cage until fully awake. The birds then were returned to their groups, where they had free access to food and water 2 hours after the surgery.

Three randomly assigned quail from each group were euthanatized at days 7, 14, and 21 after the surgery by intravenous administration of overdose of pentobarbital sodium. Necropsy and histologic examination were performed by the Institute of Veterinary Bacteriology, University of Zurich. The coelomic cavity of each bird was opened, and the ventriculus and all organs showing changes were collected in 10% buffered formalin for further histologic evaluation. Attention was given to the ventriculotomy sites. All samples were evaluated by the same pathologist, and histologic findings were expressed by using a score key for each tissue characteristic (Table 1). The histologic scoring of the individual euthanasia groups was compared by using the Mann-Whitney U test (asymptotic P) in SPSS 16.0 (SPSS, Inc., Chicago, IL, USA).

Results

The presurgical physical and clinical examinations showed no abnormalities. On the day of surgery, the mean body weight of the quail was 305 g. No anesthetic complications were observed during the surgery, and recovery was uneventful. The total duration of anesthesia from the administration of preanesthetic drugs to the time when quail were able to stand on recovery did not exceed 65 minutes. All quail were returned to their groups 2 hours after surgery. After the surgery until the time of euthanasia, all female quail continued to lay eggs and no birds showed any clinical or behavioral abnormalities.

At necropsy, the ventriculotomy site could be identified macroscopically in all birds. Perforations were classified as minor or major by subjective assessment of the pathologist performing the gross and microscopic examinations. A minor perforation was a perforation site where ingesta and tissue reaction was restricted to the ventriculus. A major perforation was dissemination or reaction with adhesions or necrosis involving surrounding tissues. In one bird from group 1 and two birds from group 2, 1 mm of reactive tissue was observed at the incision site. This reaction was classified histologically as minor perforation. No signs of generalized coelomitis, such as coelomic effusion, airsacculitis, or erythema of the surrounding tissues, were detected in any birds. Additionally, in 2 birds from group 2 euthanatized at 7 and 21 days after surgery, respectively, a grey 5 x 5-mm mass with a friable consistency was present at the ventriculotomy site. In one bird, adhesions with the coelomic fat, muscle, and liver were observed; in the second bird, adhesions were with coelomic fat only.

Histologic findings are summarized in Table 2. Until day 21, the ventricular epithelium and submucosa had not healed completely in any of the birds, and varying degrees of incisional inflammation were present in all birds. Bacteria were found within the incision in all birds, and ingesta was found in 12 of 18 (67%) birds. All birds had adhesion formation.

All group 1 birds without the fat patch showed different degrees of adhesion formation between the incision site and fat, with some involvement of coelomic muscle and rarely internal organs. Only two birds from group 2 had adhesions with coelomic muscle. At the 3 time points (days 7, 14, and 21), submucosal repair at the ventricular incision site differed, the degree of which did not appear to be influenced by absence or presence of a coelomic fat patch. There was no association between the level of integrity of the koilin layer and perforation, bacterial growth, or adhesion formation.

In 2 birds from group 1 (one euthanatized on day 7 and the other euthanatized on day 14), pathologic changes were observed macroscopically. In one bird, the presence of bacteria was detected only in the ventricular koilin layer with incisional and serosal necrosis. In the second bird, bacteria and necrosis were present through the incision site. These changes were described as "major perforation."

On statistical analysis of the histologic scoring of the 2 groups, only the scores for serosal inflammation in the group euthanatized at day 21 were significantly different (P = .034), with higher scores in the group 2 birds with the coelomic fat patch.

Discussion

The results of our study in Japanese quail showed that applying a coelomic fat patch over the ventriculotomy incision site appears to result in additional inflammation and does not offer a significant advantage for healing after ventriculotomy in quail. The use of tension-relieving sutures in addition to an appositional simple interrupted suture pattern after ventriculotomy appeared to result in minimal inflammation during healing. The degree of healing and survival in ill birds should be investigated further with clinical trials as well as the use of this ventriculotomy closure technique in other species.

In the study by Ferrell et al, (12) closure of the ventriculus with appositional simple interrupted sutures was compared with the use of porcine-derived collagen patches. Their results revealed a better healing process with a simple interrupted closure pattern. The porcine-derived collagen patches induced signs of xenograft rejection. Regardless of the technique used, all birds had different degrees of adhesions between the surgical site and fat, abdominal muscles, and to some degree, viscera. Accessory lymphoid aggregates in the liver with mild to moderate hepatitis were present in most quail of both treatment groups.

In our study, we made two modifications to the method used by Ferrell et al. (12) The heterologous collagen patch was replaced by an autologous coelomic fat patch, and a tension-relieving suture was added to the simple interrupted suture used to close the ventriculus. Consideration for using a tension-relieving suture as an addition to the routine closure of the ventriculus in our study was based on the assumption that this would have a positive effect on the healing process. The rationale for use of the tension-relieving suture was that the muscular contractions in the ventriculus during digestion produce tension on the sutures, which may result in ischemia and pressure necrosis of underlying tissues. A critique of using a tension-relieving suture in our study is that it represented a potential confounding factor that could have confused interpretation if the study results had shown a difference in outcome between the our study and that with the porcine patch. Furthermore, we hypothesized that using an autologous fat patch instead of a porcine collagen patch would be beneficial in preventing leakage and inflammation. This would reduce adhesion formation with other organs and enhance the healing process after ventriculotomy.

The results of our study showed that ventriculotomy can be performed safely in quail. There were no major surgical complications after performing this procedure in all 18 birds. None of the birds showed signs of generalized coelomitis and all birds survived without showing clinical signs of disease after the surgery up to the day of euthanasia. However, clinical illness might have developed if the birds had been kept alive for more than 21 days. In addition, the use of an antibiotic (enrofloxacin) may have masked signs of leakage at the ventriculotomy site. Because we wanted to follow the method used by Ferrell et al, (12) we used enrofloxacin in our study, but in a future investigation, antibiotic treatment should be omitted.

The only significant difference found between groups 1 and 2 birds was that serosal inflammation was significantly higher in birds with the coelomic fat patch euthanatized at day 21 (group 2) than in birds without the patch (group 1). Therefore, we cannot recommend the use of a fat patch. However, compared with the results of the study by Ferrell et al, (12) inflammation and adhesions appeared to be less in our study. The main difference in the two studies other than the type of patch was the use of a tension-relieving suture in addition to the simple interrupted suture for the closure of the ventriculus. The additional suture material did not result in more inflammation. Therefore, the use of a tension-relieving suture might influence the healing process positively after ventriculotomy and should be considered in future studies.

Based on our results and those of Ferrell et al, (12) the use of patches for ventriculotomy closure cannot be recommended as they appear to result in additional inflammation, regardless of type used. The occurrence of coelomic fat not only depends on the nutritional status of the animal, but also on the species. This affects the application of this method in avian medicine. The finding that an autologous patch induces significant inflammation is of interest. The use of the liver or duodenum has been recommended for serosal patching in birds (7,17); whether these patches result in less inflammation than coelomic fat must be investigated.

Acknowledgments: We thank Dr Marcus Clauss for his advice during the study and statistical analysis, and Jeanne Peter for her anatomic drawings.

References

(1.) Lupu C, Robins S. Comparison of treatment protocols for removing metallic foreign objects from the ventriculus of budgerigars (Melopsittacus undulatus). J Avian Med Surg. 2009;23(3):186-193.

(2.) Bush M, Kennedy S. Ventriculostomy for removal of foreign bodies from sarus cranes. J Am Vet Med Assoc. 1978;173(9):1107-1110.

(3.) Poole C. Surgical treatment of lead poisoning in a mute swan (Cygnus olor). Vet Rec. 1986;119(20): 501-502.

(4.) McCluggage D. Proventriculotomy: a study of select cases. Proc Annu Conf Assoc Avian Vet. 1992;195-200.

(5.) Kummerfeld N. Gastrotomie zur Entfernung von Fremdkorpern aus dem Muskelmagen von Huhnerund Entenvogeln. (Gastrotomies for the removal of foreign bodies from the ventriculus of poultry and water fowl). Kleintierpraxis. 1982;27:49-52.

(6.) Komnenou AT, Georgiades GK, Savvas I, Dessiris A. Surgical treatment of gastric impaction in farmed ostriches. J Vet Med A Physiol Pathol Clin Med. 2003;50(9):474-477.

(7.) Forbes NA. Soft tissue surgery. In: Chitty JR, Lierz M, eds. BSA VA Manual of Raptors, Pigeons and Passerine Birds. Gloucester: British Small Animal Veterinary Association; 2008:143-156.

(8.) Bennett RA, Harrison GJ. Soft tissue surgery. In: Ritchie BW, Harrison GJ, Harrison LR, eds. Avian Medicine: Principles and Application. Lake Worth, FL: Wingers Publishing; 1994:1096-1136.

(9.) Jacobson ER, Ellison GW, McMurphy R, et al. Ventriculostomy for removal of multiple foreign bodies in an ostrich. J Am Vet Med Assoc. 1986;189(9):1117-1119.

(10.) Gasthyus F, De Meurichy W. Successful ventriculostomy for removal of foreign bodies in a kiwi (Apteryx australis mantelli bartlett). J Zoo Anim Med. 1987;18(4):166-167.

(11.) Van Sant F. Surgery of the avian gastrointestinal tract. Semin Avian Exot Pet Med. 1993;2:91-96.

(12.) Ferrell S, Werner J, Kyles A, et al. Evaluation of a collagen patch as a method of enhancing ventriculotomy healing in Japanese quail (Coturnix coturnix japonica). Vet Surg. 2003;32(2):103-112.

(13.) Black P. Cerebrospinal fluid leaks following spinal surgery: use of fat grafts for prevention and repair. J Neurosurg. 2002;96(suppl 2):250-252.

(14.) Coleman SR. Structural fat grafting: more than a permanent filler. Plast Reconstr Surg. 2006;118(3): 108S-120S.

(15.) Konig HE, Feder F, Liebich H-G. Verdauungsapparat (Apparatus digestorius). In: Konig HE, Liebich H-G, eds. Anatomie und Propadeutik des Geflugels (Anatomy and Examination of Birds). Stuttgart: Schattauer; 2001:81-104.

(16.) Schulz K. Management of muscle and tendon injury or disease. In: Fossum TW, ed. Small Animal Surgery. 3rd ed. St. Louis, MO: Elsevier; 2007: 1316-1332.

(17.) Briscoe JA, Bennett RA. Use of a duodenal serosal patch in the repair of a colon rupture in a female Solomon Island eclectus parrot. J Am Vet Med Assoc. 2011;238(7):922-926.

Stefka Simova-Curd, Dr med vet, Dipl ECZM (Avian), Ulrike Foldenauer, Dr med vet, Dipl ECZM (Avian), Tomas Guerrero, Dr med vet, Dipl ECVS, Jean-Michel Hatt, Prof Dr med vet, MSc, Dipl ACZM, Dipl ECZM (Avian), and Richard Hoop, Prof Dr med vet

From the Clinic for Zoo Animals, Exotic Pets and Wildlife, Vetsuisse Faculty, University of Zurich, Winterthurerstrasse 260, 8057 Zurich, Switzerland (Simova-Curd, Foldenauer, Guerrero, Hart); and the Institute of Veterinary Bacteriology, Vetsuisse Faculty, University of Zurich, Winterthurerstrasse 268/270, 8057 Zurich, Switzerland (Hoop).


Table 1. Score keys used for the histologic evaluation of the
surgical site and surrounding tissues after ventriculotomy
in Japanese quail.

                                        Score

   Criterion             0                1                 2

Ventricular        Intact           Small focal      Partial loss of
  epithelium                          defect           layer
Ventricular        Intact without   Fibrotic         Not intact
  submucosa          repair           repair
Incisional         None             Fibrosis only    Fibrosis/chronic
  inflammation
Serosal            None             Mild chronic     Moderate
  inflammation                                         chronic
Presence of        None             Present/giant    Present/
  ingesta                             cells            granulocytes
Presence of        None             Only in koilin   In muscle
  bacteria                            layer
Adhesion           Not present      Fat only         Fat, coelomic
  formation                                            muscle
Koilin layer       Intact           Small focal      Large focal
  integrity                           disruption       disruption
Serosal lymphoid   None             1-5              6-10
  follicles (a)
Perforation        None             Minor            Major
Accessory liver    None             0-1              2-4
  lymphoid
  tissue (a)
Liver              None             Mild chronic     Moderate
  inflammation                                         chronic
  (hepatitis)

                                           Score

   Criterion              3                  4              5

Ventricular        Total loss of      Loss beyond        --
  epithelium         site               repair
Ventricular        --
  submucosa
Incisional         Fibrosis/active    Fibrosis/          Necrosis
  inflammation                          sequestra
Serosal            Active             Severe chronic/    Necrosis
  inflammation                          active
Presence of        --                 --                 --
  ingesta
Presence of        Necrosis           --
  bacteria
Adhesion           Viscera (liver),   --                 --
  formation          fat, coelomic
                     muscle
Koilin layer       Partially absent   Totally absent     --
  integrity
Serosal lymphoid   More than 10       --                 --
  follicles (a)
Perforation        --                 --                 --
Accessory liver    5-8                More than 8        --
  lymphoid
  tissue (a)
Liver              Severe chronic     Active/w           --
  inflammation                          necrosis
  (hepatitis)

(a) Number of aggregates per microscopic field.

Table 2. Histologic evaluation scores of the surgical site after
ventriculotomy in Japanese quail. Group 1: ventriculotomy closure
with tension-relieving suture and appositional simple-interrupted
sutures; Group 2: ventriculotomy closure as described above with a
coelomic fat patch. Three birds from each group were euthanatized
randomly on days 7, 14, and 21 after surgery. See Table 1 for an
explanation of the score keys. The score of each bird is given.

                                                Group 1

           Criterion                Day 7        Day 14       Day 21

                                  4 / 3 / 3    4 / 2 / 0    2 / 1 / 1
Ventricular submucosa             2 / 1 / 1    2 / 2 / 1    1 / 1 / 2
Incisional inflammation           5 / 3 / 3    5 / 5 / 1    1 / 3 / 1
Serosal inflammation              5 / 1 / 2    5 / 1 / 0    1 / 0 / 0
Presence of ingesta               1 / 0 / 1    1 / 1 / 0    0 / 0 / 0
Presence of bacteria              1 / 2 / 2    3 / 3 / 1    1 / 1 / 1
Adhesion formation                3 / 1 / 3    1 / 1 / 1    1 / 1 / 2
Koilin layer integrity            2 / 1 / 1    3 / 3 / 1    1 / 0 / 2
Serosal lymphoid follicles (a)    0 / 0 / 2    1 / 0 / 0    0 / 0 / 0
Perforation                       2 / 0 / 0    2 / 1 / 0    0 / 0 / 0
Accessory liver lymphoid
  tissue (a)                      0 / 0 / 0    0 / 0 / 0    2 / 0 / 0
Liver inflammation (hepatitis)    0 / 0 / 0    0 / 0 / 0    1 / 0 / 1

                                                Group 2

           Criterion                Day 7        Day 14       Day 21

                                  2 / 1 / 2    3 / 2 / 3    2 / 2 / 1
Ventricular submucosa             2 / 1 / 1    1 / 1 / 2    1 / 2 / 1
Incisional inflammation           3 / 1 / 1    2 / 2 / 3    2 / 5 / 1
Serosal inflammation              2 / 1 / 3    1 / 1 / 1    2 / 2 / 2
Presence of ingesta               1 / 1 / 1    1 / 1 / 1    1 / 1 / 0
Presence of bacteria              1 / 1 / 1    1 / 1 / 1    1 / 2 / 1
Adhesion formation                1 / 2 / 1    2 / 1 / 1    1 / 1 / 1
Koilin layer integrity            1 / 1 / 1    1 / 1 / 2    1 / 3 / 1
Serosal lymphoid follicles (a)    0 / 0 / 0    0 / 0 / 0    1 / 1 / 0
Perforation                       0 / 0 / 0    0 / 0 / 1    0 / 1 / 0
Accessory liver lymphoid
  tissue (a)                      0 / 0 / 0    0 / 1 / 0    1 / 1 / 0
Liver inflammation (hepatitis)    1 / 0 / 0    0 / 0 / 0    1 / 0 / 0

(a) Number of aggregates per microscopic field.
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Author:Simova-Curd, Stefka; Foldenauer, Ulrike; Guerrero, Tomas; Hatt, Jean-Michel; Hoop, Richard
Publication:Journal of Avian Medicine and Surgery
Article Type:Report
Date:Mar 1, 2013
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