Pathology in Practice

Jeann Leal de AraujoDepartment of Veterinary Pathobiology, College of Veterinary Medicine and Biomedical Sciences, Texas A&M University, College Station, TX 77843.

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Quinci PlumleeDepartment of Veterinary Pathobiology, College of Veterinary Medicine and Biomedical Sciences, Texas A&M University, College Station, TX 77843.

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Laura KleinschmidtDepartment of Small Animal Clinical Sciences, College of Veterinary Medicine and Biomedical Sciences, Texas A&M University, College Station, TX 77843.

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Sharman M. HoppesDepartment of Small Animal Clinical Sciences, College of Veterinary Medicine and Biomedical Sciences, Texas A&M University, College Station, TX 77843.

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Raquel R. RechDepartment of Veterinary Pathobiology, College of Veterinary Medicine and Biomedical Sciences, Texas A&M University, College Station, TX 77843.

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History and Clinical Findings

An 88-g (0.193-lb) free-living juvenile male mourning dove (Zenaida microura) that had signs of depression and was unable to fly was referred to the Texas A&M University Zoological Medical Service for clinical examination. The dove had fluffed feathers and a quiet behavior. It was thin with a body condition score of 2/5. Seeds were evident in the oral cavity, suggestive of regurgitation. The pericloacal area had fecal debris denoting a lack of self-cleaning. Hematologic analysis revealed a high WBC count (48.3 × 103 cells/μL; reference interval, 10 × 103 cells/μL to 30 × 103 cells/μL) and high total protein concentration (6.0 g/dL; reference interval, 2.1 to 3.3 g/dL), suggestive of an inflammatory reaction and potential infection. The percentage of eosinophils was also high (15%; reference interval, 0% to 1.5%), suggestive of potential parasitism.

The mourning dove was placed in a warm incubator and offered fresh food (seed mix) and water. It was treated with enrofloxacina (5 mg/kg [2.27 mg/lb], SC, q 12 h) and meloxicamb (1 mg/kg [0.45 mg/lb], PO, q 12 h), and was tube fed an omnivore dietc (5 mL, PO, q 12 h).

Two days after admission, the mourning dove developed a firm swelling above the crop that resulted in dyspnea and anorexia, and regurgitation when tube fed. Owing to the deterioration of the bird's general health status and no signs of improvement during treatment; after the bird was anesthetized with isoflurane, euthanasia was performed by injection of 0.5 mL of potassium chloride solution in the venous occipital sinus. Necropsy was performed.

Necropsy Findings

On necropsy, the bird was emaciated with a prominent keel and serous atrophy of fat in the subcutaneous tissue. Mucoid, green to yellow exudate and crust were adhered to the rhinotheca and gnatotheca and extended into the oral cavity. In the caudal portion of the oral cavity, pharynx, and wall of the proximal portion of the esophagus, there was a 1.5 × 1.5 × 2.0-cm, firm, well-demarcated nodule that occluded the proximal portion of the esophageal lumen, narrowed the choana, and deviated the trachea to the left. On cut section, the nodule was tan and filled with caseous material (Figure 1). The crop was distended to 4.5 × 3.0 × 3.0 cm and filled with pale tan to white, friable, inspissated caseous exudate. Other findings included green to yellow and white dried feces and uric acid adhered to feathers surrounding the vent, and a 1.5-cm-diameter focus of hemorrhage was present in the right caudal lung lobe.

Figure 1—
Figure 1—

Photograph of a male juvenile mourning dove (Zenaida microura) that was unable to fly. During clinical observation of 2 days' duration, the bird had consistent regurgitation and developed a firm swelling above the crop. Owing to the progressive deterioration of the bird's clinical condition, it was euthanized. Notice the firm, tan, well-demarcated caseous nodule occluding the cranial esophageal lumen.

Citation: Journal of the American Veterinary Medical Association 253, 11; 10.2460/javma.253.11.1421

Formulate differential diagnoses from the history, clinical findings, and Figure 1—then turn the page

Histopathologic Findings

Various tissue samples were collected for histologic examination. The submucosa of the oral cavity and oropharynx was expanded by a severe, locally extensive inflammatory infiltrate composed of heterophils and macrophages. In the esophagus, the infiltrate extended to the tunica muscularis, tunica adventitia, adjacent skeletal muscle, and subcutaneous tissue (Figure 2). Many ovoid to round, flagellated protozoa with conspicuous 1- to 2-μm-diameter nuclei were scattered throughout the inflammatory infiltrate (Figure 3). Bacteria and foreign plant material were present at the mucosal surface of the inflammatory infiltrate. Pulmonary findings included focal, fibrinoheterophilic, and histiocytic periparabronchial pneumonia. Findings related to emaciation and anorexia were also observed, such as zymogen granule depletion of the pancreas and diffuse, moderate serous atrophy of coelomic adipose tissue. Incidental findings included splenic sinus histiocytosis and hemosiderosis, detection of ventricular intramuscular Sarcocystis cysts, and presence of degenerate intraluminal nematodes within the intestines, which was the most likely cause of the bird's high eosinophil count.

Figure 2—
Figure 2—

Photomicrograph of the nodule from the mourning dove in Figure 1. A focally extensive area of heterophilic and granulomatous infiltrate (asterisk) expands the subcutaneous tissue of the cervical region and extends to the adventitial and submucosal layers of the esophagus. H&E stain; bar = 20 μm.

Citation: Journal of the American Veterinary Medical Association 253, 11; 10.2460/javma.253.11.1421

Figure 3—
Figure 3—

Photomicrographs of protozoa within inflammatory infiltrate in the esophagus of the mourning dove in Figure 1. A—The protozoa are round and 7 to 11 μm in diameter with pale, amphophilic cytoplasm containing 1 small, round, eccentric, hyperchromatic nucleus. H&E stain; bar = 20 μm. B—Warthin-Starry staining highlights the small nucleus (arrows) of the protozoa; the cytoplasm is clear to golden yellow. The organisms have features consistent with Trichomonas gallinae. Warthin-Starry stain; bar = 20 μm.

Citation: Journal of the American Veterinary Medical Association 253, 11; 10.2460/javma.253.11.1421

Morphologic Diagnosis and Case Summary

Morphologic diagnosis: heterophilic and granulomatous stomatitis and esophagitis with intralesional trichomonads.

Case summary: Trichomonas gallinae stomatitis and esophagitis in a mourning dove.

Comments

In the mourning dove of the present report, the gross and histologic lesions were typical of avian trichomoniasis. Avian trichomoniasis is caused by T gallinae infection, which mainly results in caseous or diphtheritic lesions in the upper digestive or respiratory tract, primarily in the oral cavity, pharynx, esophagus, trachea, and crop.1,2 Systemic trichomoniasis is not a frequent finding,3 and T gallinae is not commonly observed in organs caudal to the proventriculus.2,4 Avian trichomoniasis represents a widespread and important avian disease with major medical importance for raptors and pigeons.2,5 In those species, the disease is also known as frounce and canker, respectively.6 Rock pigeons (Columba livia) are the primary host and are responsible for the extensive spread of this protozoal infection5,7; however, other members of the order Columbiformes such as mourning doves and wood pigeons (Columba palumbus) also have an important role in the maintenance and spread of infections with T gallinae.2,8 Transmission of T gallinae in columbiformes is primarily from adults to squabs through the latter's consumption of pigeon milk produced in the crop of the adults, but the disease can also be spread through consumption of contaminated water or food.6 Trichomonas gallinae infection has been less commonly identified in other avian species within the orders Psittaciformes, Corviformes, and Passeriformes but constitutes an important emerging disease in passerines.2,9,10 The frequent loss of habitat for raptors has forced several species to nest in urban areas, which has caused drastic behavior changes such as the incorporation of urban columbiformes in their diets. As a result of this change in diet, an increase in the number of cases of trichomoniasis among raptors has been observed, and this may represent an important population-level threat for several endangered and vulnerable species of birds of prey.11

Trichomonas spp are flagellated protozoa that affect the gastrointestinal or urogenital tract of humans and other animals.12 Two trichomonad species are commonly found in birds but differ in their predilection for anatomic location and avian species affected. Trichomonas gallinae causes caseous lesions in the upper digestive tract of birds of the orders Columbiformes, Falconiformes, and Strigiformes.8 Tetratrichomonas gallinarum is a trichomonad that is usually present in the large intestine of birds of the orders Galliformes and Anseriformes.13,14 Although T gallinarum is generally considered a nonpathogenic protozoan,15,16 there are some reports of hepatic,17 intestinal,18,19 or encephalitic20 tetratrichomoniasis in birds. Recently, another trichomonad that is genetically closer to Trichomonas vaginalis and Trichomonas stableri than to T gallinae has been isolated from bearded vultures (Gypaetus barbatus) and named Trichomonas gypaetinii.21

A quick, easy, and relatively noninvasive diagnostic technique for identification of T gallinae infection in birds is cytologic evaluation of a swab specimen of the caseous oropharyngeal contents; a slide preparation of the swab specimen is stained with Giemsa stain22 for examination. Trophozoites of T gallinae are ovoid or pyriform and range from 7 to 11 μm in length. The nucleus is ovoid and situated close to the basal apparatuses of the flagella.23 Histologic identification of the flagellated protozoa can be challenging, and application of special stains to sections of affected tissues may be helpful.22–24

Differential diagnoses for trichomoniasis include diphtheritic poxvirus infection (wet pox), hypovitaminosis A, and candidiasis. Several features can be helpful in the differentiation of these conditions.25 Poxvirus infection causes epithelial ballooning degeneration and intracytoplasmic, eosinophilic inclusion bodies (Bollinger bodies) within epithelial cells, which are pathognomonic for this condition.26 Hypovitaminosis A causes squamous metaplasia of the esophageal glands and hyperplasia of the mucosa, often associated with secondary infections.27 Candida albicans infection is characterized by white-gray pseudomembranous patches on the oral cavity, mouth, pharynx, esophagus, and crop.24 Histologically, sloughing of the oral and esophageal mucosa and hyphae, pseudohyphae, and budding yeastlike organisms are observed in C albicans–infected tissues.24,25 Although the lesions of these 4 disease conditions may appear grossly similar, the histologic features of trichomoniasis, such as the granulomatous and heterophilic inflammation, allow differentiation even in the absence of identification of the causative agent.10,24,27

Footnotes

a.

Baytril (22.7 mg/mL), Bayer Healthcare LLC, Shawnee Mission, Kan.

b.

Metacam oral suspension (0.5 mg/mL), Boehringer Ingelheim, St Joseph, Mo.

c.

Omnivore critical care, Oxbow Animal Health, Murdock, Neb.

References

  • 1. Ecco R, Preis IS, Vilela DA, et al. Molecular confirmation of Trichomonas gallinae and other parabasalids from Brazil using the 5.8S and ITS-1 rRNA regions. Vet Parasitol 2012;190:3642.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 2. Amin A, Bilic I, Liebhart D, et al. Trichomonads in birds—a review. Parasitology 2014;141:733747.

  • 3. Stabler RM, Engley FB Jr. Studies on Trichomonas gallinae infections in pigeon squabs. J Parasitol 1946;32:225232.

  • 4. Powell EC, Hollander WF. Trichomonas gallinae infections in the ringdove (Streptopelia risoria). J Wildl Dis 1982;18:8990.

  • 5. Stabler RM. Trichomonas gallinae: a review. Exp Parasitol 1954;3:368402.

  • 6. Cole RA. Trichomoniasis. In: Friend M, Franson JC, Ciganovich EA, eds. Field manual of wildlife diseases: general field procedures and diseases of birds. Madison, Wis: United States Geological Survey, 1999:201206.

    • Search Google Scholar
    • Export Citation
  • 7. Harmon WM, Clark WA, Hawbecker AC, et al. Trichomonas gallinae in Columbiform birds from the Galapagos Islands. J Wildl Dis 1987;23:492494.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 8. BonDurant RH, Honigberg BM. Trichomonads of veterinary importance, In: Krieger JN, ed. Parasitic protozoa. New York: Academic Press 1994;111188.

    • Search Google Scholar
    • Export Citation
  • 9. Robinson RA, Lawson B, Toms MP, et al. Emerging infectious disease leads to rapid population declines of common British birds. PLoS One 2010;5:e12215.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 10. Park FJ. Avian trichomoniasis: a study of lesions and relative prevalence in a variety of captive and free-living bird species as seen in an Australian avian practice. Aust Vet J 2011;89:8288.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 11. Krone O, Altenkamp R, Kenntner N. Prevalence of Trichomonas gallinae in northern goshawks from the Berlin area of northeastern Germany. J Wildl Dis 2005;41:304309.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 12. Kunca T, Smejkalova P, Cepicka I. Trichomonosis in Eurasian sparrowhawks in the Czech Republic. Folia Parasitol (Praha) 2015;7:6267.

    • Search Google Scholar
    • Export Citation
  • 13. Brugerolle G, Müller M. Amitochondriate flagellates. In: Leadbeater BSC, Green JC, eds. The flagellates: unity, diversity and evolution. London: Taylor & Francis, 2000;166189.

    • Search Google Scholar
    • Export Citation
  • 14. Cepicka I, Kutisova K, Tachezy J, et al. Cryptic species within the Tetratrichomonas gallinarum species complex revealed by molecular polymorphism. Vet Parasitol 2005;128:1121.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 15. Hess M, McDougald LR. Histomoniasis (Blackhead) and other protozoan diseases of the intestinal tract. In: Swayne DE, Glisson JR, McDougald LR, et al, eds. Diseases of poultry. 13th ed. Ames, Iowa: Wiley, 2013;11721182.

    • Search Google Scholar
    • Export Citation
  • 16. Morishita TY, Schaul JC. Parasites of birds. In: Flynn's parasites of laboratory animals. Baker DG, ed. Hoboken, NJ: Blackwell Publishing, 2007;217301.

    • Search Google Scholar
    • Export Citation
  • 17. Laing ST, Weber ES III, Yabsley MJ, et al. Fatal hepatic tetratrichomoniasis in a juvenile Waldrapp ibis (Geronticus eremita). J Vet Diagn Invest 2013;25:277281.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 18. Richter B, Schulze C, Kammerling J, et al. First report of typhlitis/typhlohepatitis caused by Tetratrichomonas gallinarum in three duck species. Avian Pathol 2010;39:499503.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 19. Tsai SS, Chang TC, Kuo M, et al. Respiratory and intestinal trichomoniasis in mule ducks. Avian Pathol 1997;26:651656.

  • 20. Patton CS, Patton S. Tetratrichomonas gallinarum encephalitis in a mockingbird (Mimus polyglottos). J Vet Diagn Invest 1996;8:133137.

  • 21. Martínez-Díaz RA, Ponce-Gordo F, Rodríguez-Arce I, et al. Trichomonas gypaetinii n. sp., a new trichomonad from the upper gastrointestinal tract of scavenging birds of prey. Parasitol Res 2015;114:101112.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 22. Borji H, Razmi GH, Movassaghi AH, et al. Prevalence and pathological lesion of Trichomonas gallinae in pigeons of Iran. J Parasit Dis 2011;35:186189.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 23. Mehlhorn H, Al-Quraishy S, Aziza A, et al. Fine structure of the bird parasites Trichomonas gallinae and Tetratrichomonas gallinarum from cultures. Parasitol Res 2009;105:751756.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 24. Schmidt RE, Reavill DR, Phalen DN. Gastrointestinal system and pancreas. In: Pathology of pet and aviary birds. 2nd ed. Ames, Iowa: Wiley Blackwell, 2015;6263.

    • Search Google Scholar
    • Export Citation
  • 25. Arenales A, Almeida ACO, Prado LF, et al. Cytopathology in the diagnosis of oral trichomoniasis in a rock pigeon (Columba livia). Braz J Vet Pathol 2014;7:9899.

    • Search Google Scholar
    • Export Citation
  • 26. Weli SC, Tryland M. Avipoxviruses: infection biology and their use as vaccine vectors. Virol J 2011;8:49.

  • 27. Mugale M, Bhat AA, Gavhane DS, et al. Outbreaks of thrush in pigeons in Punjab State of India. Comp Clin Path 2015;24:635638.

Contributor Notes

Address correspondence to Dr. Leal de Araujo (lealjeann@gmail.com).
  • View in gallery
    Figure 1—

    Photograph of a male juvenile mourning dove (Zenaida microura) that was unable to fly. During clinical observation of 2 days' duration, the bird had consistent regurgitation and developed a firm swelling above the crop. Owing to the progressive deterioration of the bird's clinical condition, it was euthanized. Notice the firm, tan, well-demarcated caseous nodule occluding the cranial esophageal lumen.

  • View in gallery
    Figure 2—

    Photomicrograph of the nodule from the mourning dove in Figure 1. A focally extensive area of heterophilic and granulomatous infiltrate (asterisk) expands the subcutaneous tissue of the cervical region and extends to the adventitial and submucosal layers of the esophagus. H&E stain; bar = 20 μm.

  • View in gallery
    Figure 3—

    Photomicrographs of protozoa within inflammatory infiltrate in the esophagus of the mourning dove in Figure 1. A—The protozoa are round and 7 to 11 μm in diameter with pale, amphophilic cytoplasm containing 1 small, round, eccentric, hyperchromatic nucleus. H&E stain; bar = 20 μm. B—Warthin-Starry staining highlights the small nucleus (arrows) of the protozoa; the cytoplasm is clear to golden yellow. The organisms have features consistent with Trichomonas gallinae. Warthin-Starry stain; bar = 20 μm.

  • 1. Ecco R, Preis IS, Vilela DA, et al. Molecular confirmation of Trichomonas gallinae and other parabasalids from Brazil using the 5.8S and ITS-1 rRNA regions. Vet Parasitol 2012;190:3642.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 2. Amin A, Bilic I, Liebhart D, et al. Trichomonads in birds—a review. Parasitology 2014;141:733747.

  • 3. Stabler RM, Engley FB Jr. Studies on Trichomonas gallinae infections in pigeon squabs. J Parasitol 1946;32:225232.

  • 4. Powell EC, Hollander WF. Trichomonas gallinae infections in the ringdove (Streptopelia risoria). J Wildl Dis 1982;18:8990.

  • 5. Stabler RM. Trichomonas gallinae: a review. Exp Parasitol 1954;3:368402.

  • 6. Cole RA. Trichomoniasis. In: Friend M, Franson JC, Ciganovich EA, eds. Field manual of wildlife diseases: general field procedures and diseases of birds. Madison, Wis: United States Geological Survey, 1999:201206.

    • Search Google Scholar
    • Export Citation
  • 7. Harmon WM, Clark WA, Hawbecker AC, et al. Trichomonas gallinae in Columbiform birds from the Galapagos Islands. J Wildl Dis 1987;23:492494.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 8. BonDurant RH, Honigberg BM. Trichomonads of veterinary importance, In: Krieger JN, ed. Parasitic protozoa. New York: Academic Press 1994;111188.

    • Search Google Scholar
    • Export Citation
  • 9. Robinson RA, Lawson B, Toms MP, et al. Emerging infectious disease leads to rapid population declines of common British birds. PLoS One 2010;5:e12215.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 10. Park FJ. Avian trichomoniasis: a study of lesions and relative prevalence in a variety of captive and free-living bird species as seen in an Australian avian practice. Aust Vet J 2011;89:8288.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 11. Krone O, Altenkamp R, Kenntner N. Prevalence of Trichomonas gallinae in northern goshawks from the Berlin area of northeastern Germany. J Wildl Dis 2005;41:304309.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 12. Kunca T, Smejkalova P, Cepicka I. Trichomonosis in Eurasian sparrowhawks in the Czech Republic. Folia Parasitol (Praha) 2015;7:6267.

    • Search Google Scholar
    • Export Citation
  • 13. Brugerolle G, Müller M. Amitochondriate flagellates. In: Leadbeater BSC, Green JC, eds. The flagellates: unity, diversity and evolution. London: Taylor & Francis, 2000;166189.

    • Search Google Scholar
    • Export Citation
  • 14. Cepicka I, Kutisova K, Tachezy J, et al. Cryptic species within the Tetratrichomonas gallinarum species complex revealed by molecular polymorphism. Vet Parasitol 2005;128:1121.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 15. Hess M, McDougald LR. Histomoniasis (Blackhead) and other protozoan diseases of the intestinal tract. In: Swayne DE, Glisson JR, McDougald LR, et al, eds. Diseases of poultry. 13th ed. Ames, Iowa: Wiley, 2013;11721182.

    • Search Google Scholar
    • Export Citation
  • 16. Morishita TY, Schaul JC. Parasites of birds. In: Flynn's parasites of laboratory animals. Baker DG, ed. Hoboken, NJ: Blackwell Publishing, 2007;217301.

    • Search Google Scholar
    • Export Citation
  • 17. Laing ST, Weber ES III, Yabsley MJ, et al. Fatal hepatic tetratrichomoniasis in a juvenile Waldrapp ibis (Geronticus eremita). J Vet Diagn Invest 2013;25:277281.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 18. Richter B, Schulze C, Kammerling J, et al. First report of typhlitis/typhlohepatitis caused by Tetratrichomonas gallinarum in three duck species. Avian Pathol 2010;39:499503.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 19. Tsai SS, Chang TC, Kuo M, et al. Respiratory and intestinal trichomoniasis in mule ducks. Avian Pathol 1997;26:651656.

  • 20. Patton CS, Patton S. Tetratrichomonas gallinarum encephalitis in a mockingbird (Mimus polyglottos). J Vet Diagn Invest 1996;8:133137.

  • 21. Martínez-Díaz RA, Ponce-Gordo F, Rodríguez-Arce I, et al. Trichomonas gypaetinii n. sp., a new trichomonad from the upper gastrointestinal tract of scavenging birds of prey. Parasitol Res 2015;114:101112.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 22. Borji H, Razmi GH, Movassaghi AH, et al. Prevalence and pathological lesion of Trichomonas gallinae in pigeons of Iran. J Parasit Dis 2011;35:186189.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 23. Mehlhorn H, Al-Quraishy S, Aziza A, et al. Fine structure of the bird parasites Trichomonas gallinae and Tetratrichomonas gallinarum from cultures. Parasitol Res 2009;105:751756.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 24. Schmidt RE, Reavill DR, Phalen DN. Gastrointestinal system and pancreas. In: Pathology of pet and aviary birds. 2nd ed. Ames, Iowa: Wiley Blackwell, 2015;6263.

    • Search Google Scholar
    • Export Citation
  • 25. Arenales A, Almeida ACO, Prado LF, et al. Cytopathology in the diagnosis of oral trichomoniasis in a rock pigeon (Columba livia). Braz J Vet Pathol 2014;7:9899.

    • Search Google Scholar
    • Export Citation
  • 26. Weli SC, Tryland M. Avipoxviruses: infection biology and their use as vaccine vectors. Virol J 2011;8:49.

  • 27. Mugale M, Bhat AA, Gavhane DS, et al. Outbreaks of thrush in pigeons in Punjab State of India. Comp Clin Path 2015;24:635638.

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