A review of the most common pathologies of the stomach in laboratory animals in preclinical studies of drugs

DOI: 10.29296/2618723X-2020-02-02

J.U. Ustenko, Pathomorphologist, Department of Histology and Pathomorphology, ORCID 0000-0003-1299-0200
Y.A. Gushchin, Head of the Department of Histology and Pathomorphology, ORCID 0000-0002-7656-991X

Research and manufacturing company «Home оf Pharmacy»,
188663, Russia, Leningradskiy region, Vsevolozhskiy district, Kuzmolovskiy t.s., Zavodskaya st. 3–245

Е-mail: [email protected]

 


Keywords: pathology of the stomach laboratory animals pathomorphology in preclinical studies

For citation:

Ustenko J.U., Gushchin Y.A. A review of the most common pathologies of the stomach in laboratory animals in preclinical studies of drugs. Laboratory Animals for Science. 2020; 2. https://doi.org/10.29296/2618723X-2020-02-02

Abstract

Pathomorphological analysis is an integral part of preclinical studies. It allows evaluating the pathological changes that occur in the organs of laboratory animals at macroscopic and microscopic levels. Gastric pathology can develop due to the local irritating effect of the test articles during peroral and intragastric administration, as a spontaneous or background pathology, due to various mechanisms with other routes of administration (intramuscular, subcutaneous, intraperitoneal and others). The classification and morphological criteria of gastric pathology in laboratory animals are most fully developed by the INHAD group for rats and mice. Clear recommendations have not been developed for other animal species yet. Orientation of toxic pathologists to a unified classification will be avoiding confusion in interpretations, will be ensuring reproducibility of results, and will allow comparing of the results of various researchers. А possible classification of gastric pathologies in laboratory animals in preclinical studies is presented in the article. It is based on an analysis of literary sources. Congenital pathologies such as squamous cysts and ectopic tissues are described.

Atrophic and hypertrophic changes in the mucous membrane; metaplastic changes; dystrophic changes, such as vacuolization; detection of eosinophilic globules, mineralization, amyloidosis; the formation of glandular cysts and diverticulum in the epithelium of the stomach are considered. Аpplication of additional microscopic examination techniques described: immunohistochemical staining for TFF2, CDX1 and CDX2 for differentiation of metaplastic shifts; Congo red stained to verify the diagnosis of amyloidosis. Apoptosis and necrosis of а stomach epithelium are also described in detail. Since these processes are indistinguishable during the evaluating routine sections stained with hematoxylin-eosin, additional methods (transmission electron microscopy, DNA-laddering, TUNEL, immunohistochemistry for caspases, (in particular, caspase-3) are listed. They allow to accurately differentiate apoptosis and necrosis. Inflammatory changes are described: inflammatory infiltrate and inflammation. А gastric dilatation, volvulus, detection of trichobesoars in the lumen of the stomach also are considered. For each pathology, an illustration, a brief macroscopic and microscopic characteristic is given. Possible causes of stomach pathologies in rats, mice, hamsters, gerbils, ferrets, rabbits, dwarf pigs in preclinical studies are described.

Full text avaliable in Russain only

Authors contribution:

Zh. Ustenko – literature analysis, writing the article, editing the article, providing of the photo materials.

Ya. Gushchin – idea of the research, editing the article, providing of the photo materials.

Acknowledgements. The study was performed without external funding.

 

 

References

  1. McInnes E., Pathology for Toxicologists. – John Wiley & Sons. 2017. 216 p.
  2. Nolte, T. Brander-Weber P., Dangler C., Deschl U., Elwell M. R., Greaves P., Hailey R., Leach M. W., Pandiri A. R., Rogers A., Shackelford C. C., Spencer A., Tanaka T., Ward J. M. Nonproliferative and Proliferative Lesions of the Gastrointestinal Tract, Pancreas and Salivary Glands of the Rat and Mouse // Journal of Toxicologic Pathology. 2016; 29 (1):1-125. doi: 10.1293/tox.29.1S.
  3. Макаров М.Н., Рыбакова А.В., Гущин Я.А., Шедько В.В., Мужикян А.А., Макаров В.Г. Анатомо-физиологическая характеристика пищеварительного тракта у человека и лабораторных животных // Международный вестник ветеринарии. 2016; 1: 82-104. [Makarov M.N., Rybakova A.V., Gushchin Ya.A., Shed'ko V.V., Muzhikyan A.A., Makarov V.G. Anatomo-fiziologicheskaya kharakteristika pishchevaritel'nogo trakta u cheloveka i laboratornykh zhivotnykh // Mezhdunarodnyi vestnik veterinarii. (In Russ.)].
  4. Greaves P. Histopathology of preclinical toxicity studies. Interpretation and relevance in drug safety evaluation. 4th Edition. – Amsterdam. Elsevier. 2011. 892 p.
  5. Jeppesen, G., Skydsgaard, M. Spontaneous Background Pathology in Göttingen Minipigs // Toxicologic Pathology. 2014; 43(2): 257–266. doi:10.1177/0192623314538344.
  6. Kuwamura M., Okajima R., Yamate J., Kotani T., Kuramoto T., Serikawa T. Pancreatic metaplasia in the gastro-achlorhydria in WTC-dfk rat, a potassium channel Kcnq1 mutant // Veterinary Pathology. 2008; 45(4): 586–591. doi:10.1354/vp.45-4-586.
  7. Maekawa A., Enomoto M., Hirouchi Y., Yamakawa S. Changes in the upper digestive tract and stomach. In: Pathobiology of the Aging Mouse. V2. / Edited by U. Mohr – Washington. ILSI Press. 1996. 505 p.
  8. Leininger J.R., McDonald M.M., Abbott D.P. Hepatocytes in the mouse stomach // Toxicologic Pathology. 1990; 18(4 Pt 2):678-86.
  9. McInnes E.F. Background lesions in laboratory animals. A color atlas – 1st ed. – Edinburgh, Elsevier. 2012. 256 p.
  10. Nonneoplastic Lesion Atlas [электронный ресурс]: National Toxicology Program Nonneoplastic Lesion Atlas. – Режим доступа: https://ntp.niehs.nih.gov/nnl/index.htm
  11. Radi Z.A., Vogel M.W. Gastric Parietal Cell Atrophy and Depletion after Administration of a Sphingosine-1-Phosphate 1 Inhibitor // Toxicologic Pathology. 2014; 42: 118-123. doi: 10.1177/0192623313506790.
  12. Dethloff L.A., Robertson D.G., Tierney B.M., Breider M.A., Bestervelt L. L. Gastric gland degeneration induced in monkeys by the CCK-B/gastrin receptor antagonist CI-988 // Toxicologic Pathology. 1997; 25: 441–448. doi: 10.1177/019262339702500502.
  13. Bleich A., Kohn I., Glage S., Beil W., Wagner S., Mähler M. Multiple in vivo passages enhance the ability of a clinical Helicobacter pylori isolate to colonize the stomach of Mongolian gerbils and to induce gastritis //Laboratory Animals. 2005; 39 (2): 221-229. doi: 10.1258/0023677053739800.
  14. Hong F., Wu N., Zhou Y., Ji L., Chen T., Wang L. Gastric toxicity involving alterations of gastritis-related protein expression in mice following long-term exposure to nano TiO 2 // Food Research International. 2017; 95: 38–45. doi:10.1016/j.foodres.2017.02.013.
  15. Hollander D., Tarnawski A., Stachura J., Gergely, H. Morphologic changes in gastric mucosa of aging rats // Digestive Diseases and Sciences. 1989; 34(11), 1692–1700. doi:10.1007/bf01540046.
  16. Rogers A.B., Houghton J-M. Helicobater-based models of digestive system carcinogenesis // Methods in molecular biology– 2009; 511:267-95. doi: 10.1007/978-1-59745-447-6_11.
  17. Rogers A.B. Histologic scoring of gastritis and gastric cancer in mouse models // Methods in molecular biology. 2012; 921: 189–203. doi: 10.1007/978-1-62703-005-2_22.
  18. Fox J.G., Rogers A.B., Whary M.T., Ge Z., Ohtani M., Jones E.K., Wang T. C. Accelerated progression of gastritis to dysplasia in the pyloric antrum of TFF2 -/- C57BL6 x Sv129 Helicobacter pylori-infected mice // The American Journal of Pathology. 2007; 171: 1520–1528. doi: 10.2353/ajpath.2007.070249.
  19. Brown H,R,, Hardisty J.F. Oral Cavity, Esophagus, and Stomach. In: Pathology of the Fischer Rat: Reference and Atlas // Edited by Boorman G.A. – San Diego, Academic Press, 1990. 580 p.
  20. Bertram T.A., Ludlow J.W., Basu J., Muthupalani S. Gastrointestinal Tract. In: Handbook of Toxicologic Pathology. 3rd Edition / Edited by W.M. Haschek, C.G. Rousseaux, M.A. Wallig. – San Diego, Academic Press. 2013. 2963 p.
  21. Yoshimura K., Delbarre S.G., Kraus E., Boland C.R The effects of omeprazole and famotidine on mucin and PGE2 release in the rat stomach // Alimentary Pharmacology & Therapeutics. 1996; 10: 111–117. doi:10.1111/j.1365-2036.1996.tb00184.x.
  22. McKee J.S, Gass J.H. Acetaminophen-Induced Forestomach Lesion in Normal Rats Following Intravenous Exposure // Toxicologic Pathology. 2011; 39: 861-866. doi:10.1177/0192623311413789.
  23. Sano T., Ozaki K., Kodama Y., Matsuura T. Effects of the antifungal agent itraconazole on proliferative changes of the forestomach mucosa in alloxan-induced diabetic rats // Toxicologic Pathology. 2009; 37: 790. doi:10.1177/0192623309344204.
  24. Hibino T., Hirasawa Y., Arai M. Morphologic changes in the urinary bladder and stomach after long-term administration of sodium saccharin in F344 rats // Cancer Letters. 1985; 29:255-63. doi:10.1016/0304-3835(85)90135-1.
  25. Levin S. Structural changes of the gastrointestinal mucosa induced by prostaglandins // Toxicologic Pathology. 1988; 16:237-44. doi:10.1177/019262338801600216.
  26. Kramer AW, Dougherty WJ, Belson AR, Iatropoulos MJ. Morphologic changes in the gastric mucosa of rats and dogs treated with an analog of prostaglandin E1. Toxicologic Pathology 1985; 13:26. doi:10.1177/019262338501300105
  27. Kotsonis F.N., Dodd D.C., Regnier B., Kohn F.E. Preclinical toxicology profile of misoprostol // Digestive Diseases and Sciences. 1985; 30:142-5. doi:10.1007/BF01309401.
  28. Toxicology and carcinogenesis studies of ampicillin trihydrate in F344/N rats and B6C3F1 mice. In National toxicology program technical report. 1987; 318:1-190.
  29. Iverson F., Truelove J., Nera E., Wong J., Lok E., Clayson D.B. An 85-day study of butylated hydroxyanisole in the cynomolgus monkey // Cancer Letters. 1985; 26:43. doi: 10.1016/0304-3835(85)90171-5.
  30. Feyen B., Penard L., van Heerden M., Fant P. E,. Marsdenb De Jonghea S., Desmidta M., S. Maki, Graham M., Baileya P. “All pigs are equal” Does the background data from juvenile Göttingen minipigs support this? // Reproductive Toxicology. 2016; 64: 105–115. doi:10.1016/j.reprotox.2016.04.019.
  31. Dänicke S., Beineke A., Berk A., Kersten S. Deoxynivalenol (DON) Contamination of Feed and Grinding Fineness: Are There Interactive Implications on Stomach Integrity and Health of Piglets? // Toxins. 2017; 9(1): 16. doi:10.3390/toxins9010016.
  32. Dean H. P., Stephen W. B. Pathology of laboratory rodents and rabbits —3rd ed. – Wiley-Blackwell. 2007. 325 p.
  33. Yu J., Russell M., Salomon N., Murphy J. Effect of Helicobacter mustelase infection on ferret gastric epithelial cell proliferation // Carcinogenesis. 1995; 16(8): 1927–1931. doi: 10.1093/carcin/16.8.1927.
  34. Bock P., Peters M., Bago Z., Wolf P. Thiele A., Baumgärtner W. Spontaneously occurring alimentary osteofluorosis associated with proliferative gastroduodenopathy in rabbits // Veterinary Pathology. 2007; 44(5): 703–706. doi:10.1354/vp.44-5-703.
  35. Kinoshita H., Hayakawa Y., Konishi M., Hata M. Tsuboi M., Hayata Y., Hikiba Y., Ihara S., Nakagawa H., Ikenoue T., Ushiku T., Fukayama M., Hirata Y., Koike K. Three types of metaplasia models through Kras activation, Pten deletion, or Cdh1 deletion in the gastric epithelium // The Journal of Pathology. 2019; 247(1):35-47. doi:10.1002/path.5163.
  36. Duckworth C. A., Burkitt M. D., Williams J. M., Parsons B. N., Tang J.M. F., Mark D. Pritchard Murine Models of Helicobacter(pylori or felis)-associated Gastric Cancer // Current Protocols in Pharmacology. 2015; 69: 14.34.1–14.34.35. doi: 10.1002/0471141755.ph1434s69.
  37. Goldenring J.R., Nomura S. Differentiation of the gastric mucosa III. Animal models of oxyntic atrophy and metaplasia // American Journal of Physiology: Gastrointestinal and Liver Physiology. 2006; 291(6):999-1004. doi: 10.1152/ajpgi.00187.2006.
  38. Ghanayem B.I., Maronpot R.R., Matthews H.B Ethyl acrylate-induced gastric toxicity. I. Effect of single and repetitive dosing // Toxicology and Applied Pharmacology. 1985; 80(2):323-35. doi: 10.1016/0041-008x(85)90090-0.
  39. Thompson C.M., Suh M., Proctor D.M., Chappell G., Borghoff S., Ellis-Hutchings R., Wiench K., Finch L. Assessment of the mode of action underlying development of forestomach tumors in rodents following oral exposure to ethyl acrylate and relevance to humans // Regulatory Toxicology and Pharmacology. 2018; 96; 178–189. doi:10.1016/j.yrtph.2018.05.006.
  40. Karam S.M, Alexander G. Blocking of histamine H2 receptors enhances parietal cell degeneration in the mouse stomach // Histology and Histopathology/ 2001; 16: 469–480. doi: 10.14670/HH-16.469
  41. Ito K., Ishida K., Shishido T., Tabata H., Miura H., Okamiya H., Hanada T. Acute parietal and chief cell changes induced by a lethal dose of lipopolysaccharide in mouse stomach before thrombus formation // Toxicologic Pathology. 2000; 28: 304–309. doi:10.1177/019262330002800210.
  42. Brown H.R., Leininger J.R. Changes in the Oral Cavity. In: Pathobiology of the Aging Rat / Edited by U. Mohr. – Washington, ILSI Press.1994. 647 p.
  43. Ward J.M., Yoon M., Anver M.R., Haines D.C., G. Kudo, Gonzalez F. J., Kimura S. Hyalinosis and Ym1/Ym2 gene expression in the stomach and respiratory tract of 129S4/SvJae and wild-type and CYP1A2-null B6, 129 mice // The American Journal of Pathology. 2001; 158: 323–332. doi: 10.1016/S0002-9440(10)63972-7.
  44. Bertram T.A, Markovits J.E, Juliana M.M. Non-proliferative lesions of the alimentary canal in rats. In Guides for Toxicologic Pathology. – Washington. STP/ARP/AFIP.1996. 16 p.
  45. Betton G.R, Dormer C.S, Wells T., Pert P., Price C. A., Buckley P. Gastric ECL-cell hyperplasia and carcinoids in rodents following chronic administration of H2-antagonists SK&F 93479 and oxmetidine and omeprazole // Toxicologic Pathology. 1988; 16: 288–298. doi:10.1177/019262338801600222.
  46. Majeed S.K. Survey on spontaneous systemic amyloidosis in aging mice. Arzneimittel-forschung. 1993;43(2):170-8.
  47. Lipman R.D., Gaillard E.T., Harrison D.E., Bronson R.T. Husbandry factors and the prevalence of age-related amyloidosis in mice // Laboratory animal science. 1993; 43(5):439-44.
  48. Kangawa A., Nishimura T., Nishimura T., Otake M., Enya S., Yoshida T., Shibata M. Spontaneous Age-Related Histopathological Changes in Microminipigs // Toxicologic Pathology. 2019; 47(7):817-832. doi: 10.1177/0192623319861350.
  49. Sano, K. Experimental amyloidosis induced by saponin // Acta Pathologica Japonica. 1988; 38(10), 1241–1253. doi:10.1111/j.1440-1827.1988.tb02276.x.
  50. Kobayashi Y., Shimada Y., Terasawa K. Amyloid deposition in the digestive tract in casein-induced experimental amyloidosis in mice // Journal of Gastroenterology. 1994; 29(1), 6–14. doi:10.1007/bf01229066.
  51. Snel F.W., Niewold T.A., Baltz M.L., Hol P.R., Van Ederen A. M., Pepys M. B., Gruys E. Experimental amyloidosis in the hamster: correlation between hamster female protein levels and amyloid deposition // Clinical and Experimental Immunology. 1989; 76(2):296-300.
  52. Leininger J.R., Jokinen M.P., Dangler C.A., Whiteley L.O. Oral Cavity, esophagus and stomach. In: Pathology of the Mouse // Edited by R.R. Maronpot. – Vienna, Cache River Press. 1999. 699 p.
  53. Rees J., Spencer A., Wilson S., Reid A., Harpur E. Time Course of Stomach Mineralization, Plasma, and Urinary Changes After a Single Intravenous Administration of Gadolinium(III) Chloride in the Male Rat // Toxicologic Pathology. 1997; 25(6), 582–589. doi:10.1177/019262339702500607.
  54. Diaz D., Allamneni K., Tarrant J. M., Lewin-Koh S.-C., Pai R., Dhawan P., Cain G. R., Kozlowski C., Hiraragi H., La N., Hartley D.P., Ding X.,. Dean B. J, Bheddah S., Dambach D. M. Phosphorous Dysregulation Induced by MEK Small Molecule Inhibitors in the Rat Involves Blockade of FGF-23 Signaling in the Kidney // Toxicological Sciences. 2011; 125(1): 187–195. doi:10.1093/toxsci/kfr263.
  55. Chang L., Yue Z., She R., Sun Y., Zhu J. The toxic effect of a mixture of melamine and cyanuric acid on the gastrointestinal tract and liver in mice // Research in Veterinary Science. 2015; 102: 234–237. doi:10.1016/j.rvsc.2015.08.018.
  56. Elmore S.A., Dixon D., Hailey J.R., Harada T., Herbert R. A., Maronpot R. R., Nolte T., Rehg J. E., Rittinghausen S., Rosol T.J., Satoh H., Vidal J. D., Willard-Mack C. L., Creasy D.M. Affiliations expand Recommendations from the INHAND Apoptosis/Necrosis Working Group // Toxicologic Pathology. 2016; Feb;44(2):173-88. doi: 10.1177/0192623315625859.
  57. Elmore, S.A. Apoptosis: A Review of Programmed Cell Death // Toxicologic Pathology. 2007; 35(4); 495–516. doi:10.1080/01926230701320337.
  58. Stokar-Regenscheit N., Sydler T., Bürgi E., Lippuner A., Naegeli H., Sidler X. Lethal Gastric Mucosal Necrosis due to Administration of Oral Ferrous Bisglycinate Chelate to Suckling Piglets // Journal of Comparative Pathology. 2017; 157(1): 39–45. doi:10.1016/j.jcpa.2017.04.004.
  59. Magalhaes M.A., Barbosa A.J., Figueiredo J.A., Alberti L.R., Petroianu A. Effects of different periods of gastric ischaemia in the viability of the tissue of body, fundus and antrum region of rabbit stomach // Arquivos Brasileiros de Cirurgia Digestiva. 2015; 28(3):167-70. doi: 10.1590/S0102-67202015nahead00001.
  60. Friendship, R.M. Gastric ulceration in swine // Journal of Swine Health and Production. 2004; 12: 34–35.
  61. Swindle M.M., Makin A., Herron A.J., Clubb F.J. Jr. Swine as Models in Biomedical Research and Toxicology Testing // Veterinary Pathology. 2011; 49(2): 344–356. doi:10.1177/0300985811402846.
  62. Kumar, G., Hota, D., Nahar Saikia, U. Evaluation of analgesic efficacy, gastrotoxicity and nephrotoxicity of fixed-dose combinations of nonselective, preferential and selective cyclooxgenase inhibitors with paracetamol in rats // Experimental and Toxicologic Pathology. 2010; 62(6): 653–662. doi:10.1016/j.etp.2009.08.011.
  63. Tabata K., Okabe S. Effects of 16,16-Dimethyl-PGE2-Methyl Ester on Aspirin- and Indomethacin-Induced Gastric and Intestinal Lesions in Mini Pigs // Digestion. 1983; 26(2): 61–66. doi:10.1159/000198869/
  64. Yoshida N., Sugimoto N., Hirayama F., Nakamura Y., Ichikawa H., Naito Y., Yoshikawa T. Helicobacter pylori infection potentiates aspirin induced gastric mucosal injury in Mongolian gerbils // Gut. 2002; 50(5): 594–598. doi:10.1136/gut.50.5.594.
  65. Paxton B.E., Alley C.L., Crow J.H., Burchette J., Weiss C.R. , Kraitchman D.L., Arepally A., Kim C. Y. Histopathologic and Immunohistochemical Sequelae of Bariatric Embolization in a Porcine Model // Journal of Vascular and Interventional Radiology. 2014; 25(3): 455–461. doi: 10.1016/j.jvir.2013.09.016.
  66. Fujishiro M., Yahagi N., Kashimura K., Matsuura T. Tissue damage of different submucosal injection solutions for EMR // Gastrointestinal Endoscopy. 2005; 62(6): 933–942. doi:10.1016/j.gie.2005.07.052.
  67. Palus K., Bulc M., Całka J. Changes in VIP-, SP- and CGRP- like immunoreactivity in intramural neurons within the pig stomach following supplementation with low and high doses of acrylamide // Neurotoxicology. 2018; 69: 47–59. doi:10.1016/j.neuro.2018.09.002.
  68. Pfeiffer C. J., & Weibel J. The gastric mucosal response to acetylsalicylic acid in the ferret // The American Journal of Digestive Diseases. 1973; 18(10): 834–846. doi:10.1007/bf01073333.
  69. Beach, J.E. The ferret for non-rodent toxicity studies - a pathologist's view // Archives of Toxicology. 1982; 5:279-82.
  70. David Perpinan, Cathy A. Johnson-Delaney, Ferret medicine and surgery // Edited by Cathy A. Johnson-Delaney. – ‎Boca Raton, Florida. CRC Press, 2018. 514 p.
  71. Redfern J.S., Lin H.J., McArthur K.E., Prince M. D., Feldman M. Gastric acid and pepsin secretion in conscious rabbits // American Journal of Physiology. 1991; 261:G295–304. doi: 10.1152/ajpgi.1991.261.2.G295.
  72. Hinton M. Gastric ulceration in the rabbit // Journal of Comparative Pathology. 1980; 90:475–81. doi: 10.1016/0021-9975(80)90017-1.
  73. Man W.K., Silcocks P.B., Wales R., Spencer J. Histology of experimental stress ulcer: the effects of cimetidine on adrenaline gastric lesions in the rabbit // British journal of experimental pathology 1981; 62(4):411–8.
  74. Collin B.J. Stress ulcer induced by hypovolemic shock in female rabbit. Anatomia, Histologia, Embryologia. 1977; 6(1): 94.
  75. Saganuwan, S. A., Orinya, O. A. Toxico-neurological effects of piroxicam in monogastric animals // Journal of Experimental Neuroscience. 2016; (10):121 doi:10.4137/jen.s40144.
  76. Helke K.L., Nelson K.N., Sargeant A.M., Jacob B., McKeag S., Haruna J., Vemireddi V., Greeley M., Brocksmith D., Navratil N., Stricker-Krongrad A., Hollinger C. Background Pathological Changes in Minipigs: A Comparison of the Incidence and Nature among Different Breeds and Populations of Minipigs // Toxicologic Pathology. 2016; 44(3): 325-337. doi: 10.1177/0192623315611762.
  77. Birck M.M., Vegge A., Moesgaard S.G., Eriksen T. Single port laparoscopic long-term tube gastrostomy in Gottingen minipigs // Laboratory Animals. 2015; 49(3): 220–227. doi: 10.1177/0023677214562097.
  78. Giday S., Van Alstine W., Van Vleet J., Ducharme R. Safety Analysis of a Hemostatic Powder in a Porcine Model of Acute Severe Gastric Bleeding // Digestive Diseases and Sciences. 2013; 58(12): 3422–3428. doi:10.1007/s10620-013-2846-z.
  79. Feitoza A. B., Gostout C. J., Rajan E., Smoot R. L., Burgart L. J., Schleck C., Zinsmeister A.R. Understanding endoluminal gastroplications: A histopathologic analysis of intraluminal suture plications // Gastrointestinal Endoscopy. 2003; 57(7): 868–876. doi:10.1016/s0016-5107(03)70022-4.
  80. Cuenca R., Blanchard T., Czinn S., Nedrud J., Monath T. P., Lee C. K., Redline R. W. Therapeutic immunization against Helicobacter mustelae in naturally infected ferrets // Gastroenterology. 1996; 110(6): 1770–1775. doi:10.1053/gast.1996.v110.pm8964402 .
  81. Rogers, A. B. Gastric Helicobacter spp. in Animal Models: Pathogenesis and modulation by extragastric coinfections // Methods in Molecular Biology. 2012; 921:175-88. doi:10.1007/978-1-62703-005-2_21.
  82. Erkan M., Erhan E., Sağlam A., Arslan S. Compensatory mechanisms in rats with nasal obstructions // Tokai journal of experimental and clinical medicine. 1994; 19(1-2):67-71.
  83. DeCubellis J., Graham, J. Gastrointestinal Disease in Guinea Pigs and Rabbits // Veterinary Clinics of North America: Exotic Animal Practice. 2013; 16(2): 421–435. doi:10.1016/j.cvex.2013.01.002.
  84. Kirk J. M., James G. F. Biology and diseases of the ferret – Third edition / edited by James G. F., Robert P. – John Wiley & Sons. 2014. 835p.
  85. Fisher P.G, Carpenter J.W. Ferrets, rabbits, and rodents: clinical medicine and surgery. 3rd edition: Neurologic and musculoskeletal diseases // Edited by Quesenberry K.E., Carpenter J.W. – St Louis, Saunders Elsevier, 2012. 608 p.

You may be interested