Histopathological analysis of Salmonella chronic carriage in the mouse hepatopancreatobiliary system

PLoS ONE

Volumn 8, Issue 12, 2013, Pages

  Gonzalez Escobedo, Geoffrey ^a   La Perle, Krista M D ^a   Gunn, John S ^a  

^a OHIO STATE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BACTERIAL COLONIZATION; BACTERIAL LOAD; BACTERIUM CARRIER; BACTERIUM ISOLATION; BILIARY TRACT DISEASE; CHRONIC CHOLECYSTITIS; CHRONIC INFLAMMATION; COLONY FORMING UNIT; CONTROLLED STUDY; DISEASE CARRIER; DYSPLASIA; FEMALE; GALLBLADDER DISEASE; GALLSTONE; HEPATITIS; HEPATOBILIARY SYSTEM; HEPATOPANCREATOBILIARY SYSTEM; HISTIOCYTE; HISTOPATHOLOGY; HYPERPLASIA; IMMUNOHISTOCHEMISTRY; INFECTION; METAPLASIA; MOUSE; NONHUMAN; PANCREATITIS; TYPHOID FEVER;

ANIMALS; CHRONIC DISEASE; GALLBLADDER; GALLBLADDER NEOPLASMS; MICE; PANCREAS, EXOCRINE; PANCREATIC NEOPLASMS; PRECANCEROUS CONDITIONS; SALMONELLA INFECTIONS; SALMONELLA TYPHIMURIUM; TIME FACTORS;

EID: 84892620607     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0084058     Document Type: Article

References (81)

1. Crump JA, Luby SP, Mintz ED (2004) The global burden of typhoid fever. Bull World Health Organ 82: 346-353. PubMed: 15298225.
2. Jepson MA, Clark MA (2001) The role of M cells in Salmonella infection. Microbes Infect 3: 1183-1190. doi:10.1016/S1286-4579(01)01478-2. PubMed: 11755406.
3. Vazquez-Torres A, Jones-Carson J, Bäumler AJ, Falkow S, Valdivia R et al. (1999) Extraintestinal dissemination of Salmonella by CD18-expressing phagocytes. Nature 401: 804-808. doi:10.1038/44593. PubMed: 10548107.
4. Wain J, Diep TS, Ho VA, Walsh AM, Nguyen TT et al. (1998) Quantitation of bacteria in blood of typhoid fever patients and relationship between counts and clinical features, transmissibility, and antibiotic resistance. J Clin Microbiol 36: 1683-1687. PubMed: 9620400.
5. Vladoianu IR, Chang HR, Pechère JC (1990) Expression of host resistance to Salmonella Typhi and Salmonella Typhimurium: bacterial survival within macrophages of murine and human origin. Microb Pathog 8: 83-90. doi:10.1016/0882-4010(90)90072-X. PubMed: 2190062.
6. Crum NF (2003) Current trends in typhoid fever. Curr Gastroenterol Rep 5: 279-286. doi:10.1007/s11894-003-0064-0. PubMed: 12864957.
7. Cohen JI, Bartlett JA, Corey GR (1987) Extra-intestinal manifestations of Salmonella infections. Medicine (Baltimore) 66: 349-388. PubMed: 3306260.
8. Parry CM, Hien TT, Dougan G, White NJ, Farrar JJ (2002) Typhoid fever. N Engl J Med 347: 1770-1782. doi:10.1056/NEJMra020201. PubMed: 12456854.
9. Everest P, Wain J, Roberts M, Rook G, Dougan G (2001) The molecular mechanisms of severe typhoid fever. Trends Microbiol 9: 316-320. doi:10.1016/S0966-842X(01)02067-4. PubMed: 11435104.
10. Vogelsang TM, Boe J (1948) Temporary and chronic carriers of Salmonella Typhi and Salmonella Paratyphi BJ Hyg (Lond) 46: 252-261.
11. Vaishnavi C, Singh S, Kochhar R, Bhasin D, Singh G et al. (2005) Prevalence of Salmonella enterica serovar Typhi in bile and stool of patients with biliary diseases and those requiring biliary drainage for other purposes. Jpn J Infect Dis 58: 363-365. PubMed: 16377868.
12. Shetty PB, Broome DR (1998) Sonographic analysis of gallbladder findings in Salmonella enteric fever. J Ultrasound Med 17: 231-237. PubMed: 9544606.
13. Mateen MA, Saleem S, Rao PC, Reddy PS, Reddy DN (2006) Ultrasound in the diagnosis of typhoid fever. Indian J Pediatr 73: 681-685. doi:10.1007/ BF02898444. PubMed: 16936362.
14. Ramachandran S, Godfrey JJ, Perera MV (1974) Typhoid hepatitis. JAMA 230: 236-240. doi:10.1001/jama.230.2.236. PubMed: 4213522.
15. Pramoolsinsap C, Viranuvatti V (1998) Salmonella hepatitis. J Gastroenterol Hepatol 13: 745-750. doi:10.1111/j.1440-1746.1998.tb00726.x. PubMed: 9715430.
16. Khosla SN (1990) Typhoid hepatitis. Postgrad Med J 66: 923-925. doi:10.1136/pgmj.66.781.923. PubMed: 2267203.
17. Rovito V, Bonanno CA (1982) Salmonella hepatic abscess: an unusual complication of the Salmonella carrier state? Am J Gastroenterol 77: 338-339. PubMed: 7081193.
18. Levine MM, Black RE, Lanata C (1982) Precise estimation of the numbers of chronic carriers of Salmonella Typhi in Santiago, Chile, an endemic area. J Infect Dis 146: 724-726. doi:10.1093/infdis/146.6.724. PubMed: 7142746.
19. Merselis JG Jr., Kaye D, Connolly CS, Hook EW (1964) Quantitative Bacteriology of the Typhoid Carrier State. Am J Trop Med Hyg 13: 425-429. PubMed: 14159980.
20. Bhan MK, Bahl R, Bhatnagar S (2005) Typhoid and paratyphoid fever. Lancet 366: 749-762. doi:10.1016/S0140-6736(05)67181-4. PubMed: 16125594.
21. Sinnott CR, Teall AJ (1987) Persistent gallbladder carriage of Salmonella Typhi. Lancet 1: 976. PubMed: 2882361.
22. Shpargel JS, Berardi RS, Lenz D (1985) Salmonella Typhi carrier state 52 years after illness with typhoid fever: a case study. Am J Infect Control 13: 122-123. doi:10.1016/S0196-6553(85)80013-4. PubMed: 3849271.
23. Gosbell I, Jones PD, Matthews A, Yeo B (1995) Surgical presentation of hepatobiliary disease due to Salmonella Typhi. Aust N Z J Surg 65: 898-899. doi:10.1111/j.1445-2197.1995.tb00588.x. PubMed: 8611118.
24. Schiøler H, Christiansen ED, Høybye G, Rasmussen SN, Greibe J (1983) Biliary calculi in chronic Salmonella carriers and healthy controls: a controlled study. Scand J Infect Dis 15: 17-19. PubMed: 6405479.
25. Karaki K, Matsubara Y (1984) Surgical treatment of chronic biliary typhoid and paratyphoid carriers. Nippon Shokakibyo Gakkai Zasshi 81: 2978-2985. PubMed: 6442374.
26. Lai CW, Chan RC, Cheng AF, Sung JY, Leung JW (1992) Common bile duct stones: a cause of chronic salmonellosis. Am J Gastroenterol 87: 1198-1199. PubMed: 1519582.
27. Vaishnavi C, Kochhar R, Singh G, Kumar S, Singh S et al. (2005) Epidemiology of typhoid carriers among blood donors and patients with biliary, gastrointestinal and other related diseases. Microbiol Immunol 49: 107-112. doi:10.1111/j.1348-0421.2005.tb03709.x. PubMed: 15722595.
28. Scott AJ (1971) Bacteria and disease of the biliary tract. Gut 12: 487-492. doi:10.1136/gut.12.6.487. PubMed: 4933136.
29. Crawford RW, Rosales-Reyes R, Mde Ramirez-Aguilar L, Chapa-Azuela O, Alpuche-Aranda C et al. (2010) Gallstones play a significant role in Salmonella spp. gallbladder colonization and carriage. Proc Natl Acad Sci U S A 107: 4353-4358. doi:10.1073/pnas.1000862107. PubMed: 20176950. Available online at: doi:10.1073/pnas.1000862107 Available online at: PubMed: 20176950
30. Cappelli G, Tetta C, Canaud B (2005) Is biofilm a cause of silent chronic inflammation in haemodialysis patients? A fascinating working hypothesis. Nephrol Dial Transplant 20: 266-270. doi:10.1093/ndt/20.suppl-5.v266. PubMed: 15647310.
31. Miller G, Jarnagin WR (2008) Gallbladder carcinoma. Eur J Surg Oncol 34: 306-312. doi:10.1016/j.ejso.2007.07.206. PubMed: 17964753.
32. Lazcano-Ponce EC, Miquel JF, Muñoz N, Herrero R, Ferrecio C et al. (2001) Epidemiology and molecular pathology of gallbladder cancer. CA Cancer J Clin 51: 349-364. doi:10.3322/canjclin.51.6.349. PubMed: 11760569.
33. Randi G, Franceschi S, La Vecchia C (2006) Gallbladder cancer worldwide: geographical distribution and risk factors. Int J Cancer 118: 1591-1602. doi:10.1002/ijc.21683. PubMed: 16397865.
34. Dutta U, Garg PK, Kumar R, Tandon RK (2000) Typhoid carriers among patients with gallstones are at increased risk for carcinoma of the gallbladder. Am J Gastroenterol 95: 784-787. doi:10.1111/j.1572-0241.2000.01860.x. PubMed: 10710075.
35. Shukla VK, Singh H, Pandey M, Upadhyay SK, Nath G (2000) Carcinoma of the gallbladder - is it a sequel of typhoid? Dig Dis Sci 45: 900-903. doi:10.1023/A:1005564822630. PubMed: 10795752.
36. Caygill CP, Hill MJ, Braddick M, Sharp JC (1994) Cancer mortality in chronic typhoid and paratyphoid carriers. Lancet 343: 83-84. doi:10.1016/S0140-6736(94)90816-8. PubMed: 7903779.
37. Nath G, Singh H, Shukla VK (1997) Chronic typhoid carriage and carcinoma of the gallbladder. Eur J Cancer Prev 6: 557-559. doi:10.1097/00008469- 199712000-00011. PubMed: 9496458.
38. Nath G, Singh YK, Kumar K, Gulati AK, Shukla VK et al. (2008) Association of carcinoma of the gallbladder with typhoid carriage in a typhoid endemic area using nested PCR. J Infect Dev Ctries 2: 302-307. PubMed: 19741293.
39. Chang HR, Dulloo AG, Vladoianu IR, Piguet PF, Arsenijevic D et al. (1992) Fish oil decreases natural resistance of mice to infection with Salmonella Typhimurium. Metabolism 41: 1-2. doi:10.1016/0026-0495(92)90181-9. PubMed: 1538638.
40. Csendes A, Fernandez M, Uribe P (1975) Bacteriology of the gallbladder bile in normal subjects. Am J Surg 129: 629-631. doi:10.1016/0002-9610(75)90334- 7. PubMed: 805546.
41. el-Zayadi A, Ghoneim M, Kabil SM, el Tawil A, Sherif A et al. (1991) Bile duct carcinoma in Egypt: possible etiological factors. Hepatogastroenterology 38: 337-340. PubMed: 1657750.
42. Welton JC, Marr JS, Friedman SM (1979) Association between hepatobiliary cancer and typhoid carrier state. Lancet 1: 791-794. PubMed: 86039.
43. Kumar S (2006) Infection as a risk factor for gallbladder cancer. J Surg Oncol 93: 633-639. doi:10.1002/jso.20530. PubMed: 16724347.
44. Tazuma S, Kajiyama G (2001) Carcinogenesis of malignant lesions of the gall bladder. The impact of chronic inflammation and gallstones. Langenbecks Arch Surg 386: 224-229. doi:10.1007/s004230100220. PubMed: 11382326.
45. Sośnik K, Sośnik H (2005) Some aspects of gallbladder carcinogenesis. Wiad Lek 58: 678-681. PubMed: 16594482.
46. Santos RL, Zhang S, Tsolis RM, Kingsley RA, Adams LG et al. (2001) Animal models of Salmonella infections: enteritis versus typhoid fever. Microbes Infect 3: 1335-1344. doi:10.1016/S1286-4579(01)01495-2. PubMed: 11755423.
47. Monack DM, Bouley DM, Falkow S (2004) Salmonella Typhimurium persists within macrophages in the mesenteric lymph nodes of chronically infected Nramp1+/+ mice and can be reactivated by IFNγ neutralization. J Exp Med 199: 231-241.
48. Forbes JR, Gros P (2001) Divalent-metal transport by NRAMP proteins at the interface of host-pathogen interactions. Trends Microbiol 9: 397-403. doi:10.1016/S0966-842X(01)02098-4. PubMed: 11514223.
49. Fritsche G, Nairz M, Libby SJ, Fang FC, Weiss G (2012) Slc11a1 (Nramp1) impairs growth of Salmonella enterica serovar Typhimurium in macrophages via stimulation of lipocalin-2 expression. J Leukoc Biol 92: 353-359. doi:10.1189/jlb.1111554. PubMed: 22706314.
50. Fadl AA, Sha J, Klimpel GR, Olano JP, Niesel DW et al. (2005) Murein lipoprotein is a critical outer membrane component involved in Salmonella enterica serovar Typhimurium systemic infection. Infect Immun 73: 1081-1096. doi:10.1128/IAI.73.2.1081-1096.2005. PubMed: 15664952. Available online at: doi:10.1128/IAI.73.2.1081-1096.2005 Available online at: PubMed: 15664952
51. Gonzalez-Escobedo G, Gunn JS (2013) The Gallbladder Epithelium as a Niche for Chronic Salmonella Carriage. Infect Immun 8: 2920-2930.
52. Haschek W, Wallig M, Rousseaux C (2010) Fundamentals of Toxicologic Pathology. London, UK: Elsevier.
53. Monga S (2011) Molecular Pathology of Liver Diseases. New York, USA: Springer.
54. Pilgrim CH, Groeschl RT, Christians KK, Gamblin TC (2013) Modern perspectives on factors predisposing to the development of gallbladder cancer. HPB Oxford.
55. Rustagi T, Dasanu CA (2012) Risk factors for gallbladder cancer and cholangiocarcinoma: similarities, differences and updates. J Gastrointest Cancer 43: 137-147. doi:10.1007/s12029-011-9284-y. PubMed: 21597894.
56. Menendez A, Arena ET, Guttman JA, Thorson L, Vallance BA et al. (2009) Salmonella infection of gallbladder epithelial cells drives local inflammation and injury in a model of acute typhoid fever. J Infect Dis 200: 1703-1713. doi:10.1086/646608. PubMed: 19852670.
57. Knodler LA, Vallance BA, Celli J, Winfree S, Hansen B et al. (2010) Dissemination of invasive Salmonella via bacterial-induced extrusion of mucosal epithelia. Proc Natl Acad Sci U S A 107: 17733-17738. doi:10.1073/pnas. 1006098107. PubMed: 20876119.
58. Richter-Dahlfors A, Buchan AM, Finlay BB (1997) Murine salmonellosis studied by confocal microscopy: Salmonella Typhimurium resides intracellularly inside macrophages and exerts a cytotoxic effect on phagocytes in vivo. J Exp Med 186: 569-580. doi:10.1084/jem.186.4.569. PubMed: 9254655.
59. Nnalue NA, Shnyra A, Hultenby K, Lindberg AA (1992) Salmonella Choleraesuis and Salmonella Typhimurium associated with liver cells after intravenous inoculation of rats are localized mainly in Kupffer cells and multiply intracellularly. Infect Immun 60: 2758-2768. PubMed: 1612743.
60. Axelrod L, Munster AM, O'Brien TF (1971) Typhoid cholecystitis and gallbladder carcinoma after interval of 67 years. JAMA 217: 83. doi:10.1001/jama.217.1.83b. PubMed: 5108716.
61. Roa I, Ibacache G, Carvallo J, Melo A, Araya J et al. (1999) Microbiological study of gallbladder bile in a high risk zone for gallbladder cancer. Rev Med Chil 127: 1049-1055. PubMed: 10752267.
62. Lavoie B, Nausch B, Zane EA, Leonard MR, Balemba OB et al. (2012) Disruption of gallbladder smooth muscle function is an early feature in the development of cholesterol gallstone disease. Neurogastroenterol Motil 24: e313-e324. doi:10.1111/j.1365-2982.2012.01935.x. PubMed: 22621672.
63. Ichikawa H, Imano M, Takeyama Y, Shiozaki H, Ohyanagi H (2009) Involvement of osteopontin as a core protein in cholesterol gallstone formation. J Hepatobiliary Pancreat Surg 16: 197-203. doi:10.1007/s00534-009-0043-4. PubMed: 19214371.
64. Rege RV, Prystowsky JB (1998) Inflammation and a thickened mucus layer in mice with cholesterol gallstones. J Surg Res 74: 81-85. doi:10.1006/jsre.1997. 5213. PubMed: 9536979.
65. Khosla SN (2008) Typhoid Fever: Its Cause, Transmission And Prevention. New Delhi, India: Atlantic Publishers & Distributors. 245 p
66. Mert A, Tabak F, Ozaras R, Ozturk R, Aki H et al. (2004) Typhoid fever as a rare cause of hepatic, splenic, and bone marrow granulomas. Intern Med 43: 436-439. doi:10.2169/internalmedicine.43.436. PubMed: 15206561.
67. Hermans P, Gerard M, De Wit S, Van Laethem Y (1990) Pancreatitis and typhoid fever. Am J Med 89: 546-547. doi:10.1016/0002-9343(90)90401-X. PubMed: 2220896.
68. Kadappu KK, Rao PV, Srinivas N, Shastry BA (2002) Pancreatitis in enteric fever. Indian J Gastroenterol 21: 32-33. PubMed: 11871836.
69. Khan FY, Al-Ani A, Ali HA (2009) Typhoid rhabdomyolysis with acute renal failure and acute pancreatitis: a case report and review of the literature. Int J Infect Dis 13: e282-e285. doi:10.1016/j.ijid.2008.11.009. PubMed: 19147385.
70. Parenti DM, Steinberg W, Kang P (1996) Infectious causes of acute pancreatitis. Pancreas 13: 356-371. doi:10.1097/00006676-199611000-00005. PubMed: 8899796.
71. Hornick RB, Greisman SE, Woodward TE, DuPont HL, Dawkins AT et al. (1970) Typhoid fever: pathogenesis and immunologic control. N Engl J Med 283: 686-691. doi:10.1056/NEJM197009242831306. PubMed: 4916913.
72. Wistuba II, Sugio K, Hung J, Kishimoto Y, Virmani AK et al. (1995) Allele-specific mutations involved in the pathogenesis of endemic gallbladder carcinoma in Chile. Cancer Res 55: 2511-2515. PubMed: 7780959.
73. Wee A, Teh M, Raju GC (1994) Clinical importance of p53 protein in gall bladder carcinoma and its precursor lesions. J Clin Pathol 47: 453-456. doi:10.1136/jcp.47.5.453. PubMed: 8027399.
74. Rai R, Tewari M, Kumar M, Singh AK, Shukla HS (2011) p53: its alteration and gallbladder cancer. Eur J Cancer Prev 20: 77-85. doi:10.1111/j.1365-2354. 2009.01141.x. PubMed: 21131824.
75. Legan M (2010) Cyclooxygenase-2, p53 and glucose transporter-1 as predictors of malignancy in the development of gallbladder carcinomas. Bosn J Basic Med Sci 10: 192-196. PubMed: 20846124.
76. Chang HJ, Suh JI, Kwon SY (1999) Gallstone formation and gallbladder mucosal changes in mice fed a lithogenic diet. J Korean Med Sci 14: 286-292. PubMed: 10402171.
77. Mathur SK, Duhan A, Singh S, Aggarwal M, Aggarwal G et al. (2012) Correlation of gallstone characteristics with mucosal changes in gall bladder. Trop Gastroenterol 33: 39-44. doi:10.7869/tg.2012.6. PubMed: 22803294.
78. phox-deficient mice. J Biol Chem 277: 5468-5475. doi:10.1074/jbc.M110635200. PubMed: 11733538.
79. Ward JM, Yoon M, Anver MR, Haines DC, Kudo G et al. (2001) Hyalinosis and Ym1/Ym2 gene expression in the stomach and respiratory tract of 129S4/SvJae and wild-type and CYP1A2-null B6, 129 mice. Am J Pathol 158: 323-332. doi:10.1016/S0002-9440(10)63972-7. PubMed: 11141507.
80. Goldin RD, Roa JC (2009) Gallbladder cancer: a morphological and molecular update. Histopathology 55: 218-229. doi:10.1111/j.1365-2559.2008. 03192.x. PubMed: 19490172.
81. Cao W, Adley BP, Liao J, Lin X, Talamonti M et al. (2010) Mucinous nonneoplastic cyst of the pancreas: apomucin phenotype distinguishes this entity from intraductal papillary mucinous neoplasm. Hum Pathol 41: 513-521. doi:10.1016/j.humpath.2009.05.017. PubMed: 19954814.