Diagnosis for cases with <i>Tropheryma whipplei</i> detected from respiratory samples: West China suggestions_West China Medical Journal

Authors：

HU Ya ¹ , TANG Guangmin ¹ , BI Hongxia ¹ , HE Da ¹ , ZHOU Yongzhao ^2,3 , XIAO Yuling ⁴ ,  ZONG Zhiyong ¹

1. Center of Infectious Diseases, West China Hospital, Sichuan University, Chengdu, Sichuan 610041, P. R. China;
2. Institute of Respiratory Health and Multimorbidity, West China Hospital, Sichuan University, Chengdu, Sichuan 610041, P. R. China;
3. Integrated Care Management Center, West China Hospital, Sichuan University, Chengdu, Sichuan 610041, P. R. China;
4. Department of Laboratory Medicine, West China Hospital, Sichuan University, Chengdu, Sichuan 610041, P. R. China;

Corresponding author：

ZONG Zhiyong, Email: zongzhiy@scu.edu.cn

Keywords：

Tropheryma whipplei; pulmonary infection; grading diagnostic schemes

DOI：

10.7507/1002-0179.202402120

Video：

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Whipple’s disease is a multisystemic disease caused by Tropheryma (T.) whipplei that primarily affects the gastrointestinal tract. In literature, T. whipplei can also cause pulmonary infections. The detection of T. whipplei depends on nucleic acid-based test. With the application of next-generation sequencing (NGS), cases with T. whipplei detected from respiratory tract samples by NGS are increasingly found but there is lack of recognized diagnostic criteria for these cases. Within the context, we propose a grading diagnostic scheme for the situation that T. whipplei is detected from respiratory tract samples, based on clinical experience and diagnostic thinking, and referring to the international classifications of invasive fungal infections. The scheme comprises five levels: confirmed, probable, possible, impossible, and excluded. There were 26 such cases from West China Hospital of Sichuan University and we used our diagnostic scheme to define probable in 6 cases, possible in 9 cases, impossible in 8 cases, and excluded in 3 cases. Based on this, we also propose specific suggestions for sample collection and testing, patient management, and further research directions. These recommendations are preliminary based on the existing cases from West China Hospital of Sichuan University and therefore needs to be verified, modified, optimized, and even reconstructed when more clinical evidence and further clinical studies become available.

Citation： HU Ya, TANG Guangmin, BI Hongxia, HE Da, ZHOU Yongzhao, XIAO Yuling, ZONG Zhiyong. Diagnosis for cases with Tropheryma whipplei detected from respiratory samples: West China suggestions. West China Medical Journal, 2024, 39(3): 338-343. doi: 10.7507/1002-0179.202402120 Copy

1.	Whipple GH. A hitherto undescribed disease characterized anatomically by deposits of fat and fatty acids in the intestinal and mesenteric lymphatic tissues. Bull Johns Hopkins Hosp, 1907, 18: 382-393.
2.	Fenollar F, Puéchal X, Raoult D. Whipple’s disease. N Engl J Med, 2007, 356(1): 55-66.
3.	Boumaza A, Ben Azzouz E, Arrindell J, et al. Whipple’s disease and Tropheryma whipplei infections: from bench to bedside. Lancet Infect Dis, 2022, 22(10): e280-e291.
4.	Dolmans RA, Boel CH, Lacle MM, et al. Clinical manifestations, treatment, and diagnosis of Tropheryma whipplei Infections. Clin Microbiol Rev, 2017, 30(2): 529-555.
5.	La Scola B, Fenollar F, Fournier PE, et al. Description of Tropheryma whipplei gen. nov. , sp. nov. , the Whipple’s disease bacillus. Int J Syst Evol Microbiol, 2001, 51(Pt4): 1471-1479.
6.	Wilson KH, Blitchington R, Frothingham R, et al. Phylogeny of the Whipple’s-disease-associated bacterium. Lancet, 1991, 338(8765): 474-475.
7.	Relman DA, Schmidt TM, MacDermott RP, et al. Identification of the uncultured bacillus of Whipple’s disease. N Engl J Med, 1992, 327(5): 293-301.
8.	Roth RI, Owen RL, Keren DF, et al. Intestinal infection with Mycobacterium avium in acquired immune deficiency syndrome (AIDS). Histological and clinical comparison with Whipple’s disease. Dig Dis Sci, 1985, 30(5): 497-504.
9.	Maiwald M, Schuhmacher F, Ditton HJ, et al. Environmental occurrence of the Whipple’s disease bacterium ( Tropheryma whippelii). Appl Environ Microbiol, 1998, 64(2): 760-762.
10.	Schöniger-Hekele M, Petermann D, Weber B, et al. Tropheryma whipplei in the environment: survey of sewage plant influxes and sewage plant workers. Appl Environ Microbiol, 2007, 73(6): 2033-2035.
11.	Street S, Donoghue HD, Neild GH. Tropheryma whippelii DNA in saliva of healthy people. Lancet, 1999, 354(9185): 1178-1179.
12.	Dutly F, Hinrikson HP, Seidel T, et al. Tropheryma whippelii DNA in saliva of patients without Whipple’s disease. Infection, 2000, 28(4): 219-222.
13.	Maibach RC, Dutly F, Altwegg M. Detection of Tropheryma whipplei DNA in feces by PCR using a target capture method. J Clin Microbiol, 2002, 40(7): 2466-2471.
14.	Fenollar F, Laouira S, Lepidi H, et al. Value of Tropheryma whipplei quantitative polymerase chain reaction assay for the diagnosis of Whipple disease: usefulness of saliva and stool specimens for first-line screening. Clin Infect Dis, 2008, 47(5): 659-667.
15.	Fenollar F, Trape JF, Bassene H, et al. Tropheryma whipplei in fecal samples from children, senegal. Emerg Infect Dis, 2009, 15(6): 922-924.
16.	Amsler L, Bauernfeind P, Nigg C, et al. Prevalence of Tropheryma whipplei DNA in patients with various gastrointestinal diseases and in healthy controls. Infection, 2003, 31(2): 81-85.
17.	Fenollar F, Trani M, Davoust B, et al. Prevalence of asymptomatic Tropheryma whipplei carriage among humans and nonhuman primates. J Infect Dis, 2008, 197(6): 880-887.
18.	Ehrbar HU, Bauerfeind P, Dutly F, et al. PCR-positive tests for Tropheryma whippelii in patients without Whipple’s disease. Lancet, 1999, 353(9171): 2214.
19.	Fleming JL, Wiesner RH, Shorter RG. Whipple’s disease: clinical, biochemical, and histopathologic features and assessment of treatment in 29 patients. Mayo Clin Proc, 1988, 63(6): 539-551.
20.	Marth T, Raoult D. Whipple’s disease. Lancet, 2003, 361(9353): 239-246.
21.	Puéchal X. Whipple's disease. Ann Rheum Dis, 2013, 72(6): 797-803.
22.	Elchert JA, Mansoor E, Abou-Saleh M, et al. Epidemiology of Whipple’s disease in the USA Between 2012 and 2017: a population-based national study. Dig Dis Sci, 2019, 64(5): 1305-1311.
23.	Biagi F, Balduzzi D, Delvino P, et al. Prevalence of Whipple’s disease in north-western Italy. Eur J Clin Microbiol Infect Dis, 2015, 34(7): 1347-1348.
24.	Durand DV, Lecomte C, Cathébras P, et al. Whipple disease. Clinical review of 52 cases. The SNFMI research group on Whipple disease. Société nationale française de médecine interne. Medicine (Baltimore), 1997, 76(3): 170-184.
25.	Bally JF, Méneret A, Roze E, et al. Systematic review of movement disorders and oculomotor abnormalities in Whipple’s disease. Mov Disord, 2018, 33(11): 1700-1711.
26.	Matthews BR, Jones LK, Saad DA, et al. Cerebellar ataxia and central nervous system whipple disease. Arch Neurol, 2005, 62(4): 618-620.
27.	Panegyres PK, Edis R, Beaman M, et al. Primary Whipple’s disease of the brain: characterization of the clinical syndrome and molecular diagnosis. QJM, 2006, 99(9): 609-623.
28.	Louis ED, Lynch T, Kaufmann P, et al. Diagnostic guidelines in central nervous system Whipple’s disease. Ann Neurol, 1996, 40(4): 561-568.
29.	Gubler JG, Kuster M, Dutly F, et al. Whipple endocarditis without overt gastrointestinal disease: report of four cases. Ann Intern Med, 1999, 131(2): 112-116.
30.	Fenollar F, Lepidi H, Raoult D. Whipple’s endocarditis: review of the literature and comparisons with Q fever, bartonella infection, and blood culture-positive endocarditis. Clin Infect Dis, 2001, 33(8): 1309-1316.
31.	Lepidi H, Fenollar F, Dumler JS, et al. Cardiac valves in patients with Whipple endocarditis: microbiological, molecular, quantitative histologic, and immunohistochemical studies of 5 patients. J Infect Dis, 2004, 190(5): 935-945.
32.	Geissdörfer W, Moos V, Moter A, et al. High frequency of Tropheryma whipplei in culture-negative endocarditis. J Clin Microbiol, 2012, 50(2): 216-222.
33.	Marín M, Muñoz P, Sánchez M, et al. Tropheryma whipplei infective endocarditis as the only manifestation of Whipple’s disease. J Clin Microbiol, 2007, 45(6): 2078-2081.
34.	Urbanski G, Rivereau P, Artru L, et al. Whipple disease revealed by lung involvement: a case report and literature review. Chest, 2012, 141(6): 1595-1598.
35.	Damaraju D, Steiner T, Wade J, et al. Clinical problem-solving. A surprising cause of chronic cough. N Engl J Med, 2015, 373(6): 561-566.
36.	Lagier JC, Papazian L, Fenollar F, et al. Tropheryma whipplei DNA in bronchoalveolar lavage samples: a case control study. Clin Microbiol Infect, 2016, 22(10): 875-879.
37.	Fang Z, Liu Q, Tang W, et al. Experience in the diagnosis and treatment of pneumonia caused by infection with Tropheryma whipplei: A case series. Heliyon, 2023, 9(6): e17132.
38.	Lu Z, Zhang A, Guo J, et al. An unusual case of severe pneumonia caused by Tropheryma whipplei combined with Legionella pneumophila. World J Emerg Med, 2023, 14(6): 492-494.
39.	Yan J, Zhang B, Zhang Z, et al. Case report: Tropheryma whipplei hide in an AIDS patient With Pneumocysti s pneumonia. Front Public Health, 2021, 9: 663093.
40.	Raoult D, La Scola B, Lecocq P, et al. Culture and immunological detection of Tropheryma whippelii from the duodenum of a patient with Whipple disease. JAMA, 2001, 285(8): 1039-1043.
41.	Maiwald M, von Herbay A, Fredricks DN, et al. Cultivation of Tropheryma whipplei from cerebrospinal fluid. J Infect Dis, 2003, 188(6): 801-808.
42.	Raoult D, Fenollar F, Birg ML. Culture of T. Whipplei from the stool of a patient with Whipple’s disease. N Engl J Med, 2006, 355(14): 1503-1505.
43.	Renesto P, Crapoulet N, Ogata H, et al. Genome-based design of a cell-free culture medium for Tropheryma whipplei. Lancet, 2003, 362(9382): 447-449.
44.	Fenollar F, Raoult D. Molecular techniques in Whipple’s disease. Expert Rev Mol Diagn, 2001, 1(3): 299-309.
45.	Moter A, Janneck M, Wolters M, et al. Potential role for urine polymerase chain reaction in the diagnosis of Whipple’s disease. Clin Infect Dis, 2019, 68(7): 1089-1097.
46.	Donnelly JP, Chen SC, Kauffman CA, et al. Revision and update of the consensus definitions of invasive fungal disease from the european organization for research and treatment of cancer and the mycoses study group education and research consortium. Clin Infect Dis, 2020, 71(6): 1367-1376.
47.	Pappas PG, Chen SC, Donnelly JP. The evidence supporting the revised EORTC/MSGERC definitions for invasive fungal infections. Clin Infect Dis, 2021, 72(Suppl 2): s77-s78.
48.	Feurle GE, Junga NS, Marth T. Efficacy of ceftriaxone or meropenem as initial therapies in Whipple’s disease. Gastroenterology, 2010, 138(2): 478-486.
49.	Lévy M, Poyart C, Lamarque D, et al. Whipple’s disease: acquired resistance to trimethoprim-sulfamethoxazole. Am J Gastroenterol, 2000, 95(9): 2390-2391.
50.	Keinath RD, Merrell DE, Vlietstra R, et al. Antibiotic treatment and relapse in Whipple’s disease. Long-term follow-up of 88 patients. Gastroenterology, 1985, 88(6): 1867-1873.
51.	Lagier JC, Fenollar F, Lepidi H, et al. Treatment of classic Whipple’s disease: from in vitro results to clinical outcome. J Antimicrob Chemother, 2014, 69(1): 219-227.
52.	Feurle GE, Marth T. An evaluation of antimicrobial treatment for Whipple’s disease. Tetracycline versus trimethoprim-sulfamethoxazole. Dig Dis Sci, 1994, 39(8): 1642-1648.
53.	Boulos A, Rolain JM, Raoult D. Antibiotic susceptibility of Tropheryma whipplei in MRC5 cells. Antimicrob Agents Chemother, 2004, 48(3): 747-752.
54.	Boulos A, Rolain JM, Mallet MN, et al. Molecular evaluation of antibiotic susceptibility of Tropheryma whipplei in axenic medium. J Antimicrob Chemother, 2005, 55(2): 178-181.
55.	Cannon WR. Whipple’s disease, genomics, and drug therapy. Lancet, 2003, 361(9372): 1916.
56.	刘运喜, 邢玉斌, 巩玉秀. 软式内镜清洗消毒技术规范WS507-2016. 中国感染控制杂志, 2017, 16(6): 587-592.

1. Whipple GH. A hitherto undescribed disease characterized anatomically by deposits of fat and fatty acids in the intestinal and mesenteric lymphatic tissues. Bull Johns Hopkins Hosp, 1907, 18: 382-393.
2. Fenollar F, Puéchal X, Raoult D. Whipple’s disease. N Engl J Med, 2007, 356(1): 55-66.
3. Boumaza A, Ben Azzouz E, Arrindell J, et al. Whipple’s disease and Tropheryma whipplei infections: from bench to bedside. Lancet Infect Dis, 2022, 22(10): e280-e291.
4. Dolmans RA, Boel CH, Lacle MM, et al. Clinical manifestations, treatment, and diagnosis of Tropheryma whipplei Infections. Clin Microbiol Rev, 2017, 30(2): 529-555.
5. La Scola B, Fenollar F, Fournier PE, et al. Description of Tropheryma whipplei gen. nov. , sp. nov. , the Whipple’s disease bacillus. Int J Syst Evol Microbiol, 2001, 51(Pt4): 1471-1479.
6. Wilson KH, Blitchington R, Frothingham R, et al. Phylogeny of the Whipple’s-disease-associated bacterium. Lancet, 1991, 338(8765): 474-475.
7. Relman DA, Schmidt TM, MacDermott RP, et al. Identification of the uncultured bacillus of Whipple’s disease. N Engl J Med, 1992, 327(5): 293-301.
8. Roth RI, Owen RL, Keren DF, et al. Intestinal infection with Mycobacterium avium in acquired immune deficiency syndrome (AIDS). Histological and clinical comparison with Whipple’s disease. Dig Dis Sci, 1985, 30(5): 497-504.
9. Maiwald M, Schuhmacher F, Ditton HJ, et al. Environmental occurrence of the Whipple’s disease bacterium ( Tropheryma whippelii). Appl Environ Microbiol, 1998, 64(2): 760-762.
10. Schöniger-Hekele M, Petermann D, Weber B, et al. Tropheryma whipplei in the environment: survey of sewage plant influxes and sewage plant workers. Appl Environ Microbiol, 2007, 73(6): 2033-2035.
11. Street S, Donoghue HD, Neild GH. Tropheryma whippelii DNA in saliva of healthy people. Lancet, 1999, 354(9185): 1178-1179.
12. Dutly F, Hinrikson HP, Seidel T, et al. Tropheryma whippelii DNA in saliva of patients without Whipple’s disease. Infection, 2000, 28(4): 219-222.
13. Maibach RC, Dutly F, Altwegg M. Detection of Tropheryma whipplei DNA in feces by PCR using a target capture method. J Clin Microbiol, 2002, 40(7): 2466-2471.
14. Fenollar F, Laouira S, Lepidi H, et al. Value of Tropheryma whipplei quantitative polymerase chain reaction assay for the diagnosis of Whipple disease: usefulness of saliva and stool specimens for first-line screening. Clin Infect Dis, 2008, 47(5): 659-667.
15. Fenollar F, Trape JF, Bassene H, et al. Tropheryma whipplei in fecal samples from children, senegal. Emerg Infect Dis, 2009, 15(6): 922-924.
16. Amsler L, Bauernfeind P, Nigg C, et al. Prevalence of Tropheryma whipplei DNA in patients with various gastrointestinal diseases and in healthy controls. Infection, 2003, 31(2): 81-85.
17. Fenollar F, Trani M, Davoust B, et al. Prevalence of asymptomatic Tropheryma whipplei carriage among humans and nonhuman primates. J Infect Dis, 2008, 197(6): 880-887.
18. Ehrbar HU, Bauerfeind P, Dutly F, et al. PCR-positive tests for Tropheryma whippelii in patients without Whipple’s disease. Lancet, 1999, 353(9171): 2214.
19. Fleming JL, Wiesner RH, Shorter RG. Whipple’s disease: clinical, biochemical, and histopathologic features and assessment of treatment in 29 patients. Mayo Clin Proc, 1988, 63(6): 539-551.
20. Marth T, Raoult D. Whipple’s disease. Lancet, 2003, 361(9353): 239-246.
21. Puéchal X. Whipple's disease. Ann Rheum Dis, 2013, 72(6): 797-803.
22. Elchert JA, Mansoor E, Abou-Saleh M, et al. Epidemiology of Whipple’s disease in the USA Between 2012 and 2017: a population-based national study. Dig Dis Sci, 2019, 64(5): 1305-1311.
23. Biagi F, Balduzzi D, Delvino P, et al. Prevalence of Whipple’s disease in north-western Italy. Eur J Clin Microbiol Infect Dis, 2015, 34(7): 1347-1348.
24. Durand DV, Lecomte C, Cathébras P, et al. Whipple disease. Clinical review of 52 cases. The SNFMI research group on Whipple disease. Société nationale française de médecine interne. Medicine (Baltimore), 1997, 76(3): 170-184.
25. Bally JF, Méneret A, Roze E, et al. Systematic review of movement disorders and oculomotor abnormalities in Whipple’s disease. Mov Disord, 2018, 33(11): 1700-1711.
26. Matthews BR, Jones LK, Saad DA, et al. Cerebellar ataxia and central nervous system whipple disease. Arch Neurol, 2005, 62(4): 618-620.
27. Panegyres PK, Edis R, Beaman M, et al. Primary Whipple’s disease of the brain: characterization of the clinical syndrome and molecular diagnosis. QJM, 2006, 99(9): 609-623.
28. Louis ED, Lynch T, Kaufmann P, et al. Diagnostic guidelines in central nervous system Whipple’s disease. Ann Neurol, 1996, 40(4): 561-568.
29. Gubler JG, Kuster M, Dutly F, et al. Whipple endocarditis without overt gastrointestinal disease: report of four cases. Ann Intern Med, 1999, 131(2): 112-116.
30. Fenollar F, Lepidi H, Raoult D. Whipple’s endocarditis: review of the literature and comparisons with Q fever, bartonella infection, and blood culture-positive endocarditis. Clin Infect Dis, 2001, 33(8): 1309-1316.
31. Lepidi H, Fenollar F, Dumler JS, et al. Cardiac valves in patients with Whipple endocarditis: microbiological, molecular, quantitative histologic, and immunohistochemical studies of 5 patients. J Infect Dis, 2004, 190(5): 935-945.
32. Geissdörfer W, Moos V, Moter A, et al. High frequency of Tropheryma whipplei in culture-negative endocarditis. J Clin Microbiol, 2012, 50(2): 216-222.
33. Marín M, Muñoz P, Sánchez M, et al. Tropheryma whipplei infective endocarditis as the only manifestation of Whipple’s disease. J Clin Microbiol, 2007, 45(6): 2078-2081.
34. Urbanski G, Rivereau P, Artru L, et al. Whipple disease revealed by lung involvement: a case report and literature review. Chest, 2012, 141(6): 1595-1598.
35. Damaraju D, Steiner T, Wade J, et al. Clinical problem-solving. A surprising cause of chronic cough. N Engl J Med, 2015, 373(6): 561-566.
36. Lagier JC, Papazian L, Fenollar F, et al. Tropheryma whipplei DNA in bronchoalveolar lavage samples: a case control study. Clin Microbiol Infect, 2016, 22(10): 875-879.
37. Fang Z, Liu Q, Tang W, et al. Experience in the diagnosis and treatment of pneumonia caused by infection with Tropheryma whipplei: A case series. Heliyon, 2023, 9(6): e17132.
38. Lu Z, Zhang A, Guo J, et al. An unusual case of severe pneumonia caused by Tropheryma whipplei combined with Legionella pneumophila. World J Emerg Med, 2023, 14(6): 492-494.
39. Yan J, Zhang B, Zhang Z, et al. Case report: Tropheryma whipplei hide in an AIDS patient With Pneumocysti s pneumonia. Front Public Health, 2021, 9: 663093.
40. Raoult D, La Scola B, Lecocq P, et al. Culture and immunological detection of Tropheryma whippelii from the duodenum of a patient with Whipple disease. JAMA, 2001, 285(8): 1039-1043.
41. Maiwald M, von Herbay A, Fredricks DN, et al. Cultivation of Tropheryma whipplei from cerebrospinal fluid. J Infect Dis, 2003, 188(6): 801-808.
42. Raoult D, Fenollar F, Birg ML. Culture of T. Whipplei from the stool of a patient with Whipple’s disease. N Engl J Med, 2006, 355(14): 1503-1505.
43. Renesto P, Crapoulet N, Ogata H, et al. Genome-based design of a cell-free culture medium for Tropheryma whipplei. Lancet, 2003, 362(9382): 447-449.
44. Fenollar F, Raoult D. Molecular techniques in Whipple’s disease. Expert Rev Mol Diagn, 2001, 1(3): 299-309.
45. Moter A, Janneck M, Wolters M, et al. Potential role for urine polymerase chain reaction in the diagnosis of Whipple’s disease. Clin Infect Dis, 2019, 68(7): 1089-1097.
46. Donnelly JP, Chen SC, Kauffman CA, et al. Revision and update of the consensus definitions of invasive fungal disease from the european organization for research and treatment of cancer and the mycoses study group education and research consortium. Clin Infect Dis, 2020, 71(6): 1367-1376.
47. Pappas PG, Chen SC, Donnelly JP. The evidence supporting the revised EORTC/MSGERC definitions for invasive fungal infections. Clin Infect Dis, 2021, 72(Suppl 2): s77-s78.
48. Feurle GE, Junga NS, Marth T. Efficacy of ceftriaxone or meropenem as initial therapies in Whipple’s disease. Gastroenterology, 2010, 138(2): 478-486.
49. Lévy M, Poyart C, Lamarque D, et al. Whipple’s disease: acquired resistance to trimethoprim-sulfamethoxazole. Am J Gastroenterol, 2000, 95(9): 2390-2391.
50. Keinath RD, Merrell DE, Vlietstra R, et al. Antibiotic treatment and relapse in Whipple’s disease. Long-term follow-up of 88 patients. Gastroenterology, 1985, 88(6): 1867-1873.
51. Lagier JC, Fenollar F, Lepidi H, et al. Treatment of classic Whipple’s disease: from in vitro results to clinical outcome. J Antimicrob Chemother, 2014, 69(1): 219-227.
52. Feurle GE, Marth T. An evaluation of antimicrobial treatment for Whipple’s disease. Tetracycline versus trimethoprim-sulfamethoxazole. Dig Dis Sci, 1994, 39(8): 1642-1648.
53. Boulos A, Rolain JM, Raoult D. Antibiotic susceptibility of Tropheryma whipplei in MRC5 cells. Antimicrob Agents Chemother, 2004, 48(3): 747-752.
54. Boulos A, Rolain JM, Mallet MN, et al. Molecular evaluation of antibiotic susceptibility of Tropheryma whipplei in axenic medium. J Antimicrob Chemother, 2005, 55(2): 178-181.
55. Cannon WR. Whipple’s disease, genomics, and drug therapy. Lancet, 2003, 361(9372): 1916.
56. 刘运喜, 邢玉斌, 巩玉秀. 软式内镜清洗消毒技术规范WS507-2016. 中国感染控制杂志, 2017, 16(6): 587-592.

West China Medical Journal

Diagnosis for cases with Tropheryma whipplei detected from respiratory samples: West China suggestions

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