Salmonella Typhi and Salmonella Paratyphi A elaborate distinct systemic metabolite signatures during enteric fever

eLife

Volumn 2014, Issue 3, 2014, Pages

  Näsström, Elin ^a   Tran Vu Thieu, Nga ^b   Dongol, Sabina ^b   Karkey, Abhilasha ^b   Vinh, Phat Voong ^b   Thanh, Tuyen Ha ^b   Johansson, Anders ^a   Arjyal, Amit ^b   Thwaites, Guy ^b,c   Dolecek, Christiane ^b,c   Basnyat, Buddha ^b   Baker, Stephen ^b,c,d   Antti, Henrik ^a  

^a UMEÅ UNIVERSITY   (Sweden)

^b OXFORD UNIVERSITY CLINICAL RESEARCH UNIT   (Viet Nam)

^c UNIVERSITY OF OXFORD   (United Kingdom)

^d LONDON SCHOOL OF HYGIENE AND TROPICAL MEDICINE   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

CARBOHYDRATE; ETHANOLAMINE; GLUCONIC ACID; MONOSACCHARIDE; PHENYLALANINE; PIPECOLIC ACID;

ADULT; AREA UNDER THE CURVE; ARTICLE; BACTERIAL GROWTH; BACTERIUM IDENTIFICATION; BLOOD CULTURE; CLINICAL ARTICLE; CONTROLLED STUDY; DATA PROCESSING; GAS CHROMATOGRAPHY; HUMAN; METABOLOMICS; PARTIAL LEAST SQUARES REGRESSION; PATTERN RECOGNITION; PRINCIPAL COMPONENT ANALYSIS; RANDOMIZED CONTROLLED TRIAL (TOPIC); RECEIVER OPERATING CHARACTERISTIC; SALMONELLA PARATYPHI; SALMONELLA TYPHI; TIME OF FLIGHT MASS SPECTROMETRY; TYPHOID FEVER;

EID: 84904015319     PISSN: None     EISSN: 2050084X     Source Type: Journal    
DOI: 10.7554/eLife.03100.001     Document Type: Article

References (50)

1. Antti H, Fahlgren A, Näsström E, Kouremenos K, Sundén-Cullberg J, Guo Y, Moritz T, Wolf-Watz H, Johansson A, Fallman M. 2013. Metabolic profiling for detection of Staphylococcus aureus infection and antibiotic resistance. PLOS ONE 8: e56971. doi: 10.1371/journal.pone.0056971.
2. Arjyal A, Basnyat B, Koirala S, Karkey A, Dongol S, Agrawaal KK, Shakya N, Shrestha K, Sharma M, Lama S, Shrestha K, Khatri NS, Shrestha U, Campbell JI, Baker S, Farrar J, Wolbers M, Dolecek C. 2011. Gatifloxacin versus chloramphenicol for uncomplicated enteric fever: an open-label, randomised, controlled trial. The Lancet Infectious Diseases 11: 445-454. doi: 10.1016/S1473-3099(11)70089-5.
3. Baker S, Favorov M, Dougan G. 2010. Searching for the elusive typhoid diagnostic. BMC Infectious Diseases 10: 45. doi: 10.1186/1471-2334-10-45.
4. Baker S, Holt KE, Clements AC, Karkey A, Arjyal A, Boni MF, Dongol S, Hammond N, Koirala S, Duy PT, Nga TV, Campbell JI, Dolecek C, Basnyat B, Dougan G, Farrar JJ. 2011. Combined high-resolution genotyping and geospatial analysis reveals modes of endemic urban typhoid fever transmission. Open Biology 1: 110008. doi: 10.1098/rsob.110008.
5. Baumgarner BL, Cooper BR. 2012. Evaluation of a tandem gas chromatography/time-of-flight mass spectrometry metabolomics platform as a single method to investigate the effect of starvation on whole-animal metabolism in rainbow trout (Oncorhynchus mykiss). The Journal of Experimental Biology 215: 1627-1632.
6. Buckle GC, Walker CLF, Black RE. 2012. Typhoid fever and paratyphoid fever: systematic review to estimate global morbidity and mortality for 2010. Journal of Global Health 2: 10401. doi: 10.7189/jogh.02.010401.
7. Bylesjö M, Rantalainen M, Cloarec O, Nicholson JK, Holmes E, Trygg J. 2006. OPLS discriminant analysis: combining the strengths of PLS-DA and SIMCA classification. Journal of Chemometrics 20: 341-351. doi: 10.1002/cem.1006.
8. Castillo S, Mattila I, Miettinen J, Orešič M, Hyötyläinen T. 2011. Data analysis tool for comprehensive two-dimensional gas chromatography/time-of-flight mass spectrometry. Analytical Chemistry 83: 3058-3067. doi: 10.1021/ac103308x.
9. Cui L, Lee YH, Kumar Y, Xu F, Lu K, Ooi EE, Tannenbaum SR, Ong CN. 2013. Serum metabolome and lipidome changes in adult patients with primary dengue infection. PLOS Neglected Tropical Diseases 7: e2373. doi: 10.1371/journal.pntd.0002373.
10. Didelot X, Achtman M, Parkhill J, Thomson NR, Falush D. 2007. A bimodal pattern of relatedness between the Salmonella Paratyphi A and Salmonella Typhi genomes: convergence or divergence by homologous recombination? Genome Research 17: 61-68. doi: 10.1101/gr.5512906.
11. Eriksson L, Trygg J, Wold S. 2008. CV-ANOVA for significance testing of PLS and OPLS models. Journal of Chemometrics 22: 594-600. doi: 10.1002/cem.1187.
12. Everest P, Wain J, Roberts M, Rook G, Dougan G. 2001. The molecular mechanisms of severe typhoid fever. Trends in Microbiology 9: 316-320. doi: 10.1016/S0966-842X(01)02067-4.
13. Gilman RH, Terminel M, Levine MM, Hernandez-Mendoza P, Hornick RB. 1975. Relative efficacy of blood, urine, rectal swab, bone-marrow, and rose-spot cultures for recovery of Salmonella Typhi in typhoid fever. Lancet 1: 1211-1213. doi: 10.1016/S0140-6736(75)92194-7.
14. Glynn JR, Hornick RB, Levine MM, Bradley DJ. 1995. Infecting dose and severity of typhoid: analysis of volunteer data and examination of the influence of the definition of illness used. Epidemiology and Infection 115: 23-30. doi: 10.1017/S0950268800058088.
15. Hartonen M, Mattila I, Ruskeepää AL, Orešič M, Hyötyläinen T. 2013. Characterization of cerebrospinal fluid by comprehensive two-dimensional gas chromatography coupled to time-of-flight mass spectrometry. Journal of Chromatography A 1293: 142-149. doi: 10.1016/j.chroma.2013.04.005.
16. Herndon DN, Wilmore DW, Mason AD Jnr, Pruitt BA Jnr. 1978. Abnormalities of phenylalanine and tyrosine kinetics. Significance in septic and nonseptic burned patients. Archives of Surgery 113: 133-135. doi: 10.1001/archsurg.1978.01370140023004.
17. Holmes E, Antti H. 2002. Chemometric contributions to the evolution of metabonomics: mathematical solutions to characterising and interpreting complex biological NMR spectra. The Analyst 127: 1549-1557. doi: 10.1039/b208254n.
18. Holt KE, Thomson NR, Wain J, Langridge GC, Hasan R, Bhutta ZA, Quail MA, Norbertczak H, Walker D, Simmonds M, White B, Bason N, Mungall K, Dougan G, Parkhill J. 2009. Pseudogene accumulation in the evolutionary histories of Salmonella enterica serovars Paratyphi A and Typhi. BMC Genomics 10: 36. doi: 10.1186/1471-2164-10-36.
19. Jansen AM, Hall LJ, Clare S, Goulding D, Holt KE, Grant AJ, Mastroeni P, Dougan G, Kingsley RA. 2011. A Salmonella Typhimurium-Typhi genomic chimera: a model to study Vi polysaccharide capsule function in vivo. PLOS Pathogens 7: e1002131. doi: 10.1371/journal.ppat.1002131.
20. Jiye A, Trygg J, Gullberg J, Johansson AI, Jonsson P, Antti H, Marklund SL, Moritz T. 2005. Extraction and GC/MS analysis of the human blood plasma metabolome. Analytical Chemistry 77: 8086-8094. doi: 10.1021/ac051211v.
21. Jones BD, Falkow S. 1996. Salmonellosis: host immune responses and bacterial virulence determinants. Annual Review of Immunology 14: 533-561. doi: 10.1146/annurev.immunol.14.1.533.
22. Karkey A, Arjyal A, Anders KL, Boni MF, Dongol S, Koirala S, My PV, Nga TV, Clements AC, Holt KE, Duy PT, Day JN, Campbell JI, Dougan G, Dolecek C, Farrar J, Basnyat B, Baker S. 2010. The burden and characteristics of enteric fever at a healthcare facility in a densely populated area of Kathmandu. PLOS ONE 5: e13988. doi: 10.1371/journal.pone.0013988.
23. Karkey A, Thompson CN, Tran Vu Thieu N, Dongol S, Le Thi Phuong T, Voong Vinh P, Arjyal A, Martin LB, Rondini S, Farrar JJ, Dolecek C, Basnyat B, Baker S, Baker JA. 2013. Differential epidemiology of Salmonella Typhi and Paratyphi A in Kathmandu, Nepal: a matched case control investigation in a highly endemic enteric fever setting. PLOS Neglected Tropical Diseases 7: e2391. doi: 10.1371/journal.pntd.0002391.
24. Koirala KD, Thanh DP, Thapa SD, Arjyal A, Karkey A, Dongol S, Shrestha UM, Farrar JJ, Basnyat B, Baker S. 2012. Highly resistant Salmonella enterica serovar Typhi with a novel gyrA mutation raises questions about the long-term efficacy of older fluoroquinolones for treating typhoid fever. Antimicrobial Agents and Chemotherapy 56: 2761-2762. doi: 10.1128/AAC.06414-11.
25. Langley RJ, Tsalik EL, van Velkinburgh JC, Glickman SW, Rice BJ, Wang C, Chen B, Carin L, Suarez A, Mohney RP, Freeman DH, Wang M, You J, Wulff J, Thompson JW, Moseley MA, Reisinger S, Edmonds BT, Grinnell B, Nelson DR, Dinwiddie DL, Miller NA, Saunders CJ, Soden SS, Rogers AJ, Gazourian L, Fredenburgh LE, Massaro AF, Baron RM, Choi AM, Corey GR, Ginsburg GS, Cairns CB, Otero RM, Fowler VG Jnr, Rivers EP, Woods CW, Kingsmore SF. 2013. An integrated clinico-metabolomic model improves prediction of death in sepsis. Science Translational Medicine 5: 195. doi: 10.1126/scitranslmed.3005893.
26. Lv H, Hung CS, Chaturvedi KS, Hooton TM, Henderson JP. 2011. Development of an integrated metabolomic profiling approach for infectious diseases research. The Analyst 136: 4752-4763. doi: 10.1039/c1an15590c.
27. Madsen R, Lundstedt T, Trygg J. 2010. Chemometrics in metabolomics-a review in human disease diagnosis. Analytica Chimica Acta 659: 23-33. doi: 10.1016/j.aca.2009.11.042.
28. Marko DC, Saffert RT, Cunningham SA, Hyman J, Walsh J, Arbefeville S, Howard W, Pruessner J, Safwat N, Cockerill FR, Bossler AD, Patel R, Richter SS. 2012. Evaluation of the Bruker Biotyper and Vitek MS matrix-assisted laser desorption ionization-time of flight mass spectrometry systems for identification of nonfermenting gram-negative bacilli isolated from cultures from cystic fibrosis patients. Journal of Clinical Microbiology 50: 2034-2039. doi: 10.1128/JCM.00330-12.
29. Maskey AP, Day JN, Phung QT, Thwaites GE, Campbell JI, Zimmerman M, Farrar JJ, Basnyat B. 2006. Salmonella enterica serovar Paratyphi A and S. enterica serovar Typhi cause indistinguishable clinical syndromes in Kathmandu, Nepal. Clinical infectious diseases 42: 1247-1253. doi: 10.1086/503033.
30. Moore CE, Pan-Ngum W, Wijedoru LP, Sona S, Nga TV, Duy PT, Vinh PV, Chheng K, Kumar V, Emary K, Carter M, White L, Baker S, Day NP, Parry CM. 2014. Evaluation of the diagnostic accuracy of a typhoid IgM flow assay for the diagnosis of typhoid fever in Cambodian children using a Bayesian latent class model assuming an imperfect gold standard. The American Journal of Tropical Medicine and Hygiene 90: 114-120. doi: 10.4269/ajtmh.13-0384.
31. Nga TV, Karkey A, Dongol S, Thuy HN, Dunstan S, Holt K, Tu le TP, Campbell JI, Chau TT, Chau NV, Arjyal A, Koirala S, Basnyat B, Dolecek C, Farrar J, Baker S. 2010. The sensitivity of real-time PCR amplification targeting invasive Salmonella serovars in biological specimens. BMC Infectious Diseases 10: 125. doi: 10.1186/1471-2334-10-125.
32. Nga TVT, Parry CM, Le T, Lan NP, Diep TS, Campbell JI, Hoang NV, Dung le T, Wain J, Dolecek C, Farrar JJ, Chau NV, Hien TT, Day JN, Baker S. 2012. The decline of typhoid and the rise of non-typhoid salmonellae and fungal infections in a changing HIV landscape: bloodstream infection trends over 15 years in southern Vietnam. Transactions of the Royal Society of Tropical Medicine and Hygiene 106: 26-34. doi: 10.1016/j.trstmh.2011.10.004.
33. Ochiai RL, Acosta CJ, Danovaro-Holliday MC, Baiqing D, Bhattacharya SK, Agtini MD, Bhutta ZA, Canh do G, Ali M, Shin S, Wain J, Page AL, Albert MJ, Farrar J, Abu-Elyazeed R, Pang T, Galindo CM, von Seidlein L, Clemens JD, Domi Typhoid Study Group. 2008. A study of typhoid fever in five Asian countries: disease burden and implications for controls. Bulletin of the World Health Organization. doi: 10.2471/BLT.06.039818.
34. Pandit A, Arjyal A, Day JN, Paudyal B, Dangol S, Zimmerman MD, Yadav B, Stepniewska K, Campbell JI, Dolecek C, Farrar JJ, Basnyat B. 2007. An open randomized comparison of gatifloxacin versus cefixime for the treatment of uncomplicated enteric fever. PLOS ONE 2: e542. doi: 10.1371/journal.pone.0000542.
35. Parry CM, Hien TT, Dougan G, White NJ, Farrar JJ. 2002. Typhoid fever. The New England Journal of Medicine 347: 1770-1782. doi: 10.1056/NEJMra020201.
36. Parry CM, Thompson C, Vinh H, Chinh NT, Phuong le T, Ho VA, Hien TT, Wain J, Farrar JJ, Baker S. 2014. Risk factors for the development of severe typhoid fever in Vietnam. BMC Infectious Diseases 14: 73. doi: 10.1186/1471-2334-14-73.
37. Parry CM, Vinh H, Chinh NT, Wain J, Campbell JI, Hien TT, Farrar JJ, Baker S. 2011a. The influence of reduced susceptibility to fluoroquinolones in Salmonella enterica serovar Typhi on the clinical response to ofloxacin therapy. PLOS Neglected Tropical Diseases 5: e1163. doi: 10.1371/journal.pntd.0001163.
38. Parry CM, Wijedoru L, Arjyal A, Baker S. 2011b. The utility of diagnostic tests for enteric fever in endemic locations. Expert Review of Anti-infective Therapy 9: 711-725. doi: 10.1586/eri.11.47.
39. du Preez I, Loots DT. 2013. New sputum metabolite markers implicating adaptations of the host to Mycobacterium tuberculosis, and vice versa. Tuberculosis 93: 330-337. doi: 10.1016/j.tube.2013.02.008.
40. Sengupta A, Ghosh S, Basant A, Malusare S, Johri P, Pathak S, Sharma S, Sonawat HM. 2011. Global host metabolic response to Plasmodium vivax infection: a 1H NMR based urinary metabonomic study. Malaria Journal 10: 384. doi: 10.1186/1475-2875-10-384.
41. Stone M. 1974. Cross-validatory choice and assessment of statistical predictions. Journal of the Royal Statistical Society: Series B (Statistical Methodology) 36: 111-147.
42. Thiennimitr P, Winter SE, Winter MG, Xavier MN, Tolstikov V, Huseby DL, Sterzenbach T, Tsolis RM, Roth JR, Bäumler AJ. 2011. Intestinal inflammation allows Salmonella to use ethanolamine to compete with the microbiota. Proceedings of the National Academy of Sciences of the United States of America 108: 17480-17485. doi: 10.1073/pnas.1107857108.
43. Vogel-Adghough D, Stahl E, Návarová H, Zeier J. 2013. Pipecolic acid enhances resistance to bacterial infection and primes salicylic acid and nicotine accumulation in tobacco. Plant Signaling & Behavior 8: e26366. doi: 10.4161/psb.26366.
44. Vollaard AM, Ali S, van Asten HA, Widjaja S, Visser LG, Surjadi C, van Dissel JT. 2004. Risk factors for typhoid and paratyphoid fever in Jakarta, Indonesia. The Journal of the American Medical Association 291: 2607-2615.
45. Wain J, Diep TS, Ho VA, Walsh AM, Nguyen TT, Parry CM, White NJ. 1998. Quantitation of bacteria in blood of typhoid fever patients and relationship between counts and clinical features, transmissibility, and antibiotic resistance. Journal of Clinical Microbiology 36: 1683-1687.
46. Walters MS, Routh J, Mikoleit M, Kadivane S, Ouma C, Mubiru D, Mbusa B, Murangi A, Ejoku E, Rwantangle A, Kule U, Lule J, Garrett N, Halpin J, Maxwell N, Kagirita A, Mulabya F, Makumbi I, Freeman M, Joyce K, Hill V, Downing R, Mintz E. 2014. Shifts in geographic distribution and antimicrobial resistance during a prolonged typhoid fever outbreak-Bundibugyo and Kasese Districts, Uganda, 2009-2011. PLOS Neglected Tropical Diseases 8: e2726. doi: 10.1371/journal.pntd.0002726.
47. Wannemacher RW Jnr, Klainer AS, Dinterman RE, Beisel WR. 1976. The significance and mechanism of an increased serum phenylalanine-tyrosine ratio during infection. The American Journal of Clinical Nutrition 29: 997-1006.
48. Werth N, Beerlage C, Rosenberger C, Yazdi AS, Edelmann M, Amr A, Bernhardt W, von Eiff C, Becker K, Schäfer A, Peschel A, Kempf VA. 2010. Activation of hypoxia inducible factor 1 is a general phenomenon in infections with human pathogens. PLOS ONE 5: e11576. doi: 10.1371/journal.pone.0011576.
49. Wold S, Esbensen K, Geladi P. 1987. Principal component analysis. Chemometrics and Intelligent Laboratory Systems 2: 37-52. doi: 10.1016/0169-7439(87)80084-9.
50. Zoller H, Schloegl A, Schroecksnadel S, Vogel W, Fuchs D. 2012. Interferon-alpha therapy in patients with hepatitis C virus infection increases plasma phenylalanine and the phenylalanine to tyrosine ratio. Journal of interferon & cytokine research 32: 216-220. doi: 10.1089/jir.2011.0093.