Skip to main content

Advertisement

SpringerLink
Log in

Hyperammonemia Syndrome Due to Ureaplasma and Mycoplasma Infections in Solid Organ Transplant Recipients: Treatment and Prophylaxis Strategies

  • Published:
Current Treatment Options in Infectious Diseases Aims and scope Submit manuscript

Opinion statement

Hyperammonemia syndrome (HS) linked to Ureaplasma and Mycoplasma infections was first identified in lung transplant recipients. It is a highly morbid syndrome with mortality estimated to be as high as 70%. Yet there remains no consensus as to the best treatment and prophylaxis strategies. We aim to review existing data to guide decisions about choice and duration of empiric antimicrobials for HS secondary to Mollicute infections. Fluroquinolones, tetracyclines, macrolides, and lincosamides are the preferred agents for the treatment of Ureaplasma and Mycoplasma infections. Resistance to these agents remains low in the USA; however, rates vary significantly worldwide. The ideal duration of treatment is ill-defined although a 14-day course is often employed for HS. A high index of suspicion and rapid initiation of therapy is critical for the diagnosis and prognosis of hyperammonemia syndrome from Ureaplasma and Mycoplasma infections. However, close consideration must be given to the choice of empiric antimicrobials as significant species specific and regional variation in resistance rates has been reported.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

References and Recommended Reading

Papers of particular interest, published recently, have been highlighted as: • Of importance •• Of major importance

  1. • Krutsinger D, Pezzulo A, Blevins AE, Reed RM, Voigt MD, Eberlein M. Idiopathic hyperammonemia after solid organ transplantation: primarily a lung problem? A single-center experience and systematic review. Clin Transplant [Internet]. John Wiley & Sons, Ltd; 2017 [cited 2023 Mar 12];31:e12957. Available from: https://onlinelibrary.wiley.com/doi/full/10.1111/ctr.12957. This was a systemic review of hyperammonemia syndrome in solid organ transplant recipients. Reported on incidence of HS in varied SOTR in the literature, mortality, and different treatment options employed.

  2. Lichtenstein GR, Yang YX, Nunes FA, Lewis JD, Tuchman M, Tino G, et al. Fatal hyperammonemia after orthotopic lung transplantation. Ann Intern Med. Am College Phys. 2000;132:283–7.

    CAS  Google Scholar 

  3. Leger RF, Silverman MS, Hauck ES, Guvakova KD. Hyperammonemia post lung transplantation: a review. Clin Med Insights Circ Respir Pulm Med [Internet]. 2020 [cited 2023 Feb 11];14:1–7. Available from: https://journals.sagepub.com/doi/pdf/https://doi.org/10.1177/1179548420966234

  4. Bharat A, Cunningham SA, Budinger GRS, Kreisel D, DeWet CJ, Gelman AE, et al. Disseminated Ureaplasma infection as a cause of fatal hyperammonemia in humans. Sci Transl Med [Internet]. NIH Public Access; 2015 [cited 2022 Dec 8];7:284re3. Available from: /pmc/articles/PMC4677674/

  5. Wang X, Greenwood-Quaintance KE, Karau MJ, Block DR, Mandrekar JN, Cunningham SA, et al. Ureaplasma parvum causes hyperammonemia in a pharmacologically immunocompromised murine model HHS public access. Eur J Clin Microbiol Infect Dis. 2017;36:517–22.

    Article  CAS  PubMed  Google Scholar 

  6. Wang X, Karau MJ, Greenwood-Quaintance KE, Block DR, Mandrekar JN, Cunningham SA, et al. Ureaplasma urealyticum causes hyperammonemia in an experimental immunocompromised murine model. PLoS One [Internet]. Public Library of Science; 2016 [cited 2023 Mar 10];11:e0161214. Available from: https://journals.plos.org/plosone/article?id=https://doi.org/10.1371/journal.pone.0161214

  7. Waites K, Taylor-Robinson D. Manual of clinical microbiology: Mycoplasma and Ureaplasma [Internet]. 11th ed. Jorgensen J, Carroll K, Funke G, Pfaller M, Landry M, Richter S, et al., editors. ASM Press; 2015 [cited 2023 Feb 13]. Available from: https://eds-p-ebscohost-com.proxy-hs.researchport.umd.edu/eds/ebookviewer/ebook/ZTAyNXhuYV9fMTAyMDI4OV9fQU41?sid=9ddb33ba-2032-46ef-91df-87f9efe01f5c@redis&vid=2&format=EB

  8. Waites KB, Katz B, Schelonka RL. Mycoplasmas and Ureaplasmas as neonatal pathogens. Clin Microbiol Rev [Internet]. American Society for Microbiology (ASM); 2005 [cited 2023 Feb 11];18:757. Available from: /pmc/articles/PMC1265909/

  9. Nakashima K, Shigehara K, Kawaguchi S, Wakatsuki A, Kobori Y, Nakashima K, et al. Prevalence of human papillomavirus infection in the oropharynx and urine among sexually active men: a comparative study of infection by papillomavirus and other organisms, including Neisseria gonorrhoeae, Chlamydia trachomatis, Mycoplasma spp., and Ureaplasma spp. BMC Infect Dis [Internet]. BioMed Central; 2014 [cited 2023 Mar 18];14:43. Available from: /pmc/articles/PMC3907364/

  10. Buzo BF, Preiksaitis JK, Halloran K, Nagendran J, Townsend DR, Zelyas N, et al. Association between Mycoplasma and Ureaplasma airway positivity, ammonia levels, and outcomes post–lung transplantation: a prospective surveillance study. American Journal of Transplantation [Internet]. John Wiley and Sons Inc; 2021 [cited 2023 Feb 11];21:2123–31. Available from: http://www.amjtransplant.org/article/S1600613522085884/fulltext

  11. •• Roberts SC, Bharat A, Kurihara C, Tomic R, Ison MG. Impact of screening and treatment of Ureaplasma species on hyperammonemia syndrome in lung transplant recipients: a single center experience. Clin Infect Dis [Internet]. Oxford University Press; 2021 [cited 2023 Feb 11];73:e2531. Available from: /pmc/articles/PMC8563172/. This single center study showed that donor derived Ureaplasma species infection in lung transplant recipients was associated with hyperammonemia syndrome and that there was a benefit to screening for Ureaplasma infections and employing a prophylactic antimicrobial strategy.

  12. Waites KB, Xiao L, Paralanov V, Viscardi RM, Glass JI. Molecular methods for the detection of Mycoplasma and Ureaplasma infections in humans: a paper from the 2011 William Beaumont Hospital Symposium on Molecular Pathology. J Mol Diagn [Internet]. American Society for Investigative Pathology; 2012 [cited 2023 Feb 19];14:437. Available from: /pmc/articles/PMC3427874/

  13. Xiao L, Glass JI, Paralanov V, Yooseph S, Cassell GH, Duffy LB, et al. Detection and characterization of human Ureaplasma species and Serovars by real-time PCR. J Clin Microbiol [Internet]. American Society for Microbiology (ASM); 2010 [cited 2023 Feb 19];48:2715. Available from: /pmc/articles/PMC2916572/

  14. O’Sullivan MVN, Isbel NM, Johnson DW, Rencken K, Byrne S, Graham MM, et al. Disseminated pyogenic Mycoplasma pneumoniae infection in a renal transplant recipient, detected by broad-range polymerase chain reaction. Clinical Infectious Diseases [Internet]. Oxford Academic; 2004 [cited 2023 Feb 11];39:e98–9. Available from: https://academic.oup.com/cid/article/39/9/e98/407703

  15. Garcia-Porrua C, Blanco FJ, Hernandez A, Atanes A, Galdo F, Moure R, et al. Septic arthritis by Mycoplasma hominis: a case report and review of the medical literature. Ann Rheum Dis [Internet]. BMJ Publishing Group Ltd; 1997 [cited 2023 Feb 11];56:699–700. Available from: https://ard.bmj.com/content/56/11/699

  16. Smibert OC, Wilson HL, Sohail A, Narayanasamy S, Schultz MB, Ballard SA, et al. Donor-derived Mycoplasma hominis and an apparent cluster of M. hominis cases in solid organ transplant recipients. Clinical Infectious Diseases [Internet]. Oxford Academic; 2017 [cited 2023 Mar 17];65:1504–8. Available from: https://academic.oup.com/cid/article/65/9/1504/3925587

  17. Hopkins PM, Winlaw DS, Chhajed PN, Harkness JL, Horton MD, Keogh AM, et al. BRIEF COMMUNICATIONS: Mycoplasma infection in heart and lung transplantation. 2002;

  18. Sampath R, Patel R, Cunningham SA, Arif S, Daly RC, Badley AD, et al. Cardiothoracic transplant recipient mycoplasma hominis: an uncommon infection with probable donor transmission. EBioMedicine Elsevier BV. 2017;19:84–90.

    Article  Google Scholar 

  19. Loupy A, Join-Lambert OF, Bébéar C-M, Legendre C, Anglicheau D. Urogenital mycoplasma: an emerging cause of deep wound infection after kidney transplantation? NDT Plus [Internet]. 2008 [cited 2023 Mar 18];4:239–40. Available from: https://academic.oup.com/ckj/article/1/4/239/334908

  20. Divithotewala C, Sweeney EL, Burke A, Graves B, Stewart A, Whiley D, et al. Mycoplasma hominis and Ureaplasma urealyticum infections in the immediate post-lung transplant period: a case series and literature review. Transplant Infectious Disease: John Wiley and Sons Inc; 2023.

    Google Scholar 

  21. Hagiya H, Yoshida H, Yamamoto N, Kimura K, Ueda A, Nishi I, et al. Mycoplasma hominis periaortic abscess following heart–lung transplantation. Transplant Infectious Disease [Internet]. John Wiley & Sons, Ltd; 2017 [cited 2023 Feb 12];19:e12697. Available from: https://onlinelibrary.wiley.com/doi/full/10.1111/tid.12697

  22. Gerber L, Gaspert A, Braghetti A, Zwahlen H, Wüthrich R, Zbinden R, et al. Ureaplasma and Mycoplasma in kidney allograft recipients—a case series and review of the literature. Transplant Infectious Disease [Internet]. John Wiley & Sons, Ltd; 2018 [cited 2023 Feb 12];20:e12937. Available from: https://onlinelibrary.wiley.com/doi/full/10.1111/tid.12937

  23. Eilers E, Moter A, Bollmann R, Haffner D, Querfeld U. Intrarenal abscesses due to Ureaplasma urealyticum in a transplanted kidney. J Clin Microbiol [Internet]. J Clin Microbiol; 2007 [cited 2023 Feb 12];45:1066–8. Available from: https://pubmed.ncbi.nlm.nih.gov/17229853/

  24. García C, Ugalde E, Monteagudo I, Saez A, Agüero J, Martinez-Martinez L, et al. Isolation of Mycoplasma hominis in critically ill patients with pulmonary infections: clinical and microbiological analysis in an intensive care unit. Intensive Care Med [Internet]. Springer; 2007 [cited 2023 Feb 11];33:143–7. Available from: https://link.springer.com/article/https://doi.org/10.1007/s00134-006-0435-8

  25. • Fernandez R, Ratliff A, Crabb D, Waites KB, Bharat A. Ureaplasma transmitted from donor lungs is pathogenic after lung transplantation. Ann Thorac Surg. Elsevier; 2017;103:670–1. In this report, the authors showed that a case of Ureaplasma associated hyperammonemia syndrome in a lung transplant recipient was a donor derived infection.

  26. Vogel U, Luneberg E, Kuse ER, Nuelinger AL, Frosch M. Extragenital Mycoplasma hominis infection in two liver transplant recipients. Clinical Infectious Diseases [Internet]. Oxford Academic; 1997 [cited 2023 Feb 11];24:512–3. Available from: https://academic.oup.com/cid/article/24/3/512/430988

  27. Lyon GM, Andrew ; ], Meredith FT, Harrell L], Tapson V, Davis D, et al. Mycoplasma hominis pneumonia complicating bilateral lung transplantation* case report and review of the literature.

  28. Baker AW, Messina JA, Maziarz EK, Saullo J, Miller R, Miller R, et al. 1758. Epidemiology of invasive Mycoplasma and Ureaplasma infections early after lung transplantation. Open Forum Infect Dis [Internet]. Oxford University Press; 2019 [cited 2023 Mar 17];6:S646. Available from: /pmc/articles/PMC6808825/

  29. Geißdörfer W, Sandner G, John S, Gessner A, Schoerner C, Schröppel K. Ureaplasma urealyticum Meningitis in an adult patient. J Clin Microbiol [Internet]. American Society for Microbiology (ASM); 2008 [cited 2023 Feb 11];46:1141. Available from: /pmc/articles/PMC2268352/

  30. Kamel AY, Emtiazjoo AM, Adkins L, Shahmohammadi A, Alnuaimat H, Pelaez A, et al. Hyperammonemia after lung transplantation: systematic review and a mini case series.

  31. Chen C, Bain KB, Iuppa JA, Yusen RD, Byers DE, Patterson GA, et al. Hyperammonemia syndrome after lung transplantation: a single center experience. Transplantation [Internet]. Lippincott Williams and Wilkins; 2016 [cited 2023 Mar 11];100:678–84. Available from: https://journals.lww.com/transplantjournal/Fulltext/2016/03000/Hyperammonemia_Syndrome_After_Lung.36.aspx

  32. • Buzo BF, Preiksaitis JK, Halloran K, Nagendran J, Townsend DR, Zelyas N, et al. Hyperammonemia syndrome post-lung transplantation: case series and systematic review of literature. Transplant Infectious Disease. John Wiley and Sons Inc; 2022;24. This article included a case series and comprehensive systemic review of HS in lung transplant recipients. Mortality rate from HS in lung transplant recipients was found to be 59.1%.

  33. • Tantengco OAG, De Jesus FCC, Gampoy EFS, Ornos EDB, Vidal MS, Abad CLR. Hyperammonemia syndrome associated with Ureaplasma spp. Infections in immunocompromised patients and transplant recipients: a systematic review and meta-analysis. Clin Transplant. John Wiley and Sons Inc; 2021;35. This was systemic review and meta-analysis which showed an increased risk of developing hyperammonemia syndrome in Ureaplasma species infected lung transplant recipients than Ureaplasma species negative recipients.

  34. Smith DGE, Russell WC, Ingledew WJ, Thirkell D. Hydrolysis of urea by Ureaplasma urealyticum generates a transmembrane potential with resultant ATP synthesis. J Bacteriol [Internet]. American Society for Microbiology (ASM); 1993 [cited 2023 Feb 13];175:3253. Available from: /pmc/articles/PMC204721/?report=abstract

  35. Schimke RT, Barile MF. Arginine metabolism in pleuropneumonia-like organisms isolated from mammalian cell culture. J Bacteriol [Internet]. American Society for Microbiology (ASM); 1963 [cited 2023 Feb 13];86:195. Available from: /pmc/articles/PMC278408/?report=abstract

  36. Aguilar C, Gohir W, Tikkanen J, Del Sorbo L, Chaparro C, Mazzulli T, et al. Ureaplasma spp. and Mycoplasma hominis PCR in respiratory samples from lung transplant recipients with hyperammonemia syndrome and cerebral edema. The Journal of Heart and Lung Transplantation. Elsevier; 2018;37:S360.

  37. Nowbakht C, Edwards AR, Rodriguez-Buritica DF, Luce AM, Doshi PB, De Golovine A, et al. Two cases of fatal hyperammonemia syndrome due to Mycoplasma hominis and Ureaplasma urealyticum in immunocompromised patients outside lung transplant recipients. Open Forum Infect Dis [Internet]. 2019 [cited 2022 Dec 8]; Available from: https://www.mayomedicallaboratories.com/test-

  38. Waites KB, Katz B, Schelonka RL. Mycoplasmas and Ureaplasmas as neonatal pathogens. Clin Microbiol Rev. 2005;18:757–89.

    Article  PubMed  PubMed Central  Google Scholar 

  39. Beeton ML, Spiller OB. Antibiotic resistance among Ureaplasma spp. isolates: cause for concern? Journal of Antimicrobial Chemotherapy [Internet]. Oxford Academic; 2017 [cited 2023 Feb 12];72:330–7. Available from: https://academic.oup.com/jac/article/72/2/330/2290945

  40. Waites KB, Clinical and Laboratory Standards Institute. Methods for antimicrobial susceptibility testing for human mycoplasmas : approved guideline. 2011;37.

  41. Xiao L, Crabb DM, Duffy LB, Paralanov V, Glass JI, Hamilos DL, et al. Mutations in ribosomal proteins and ribosomal RNA confer macrolide resistance in human Ureaplasma spp. Int J Antimicrob Agents Elsevier. 2011;37:377–9.

    Article  CAS  Google Scholar 

  42. Li X, Crabb DM, Duffy LB, Paralanov V, Glass JI, Waites KB. Chromosomal mutations responsible for fluoroquinolone resistance in Ureaplasma species in the United States. Antimicrob Agents Chemother [Internet]. American Society for Microbiology (ASM); 2012 [cited 2023 Feb 12];56:2780. Available from: /pmc/articles/PMC3346621/

  43. Chernova OA, Medvedeva ES, Mouzykantov AA, Baranova NB, Chernov VM. Mycoplasmas and their antibiotic resistance: the problems and prospects in controlling infections. Acta Naturae [Internet]. 2016 [cited 2023 Mar 11];8:24–34. Available from: https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4947986/pdf/AN20758251-29-024.pdf

  44. Ahmadi MH. Resistance to tetracyclines among clinical isolates of Mycoplasma hominis and Ureaplasma species: a systematic review and meta-analysis. Journal of Antimicrobial Chemotherapy [Internet]. Oxford Academic; 2021 [cited 2023 Apr 9];76:865–75. Available from: https://academic.oup.com/jac/article/76/4/865/6046148

  45. Valentine-King MA, Brown MB. Antibacterial resistance in Ureaplasma species and Mycoplasma hominis isolates from urine cultures in college-aged females. Antimicrob Agents Chemother [Internet]. American Society for Microbiology (ASM); 2017 [cited 2023 Mar 18];61. Available from: /pmc/articles/PMC5610494/

  46. Morris DJ, Jones LC, Davies RL, Sands K, Portal E, Spiller OB. MYCO WELL D-ONE detection of Ureaplasma spp. and Mycoplasma hominis in sexual health patients in Wales. European Journal of Clinical Microbiology and Infectious Diseases [Internet]. Springer Science and Business Media Deutschland GmbH; 2020 [cited 2023 Apr 9];39:2427–40. Available from: https://link.springer.com/article/https://doi.org/10.1007/s10096-020-03993-7

  47. Saraçoğlu M, Eroğlu A, Divrik RT. Development of antibiotic resistance against Ureaplasma urealyticum strains isolated from urogenital samples. J Urol Surg Galenos Yayinevi. 2018;5:17–20.

    Article  Google Scholar 

  48. Kasprzykowska U, Sobieszczańska B, Duda-Madej A, Secewicz A, Nowicka J, Gościniak G. A twelve–year retrospective analysis of prevalence and antimicrobial susceptibility patterns of Ureaplasma spp. and Mycoplasma hominis in the province of Lower Silesia in Poland. European Journal of Obstetrics and Gynecology and Reproductive Biology. Elsevier Ireland Ltd; 2018;220:44–9.

  49. Lee JY, Yang JS. Prevalence and antimicrobial susceptibility of Mycoplasma hominis and Ureaplasma species in nonpregnant female patients in South Korea indicate an increasing trend of pristinamycin-resistant isolates [Internet]. 2020. Available from: 10

  50. Meygret A, Le Roy C, Renaudin H, Bébéar C, Pereyre S. Tetracycline and fluoroquinolone resistance in clinical Ureaplasma spp. and Mycoplasma hominis isolates in France between 2010 and 2015. Journal of Antimicrobial Chemotherapy [Internet]. Oxford Academic; 2018 [cited 2023 Feb 12];73:2696–703. Available from: https://academic.oup.com/jac/article/73/10/2696/5050099

  51. Wang N, Liu W, Zhou Y, Liu Y. In vitro activities of nemonoxacin and other antimicrobial agents against human mycoplasma and ureaplasmas isolates and their defined resistance mechanisms. Front Microbiol. Frontiers Media S.A.; 2019;10.

  52. Zhao L, Liu A, Li R, Zhao S. Antimicrobial resistance, genetic characterization, and molecular epidemiology of Ureaplasma species in males with infertility. European Journal of Clinical Microbiology and Infectious Diseases [Internet]. Springer Science and Business Media Deutschland GmbH; 2020 [cited 2023 Apr 9];39:2177–83. Available from: https://link.springer.com/article/https://doi.org/10.1007/s10096-020-03969-7

  53. Boujemaa S, Mlik B, Ben Allaya A, Mardassi H, Ben Abdelmoumen Mardassi B. Spread of multidrug resistance among Ureaplasma serovars, Tunisia. Antimicrob Resist Infect Control [Internet]. BioMed Central Ltd.; 2020 [cited 2023 Apr 9];9:1–10. Available from: https://aricjournal.biomedcentral.com/articles/https://doi.org/10.1186/s13756-020-0681-5

  54. Ahouga Voufo R, Maïdadi MF, Mbah EC, Esemu LF, Fouodji HP, Molu JP, et al. STUDY on the gender prevalence and sensitivity of urogenital mycoplasmas to antibiotics in YAOUNDE, CAMEROON. Sci Afr. Elsevier B.V.; 2020;8.

  55. Maldonado-Arriaga B, Escobar-Escamilla N, Pérez-Razo JC, Alcaráz-Estrada SL, Flores-Sánchez I, Moreno-García D, et al. Mollicutes antibiotic resistance profile and presence of genital abnormalities in couples attending an infertility clinic. Journal of International Medical Research. SAGE Publications Ltd; 2020;48.

  56. Jang YS, Min JW, Kim YS. Positive culture rate and antimicrobial susceptibilities of Mycoplasma hominis and Ureaplasma urealyticum. Obstet Gynecol Sci. Korean Society of Obstetrics and Gynecology; 2019;62:127–33.

  57. Beeton ML, Chalker VJ, Jones LC, Maxwell NC, Spiller OB. Antibiotic resistance among clinical Ureaplasma isolates recovered from neonates in England and Wales between 2007 and 2013. Antimicrob Agents Chemother [Internet]. American Society for Microbiology (ASM); 2016 [cited 2023 Apr 9];60:52. Available from: /pmc/articles/PMC4704235/

  58. Fernández J, Karau MJ, Cunningham SA, Greenwood-Quaintance KE, Patel R. Antimicrobial susceptibility and clonality of clinical Ureaplasma isolates in the United States. Antimicrob Agents Chemother [Internet]. American Society for Microbiology (ASM); 2016 [cited 2023 Feb 12];60:4793. Available from: /pmc/articles/PMC4958210/

  59. Song T, Ye A, Xie X, Huang J, Ruan Z, Kong Y, et al. Epidemiological investigation and antimicrobial susceptibility analysis of Ureaplasma species and Mycoplasma hominis in outpatients with genital manifestations. J Clin Pathol BMJ Publishing Group. 2014;67:817–20.

    Google Scholar 

  60. Zhu C, Liu J, Ling Y, Dong C, Wu T, Yu X, et al. Prevalence and antimicrobial susceptibility of Ureaplasma urealyticum and Mycoplasma hominis in Chinese women with genital infectious diseases. Indian J Dermatol Venereol Leprol. 2012;78:406–7.

    Article  PubMed  Google Scholar 

  61. Xie X, Zhang J. Trends in the rates of resistance of Ureaplasma urealyticum to antibiotics and identification of the mutation site in the quinolone resistance-determining region in Chinese patients. FEMS Microbiol Lett. 2006;259:181–6.

    Article  CAS  PubMed  Google Scholar 

  62. Kawai Y, Nakura Y, Wakimoto T, Nomiyama M, Tokuda T, Takayanagi T, et al. In vitro activity of five quinolones and analysis of the quinolone resistance-determining regions of gyrA, gyrB, parC, and parE in ureaplasma parvum and ureaplasma urealyticum clinical isolates from perinatal patients in Japan. Antimicrob Agents Chemother [Internet]. American Society for Microbiology; 2015 [cited 2023 Apr 9];59:2358–64. Available from: https://journals.asm.org/journal/aac

  63. Beeton ML, Chalker VJ, Maxwell NC, Kotecha S, Spiller OB. Concurrent titration and determination of antibiotic resistance in Ureaplasma species with identification of novel point mutations in genes associated with resistance. Antimicrob Agents Chemother. 2009;53:2020–7.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  64. Dumke R. Antimicrobial resistance in clinical isolates of ureaplasma spp. From samples in germany. Antimicrob Agents Chemother [Internet]. American Society for Microbiology; 2021 [cited 2023 Feb 12];65. Available from: https://doi.org/10.1128/CMR.00137-18

  65. Pereyre S, Renaudin H, Bébéar C, Bébéar CM. In vitro activities of the newer quinolones garenoxacin, gatifloxacin, and gemifloxacin against human mycoplasmas Antimicrob Agents Chemother. Am Soc Microbiol. 2004;48:3165–8.

    CAS  Google Scholar 

  66. Redelinghuys MJ, Ehlers MM, Dreyer AW, Lombaard HA, Kock MM. Antimicrobial susceptibility patterns of Ureaplasma species and Mycoplasma hominis in pregnant women. BMC Infect Dis. BioMed Central Ltd.; 2014;14.

  67. Samra Z, Rosenberg S, Dan M. Susceptibility of Ureaplasma urealyticum to tetracycline, doxycycline, erythromycin, roxithromycin, clarithromycin, azithromycin, levofloxacin and moxifloxacin. [Internet]. Taylor & Francis; 2013 [cited 2023 Mar 18];23:77–9. Available from: https://www.tandfonline.com/doi/abs/https://doi.org/10.1179/joc.2011.23.2.77

  68. Pereyre S, Gonzalez P, De Barbeyrac B, Darnige A, Renaudin H, Charron A, et al. Mutations in 23S rRNA account for intrinsic resistance to macrolides in Mycoplasma hominis and Mycoplasma fermentans and for acquired resistance to macrolides in M. hominis. Antimicrob Agents Chemother [Internet]. American Society for Microbiology; 2002 [cited 2023 Apr 9];46:3142–50. Available from: https://journals.asm.org/doi/https://doi.org/10.1128/AAC.46.10.3142-3150.2002

  69. Krausse R, Schubert S. In-Vitro activities of tetracyclines, macrolides, fluoroquinolones and clindamycin against Mycoplasma hominis and Ureaplasma ssp. isolated in Germany over 20 years. Clinical Microbiology and Infection [Internet]. Blackwell Publishing Ltd; 2010 [cited 2023 Feb 12];16:1649–55. Available from: http://www.clinicalmicrobiologyandinfection.com/article/S1198743X14605590/fulltext

  70. Pónyai K, Mihalik N, Ostorházi E, Farkas B, Párducz L, Marschalkó M, et al. Incidence and antibiotic susceptibility of genital mycoplasmas in sexually active individuals in Hungary. European Journal of Clinical Microbiology and Infectious Diseases [Internet]. Springer Verlag; 2013 [cited 2023 Feb 12];32:1423–6. Available from: https://link.springer.com/article/https://doi.org/10.1007/s10096-013-1892-y

  71. Yang T, Pan L, Wu N, Wang L, Liu Z, Kong Y, et al. Antimicrobial resistance in clinical Ureaplasma spp. and Mycoplasma hominis and structural mechanisms underlying quinolone resistance. Antimicrob Agents Chemother [Internet]. American Society for Microbiology; 2020 [cited 2023 Apr 9];64. Available from: https://journals.asm.org/doi/https://doi.org/10.1128/AAC.02560-19

  72. Kenny GE, Cartwright FD. Susceptibilities of Mycoplasma hominis, M. pneumoniae, and Ureaplasma urealyticum to GAR-936, dalfopristin, dirithromycin, evernimicin, gatifloxacin, linezolid, moxifloxacin, quinupristin-dalfopristin, and telithromycin compared to their susceptibilities to reference macrolides, tetracyclines, and quinolones. Antimicrob Agents Chemother [Internet]. American Society for Microbiology (ASM); 2001 [cited 2023 Apr 8];45:2604. Available from: /pmc/articles/PMC90699/

  73. Bébéar CM, De Barbeyrac B, Pereyre S, Renaudin H, Clerc M, Bébéar C. Activity of moxifloxacin against the urogenital mycoplasmas Ureaplasma spp., Mycoplasma hominis and Mycoplasma genitalium and Chlamydia trachomatis. Clinical Microbiology and Infection. Blackwell Publishing Ltd; 2008;14:801–5.

  74. Roberts SC, Bharat A, Kurihara C, Tomic R, Ison MG. Impact of screening and treatment of Ureaplasma species on hyperammonemia syndrome in lung transplant recipients: a single center experience. clin infect dis [internet]. Oxford University Press; 2021 [cited 2023 Feb 12];73:e2531. Available from: /pmc/articles/PMC8563172/

  75. Legouy C, Hu A, Mochel F, Weiss N, Collin A, Pereyre S, et al. Ureaplasma parvum causes hyperammonemia presenting as refractory status epilepticus after kidney transplant. J Crit Care WB Saunders. 2020;57:79–83.

    Article  CAS  Google Scholar 

  76. Cheema F, Kutzler HL, Olowofela AS, Maneckshana BT, Rochon C, Sheiner PA, et al. Successful management of noncirrhotic hyperammonemia syndrome after kidney transplantation from putative Ureaplasma infection. Transplant Infectious Disease [Internet]. John Wiley & Sons, Ltd; 2020 [cited 2023 Feb 11];22:e13332. Available from: https://onlinelibrary.wiley.com/doi/full/10.1111/tid.13332

  77. Kurihara C, Manerikar A, Kandula V, Cerier E, Bharat A. Prophylactic Ureaplasma-directed antimicrobials in lung donors can prevent fatal hyperammonemia.

  78. Waites KB, Clinical and Laboratory Standards Institute. Methods for antimicrobial susceptibility testing for human mycoplasmas : approved guideline.

  79. Zhou YH, Ma HX, Yang Y, Gu WM. Prevalence and antimicrobial resistance of Ureaplasma spp. and Mycoplasma hominis isolated from semen samples of infertile men in Shanghai, China from 2011 to 2016. European Journal of Clinical Microbiology and Infectious Diseases [Internet]. Springer Verlag; 2018 [cited 2023 Apr 9];37:729–34. Available from: https://link.springer.com/article/https://doi.org/10.1007/s10096-017-3167-5

  80. Díaz L, Cabrera L, Fernández T, Ibáñez I, Torres Y, Obregón Y, et al. Frequency and antimicrobial sensitivity of Ureaplasma urealyticum and Mycoplasma hominis in patients with vaginal discharge. MEDICC Rev [Internet]. 2013;15:45–7. Available from: http://www.liofi

  81. Schneider SC, Tinguely R, Droz S, Hilty M, Donà V, Bodmer T, et al. Antibiotic susceptibility and sequence type distribution of ureaplasma species isolated from genital samples in Switzerland. Antimicrob Agents Chemother [Internet]. American Society for Microbiology; 2015 [cited 2023 Apr 9];59:6026–31. Available from: https://journals.asm.org/doi/https://doi.org/10.1128/AAC.00895-15

  82. Ozturk S, Yildiz S, Dursun P, Yener Ilce B, Kaymaz O. Mycoplasma hominis profile in women: culture, kit, molecular diagnosis, antimicrobial resistance, and treatment. Microb Pathog. Academic Press; 2019;135.

  83. Wylam ME, Kennedy CC, Hernandez NM, Peters SG, Maleszewski JJ, Cassivi SD, et al. Fatal hyperammonaemia caused by Mycoplasma hominis. The Lancet. Elsevier; 2013;382:1956.

  84. Matson KM, Sonetti DA. Successful treatment of Ureaplasma-induced hyperammonemia syndrome post-lung transplant. Transplant Infectious Disease [Internet]. John Wiley & Sons, Ltd; 2019 [cited 2023 Mar 12];21:e13022. Available from: https://onlinelibrary.wiley.com/doi/full/10.1111/tid.13022

  85. Paparoupa M, Barten MJ, de Heer J, Giessen HS, Frings D, Kluge S. Hyperammonemia by Ureaplasma urealyticum pneumonia after lung transplantation. Respir Med Case Rep [Internet]. Elsevier; 2020 [cited 2023 Feb 11];30:101080. Available from: /pmc/articles/PMC7218208/

  86. Bächle F, Bansbach J, Hettich I, Lambeck J, Senbaklavaci, Kalbhenn J. Posterior reversible encephalopathy syndrome and hyperammonemia: two entities causing cerebral edema and status epilepticus in a female patient after lung transplantation. Anaesthesist. Springer Medizin; 2020;69:506–13.

  87. Grazioli A, Podell JE, Iacono A, Krupnik AS, Madathil RJ, Shah SR. Treatment of hyperammonemia using in-line renal replacement and hyperosmolar therapies within an extracorporeal membrane oxygenation circuit. Perfusion (United Kingdom). SAGE Publications Ltd; 2023;38:193–6.

  88. Michel C, Raimo M, Lazarevic V, Gaïa N, Leduc N, Knoop C, et al. Case report: about a case of hyperammonemia syndrome following lung transplantation: could metagenomic next-generation sequencing improve the clinical management? Front Med (Lausanne). Frontiers Media S.A.; 2021;8.

  89. Higgins AB, Farmakiotis D, Rogers R, Osband AJ, Seo A, Chen B, et al. Hyperammonemia syndrome due to Ureaplasma urealyticum in a kidney transplant recipient: a case of disseminated disease from a fluoroquinolone-resistant isolate. Transplant Infectious Disease [Internet]. John Wiley & Sons, Ltd; 2020 [cited 2023 Feb 11];22:e13328. Available from: https://onlinelibrary.wiley.com/doi/full/10.1111/tid.13328

  90. Cannon CA, Corcorran MA, Shaw KW, Montenovo M, Sibulesky L, Reyes JD, et al. Hyperammonemia syndrome due to Ureaplasma infection after liver-kidney transplant. Transpl Infect Dis [Internet]. NIH Public Access; 2020 [cited 2023 Feb 11];22:e13298. Available from: /pmc/articles/PMC7292677/

  91. Madathil RJ, Gilstrap LG, Pelletier MP, Mehra MR. Isolated hyperammonemic encephalopathy in heart transplantation. Journal of Heart and Lung Transplantation [Internet]. Elsevier USA; 2018 [cited 2023 Feb 11];37:427–9. Available from: http://www.jhltonline.org/article/S105324981732140X/fulltext

Download references

Author information

Authors and Affiliations

  1. Institute of Human Virology, University of Maryland School of Medicine, 725 W. Lombard St, Baltimore, MD, 21201, USA

    Ashley H. Barnes MD, Kapil Saharia MD & Katya Prakash MD

Authors
  1. Ashley H. Barnes MD
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Kapil Saharia MD
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Katya Prakash MD
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Katya Prakash MD.

Ethics declarations

Competing Interests

The authors declare no competing interests.

Human and Animal Rights

This article does not contain any studies with human or animal subjects performed by any of the authors.

Additional information

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Barnes, A.H., Saharia, K. & Prakash, K. Hyperammonemia Syndrome Due to Ureaplasma and Mycoplasma Infections in Solid Organ Transplant Recipients: Treatment and Prophylaxis Strategies. Curr Treat Options Infect Dis 15, 109–132 (2023). https://doi.org/10.1007/s40506-023-00265-8

Download citation

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s40506-023-00265-8

Keywords

Search

Navigation