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Nitrogenous compounds in the saliva and blood of cirrhotic patients: a cross-sectional study

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Abstract

Objectives

Serum increase of nitrogenous compounds (NC) in cirrhotic patients has been associated with the development of hepatic encephalopathy (HE). However, the relation between NC in saliva and HE is unclear. The objective of this study is to measure the levels of nitric oxide and urea in the blood and saliva in 38 cirrhotic patients and correlate them with clinical characteristics and presence and grades of HE.

Material and methods

Automated enzymatic colourimetric assays were performed to determine the levels of NC. Diagnosis and severity of HE were determined based on the West Haven criteria and by using the inhibitory control test.

Results

HE was diagnosed in 89.47% of the patients, with the majority (60.50%) presenting covert HE. With regard to the measurement of NC, although nitric oxide is moderately correlated with its amount in blood and saliva (r = 0.630; P < 0.001), only salivary levels were associated with the presence of ascites and ecchymosis (P = 0.013 and P = 0.030, respectively). In patients with HE, the serum levels of urea were higher (P = 0.013) than those in patients without HE or minimal HE.

Conclusions

Nitrogenous compounds in the saliva were correlated with neither the presence nor grades of HE, whereas in the blood, only urea was positively correlated with the severity and presence of HE.

Clinical relevance

Saliva is an excellent fluid for diagnosing several diseases, but it does not seem to be able to collaborate with the identification of HE.

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References

  1. de Oliveira Rech B, Rocha Tenório J, Bertoldi Franco J, Medina JB, Gallottini M, Pérez-Sayáns M, Ortega KL (2021) Risk of bleeding during oral surgery in patients with liver cirrhosis: a systematic review. J Am Dent Assoc (1939) 152(1):46-54.e2. https://doi.org/10.1016/j.adaj.2020.09.018

    Article  Google Scholar 

  2. Marinho GB, Tenório JR, Munhoz L, Andrade NS, Arita ES, Ortega KL (2021) Detection of calcified atheromas on panoramic radiographs of cirrhotic patients. Special care in dentistry : official publication of the American Association of Hospital Dentists, the Academy of Dentistry for the Handicapped, and the American Society for Geriatric Dentistry 41(2):164–169. https://doi.org/10.1111/scd.12551

    Article  Google Scholar 

  3. Di Profio B, Inoue G, Marui VC, de França BN, Romito GA, Ortega KL, Holzhausen M, Pannuti CM (2018) Periodontal status of liver transplant candidates and healthy controls. J Periodontol 89(12):1383–1389. https://doi.org/10.1002/JPER.17-0710

    Article  PubMed  Google Scholar 

  4. Medina JB, Andrade NS, de Paula Eduardo F, Bezinelli L, Franco JB, Gallottini M, Braz-Silva PH, Ortega KL (2018) Bleeding during and after dental extractions in patients with liver cirrhosis. Int J Oral Maxillofac Surg 47(12):1543–1549. https://doi.org/10.1016/j.ijom.2018.04.007

    Article  PubMed  Google Scholar 

  5. Di Profio B, Villar CC, Saraiva L, Ortega KL, Pannuti CM (2017) Is periodontitis a risk factor for infections in cirrhotic patients? Med Hypotheses 106:19–22. https://doi.org/10.1016/j.mehy.2017.06.022

    Article  PubMed  Google Scholar 

  6. Yu H, Chen Y, Jiang P (2019) Prognostic value of hepatic encephalopathy for survival of patients with liver failure: a systematic review and meta-analysis. Ann Hepatol 18(4):607–612. https://doi.org/10.1016/j.aohep.2019.01.006

    Article  PubMed  Google Scholar 

  7. Iwakiri Y, Groszmann RJ (2007) Vascular endothelial dysfunction in cirrhosis. J Hepatol 46(5):927–934. https://doi.org/10.1016/j.jhep.2007.02.006

    Article  PubMed  Google Scholar 

  8. Vilstrup H, Amodio P, Bajaj J, Cordoba J, Ferenci P, Mullen KD, Weissenborn K, Wong P (2014) Hepatic encephalopathy in chronic liver disease: 2014 Practice Guideline by the American Association for the Study of Liver Diseases and the European Association for the Study of the Liver. Hepatology (Baltimore, Md.) 60(2):715–735. https://doi.org/10.1002/hep.27210

    Article  Google Scholar 

  9. Quero Guillén JC, Herrerías Gutiérrez JM (2006) Diagnostic methods in hepatic encephalopathy. Clinica chimica acta international journal of clinical chemistry 365(1–2):1–8. https://doi.org/10.1016/j.cca.2005.08.003

    Article  PubMed  Google Scholar 

  10. Rahimi RS, Rockey DC (2014) Hepatic encephalopathy: how to test and treat. Curr Opin Gastroenterol 30(3):265–271. https://doi.org/10.1097/MOG.0000000000000066

    Article  PubMed  Google Scholar 

  11. Cichoż-Lach H, Michalak A (2013) Current pathogenetic aspects of hepatic encephalopathy and noncirrhotic hyperammonemic encephalopathy. World J Gastroenterol 19(1):26–34. https://doi.org/10.3748/wjg.v19.i1.26

    Article  PubMed  PubMed Central  Google Scholar 

  12. Savlan I, Liakina V, Valantinas J (2014) Concise review of current concepts on nomenclature and pathophysiology of hepatic encephalopathy. Medicina (Kaunas) 50(2):75–81. https://doi.org/10.1016/j.medici.2014.06.008

    Article  Google Scholar 

  13. Mohammed NA, Abd El-Aleem S, Appleton I, Maklouf MM, Said M, McMahon RF (2003) Expression of nitric oxide synthase isoforms in human liver cirrhosis. J Pathol 200(5):647–655. https://doi.org/10.1002/path.1377

    Article  PubMed  Google Scholar 

  14. González-Abraldes J, García-Pagán JC, Bosch J (2002) Nitric oxide and portal hypertension. Metab Brain Dis 17(4):311–324. https://doi.org/10.1023/a:1021957818240

    Article  PubMed  Google Scholar 

  15. Papadopoulos N, Soultati A, Goritsas C, Lazaropoulou C, Achimastos A, Adamopoulos A, Dourakis SP (2010) Nitric oxide, ammonia, and CRP levels in cirrhotic patients with hepatic encephalopathy: is there a connection? J Clin Gastroenterol 44(10):713–719. https://doi.org/10.1097/MCG.0b013e3181d47f71

    Article  PubMed  Google Scholar 

  16. Bezinelli LM, Eduardo FP, de Carvalho D, Dos Santos Ferreira CE, de Almeida EV, Sanches LR, Esteves I, Campregher PV, Hamerschlak N, Corrêa L (2017) Therapeutic salivary monitoring of IV busulfan in patients undergoing hematopoietic stem cell transplantation: a pilot study. Bone Marrow Transplant 52(10):1384–1389. https://doi.org/10.1038/bmt.2017.142

    Article  PubMed  Google Scholar 

  17. Castro T, Fink M, Figueiredo M, Braz-Silva PH, Pannuti CM, Ortega KL, Gallottini M (2017) Polyomavirus BK and JC in individuals with chronic kidney failure, kidney transplantation, and healthy controls. Journal of clinical virology: the official publication of the Pan American Society for Clinical Virology 89:5–9. https://doi.org/10.1016/j.jcv.2017.02.003

    Article  Google Scholar 

  18. Figueiredo MA, Domingues Fink MC, Castro T, Braz-Silva PH, Steffens JC, Eduardo FP, Gallottini M, Ortega KL (2017) Detection of human polyomaviruses JC and BK in liver pretransplant patients. Oral Dis 23(8):1127–1133. https://doi.org/10.1111/odi.12707

    Article  PubMed  Google Scholar 

  19. Lasisi TJ, Raji YR, Salako BL (2016) Salivary creatinine and urea analysis in patients with chronic kidney disease: a case control study. BMC Nephrol 17:10. https://doi.org/10.1186/s12882-016-0222-x

    Article  PubMed  PubMed Central  Google Scholar 

  20. Dupont WD, Plummer WD (1990) Power and sample size calculations: a review and computer program. Control Clin Trials 11:116–128

    Article  Google Scholar 

  21. Gupta D, Ingle M, Shah K, Phadke A, Sawant P (2015) Prospective comparative study of inhibitory control test and psychometric hepatic encephalopathy score for diagnosis and prognosis of minimal hepatic encephalopathy in cirrhotic patients in the Indian subcontinent. J Dig Dis 16(7):400–407. https://doi.org/10.1111/1751-2980.12248

    Article  PubMed  Google Scholar 

  22. Elsaid MI, Rustgi VK (2020) Epidemiology of hepatic encephalopathy. Clin Liver Dis 24(2):157–174. https://doi.org/10.1016/j.cld.2020.01.001

    Article  PubMed  Google Scholar 

  23. FerreAracil C, Núñez Gómez L, TéllezVillajos L, Albillos Martínez A (2019) Epistaxis in the cirrhotic patient: a complication to be considered. Epistaxis en el paciente cirrótico: una complicación a tener en cuenta. Gastroenterologia y hepatologia 42(1):11–15. https://doi.org/10.1016/j.gastrohep.2018.08.003

    Article  Google Scholar 

  24. Bigot A, Tchan MC, Thoreau B, Blasco H, Maillot F (2017) Liver involvement in urea cycle disorders: a review of the literature. J Inherit Metab Dis 40(6):757–769. https://doi.org/10.1007/s10545-017-0088-5

    Article  PubMed  Google Scholar 

  25. Bucsics T, Krones E (2017) Renal dysfunction in cirrhosis: acute kidney injury and the hepatorenal syndrome. Gastroenterology report 5(2):127–137. https://doi.org/10.1093/gastro/gox009

    Article  PubMed  PubMed Central  Google Scholar 

  26. Kircheis G, Lüth S (2019) Pharmacokinetic and pharmacodynamic properties of L-ornithine L-aspartate (LOLA) in hepatic encephalopathy. Drugs 79(Suppl 1):23–29. https://doi.org/10.1007/s40265-018-1023-2

    Article  PubMed  PubMed Central  Google Scholar 

  27. Allaker RP, Silva Mendez LS, Hardie JM, Benjamin N (2001) Antimicrobial effect of acidified nitrite on periodontal bacteria. Oral Microbiol Immunol 16(4):253–256. https://doi.org/10.1034/j.1399-302x.2001.160410.x

    Article  PubMed  Google Scholar 

  28. Qu XM, Wu ZF, Pang BX, Jin LY, Qin LZ, Wang SL (2016) From nitrate to nitric oxide: the role of salivary glands and oral bacteria. J Dent Res 95(13):1452–1456. https://doi.org/10.1177/0022034516673019

    Article  PubMed  Google Scholar 

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Funding

This research has been supported by the Fundação de Amparo à Pesquisa do Estado de São Paulo – FAPESP (grant # 2017/18938–6).

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Authors and Affiliations

  1. Department of Stomatology, School of Dentistry, University of São Paulo, Av. Prof. Lineu Prestes, 2227 – Cidade Universitária, São Paulo, São Paulo, 05508-000, Brazil

    Nathália Tuany Duarte, Marina Gallottini & Karem L. Ortega

  2. Department of Oral Pathology and Diagnosis, School of Dentistry, Federal University of Rio de Janeiro, Rio de Janeiro, Brazil

    Jefferson R. Tenório

  3. Department of Dentistry, Federal University of Sergipe, Lagarto, Sergipe, Brazil

    Natália Silva Andrade

  4. School of Dentistry, University of Santo Amaro, São Paulo, Brazil

    Fabiana Martins

Authors
  1. Nathália Tuany Duarte
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  2. Jefferson R. Tenório
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  3. Natália Silva Andrade
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  4. Fabiana Martins
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  5. Marina Gallottini
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  6. Karem L. Ortega
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Contributions

Conceptualisation, Nathália Tuany Duarte and Karem López Ortega; methodology, Jefferson Rocha Tenório, Nathália Tuany Duarte and Natália Silva Andrade; formal analysis and investigation, Nathália Tuany Duarte, Jefferson Rocha Tenório and Natália Andrade; writing — original draft preparation, Nathália Tuany Duarte, Fabiana Martins and Marina Gallottini; writing — review and editing, Jefferson Rocha Tenório, Marina Gallottini, Fabiana Martins and Karem López Ortega; funding acquisition, Karem López Ortega; supervision, Karem López Ortega.

Corresponding author

Correspondence to Karem L. Ortega.

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All procedures performed in studies involving human participants were in accordance with the ethical standards of the institutional and/or national research committee and with the 1964 Helsinki Declaration and its later amendments or comparable ethical standards.

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Informed consent was obtained from all individual participants included in the study.

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The authors declare no competing interests.

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Duarte, N.T., Tenório, J.R., Andrade, N.S. et al. Nitrogenous compounds in the saliva and blood of cirrhotic patients: a cross-sectional study. Clin Oral Invest 26, 4587–4592 (2022). https://doi.org/10.1007/s00784-022-04426-9

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  • DOI: https://doi.org/10.1007/s00784-022-04426-9

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