Show simple item record

Salivary exRNA biomarkers to detect gingivitis and monitor disease regression

dc.contributor.authorKaczor‐urbanowicz, Karolina E.
dc.contributor.authorTrivedi, Harsh M.
dc.contributor.authorLima, Patricia O.
dc.contributor.authorCamargo, Paulo M.
dc.contributor.authorGiannobile, William V.
dc.contributor.authorGrogan, Tristan R.
dc.contributor.authorGleber‐netto, Frederico O.
dc.contributor.authorWhiteman, Yair
dc.contributor.authorLi, Feng
dc.contributor.authorLee, Hyo Jung
dc.contributor.authorDharia, Karan
dc.contributor.authorAro, Katri
dc.contributor.authorMartin Carreras‐presas, Carmen
dc.contributor.authorAmuthan, Saarah
dc.contributor.authorVartak, Manjiri
dc.contributor.authorAkin, David
dc.contributor.authorAl‐adbullah, Hiba
dc.contributor.authorBembey, Kanika
dc.contributor.authorKlokkevold, Perry R.
dc.contributor.authorElashoff, David
dc.contributor.authorBarnes, Virginia M.
dc.contributor.authorRichter, Rose
dc.contributor.authorDeVizio, William
dc.contributor.authorMasters, James G.
dc.contributor.authorWong, David T. W.
dc.date.accessioned2018-07-13T15:47:35Z
dc.date.available2019-09-04T20:15:39Zen
dc.date.issued2018-07
dc.identifier.citationKaczor‐urbanowicz, Karolina E. ; Trivedi, Harsh M.; Lima, Patricia O.; Camargo, Paulo M.; Giannobile, William V.; Grogan, Tristan R.; Gleber‐netto, Frederico O. ; Whiteman, Yair; Li, Feng; Lee, Hyo Jung; Dharia, Karan; Aro, Katri; Martin Carreras‐presas, Carmen ; Amuthan, Saarah; Vartak, Manjiri; Akin, David; Al‐adbullah, Hiba ; Bembey, Kanika; Klokkevold, Perry R.; Elashoff, David; Barnes, Virginia M.; Richter, Rose; DeVizio, William; Masters, James G.; Wong, David T. W. (2018). "Salivary exRNA biomarkers to detect gingivitis and monitor disease regression." Journal of Clinical Periodontology 45(7): 806-817.
dc.identifier.issn0303-6979
dc.identifier.issn1600-051X
dc.identifier.urihttps://hdl.handle.net/2027.42/144647
dc.description.abstractAimThis study tests the hypothesis that salivary extracellular RNA (exRNA) biomarkers can be developed for gingivitis detection and monitoring disease regression.Materials and MethodsSalivary exRNA biomarker candidates were developed from a total of 100 gingivitis and nonâ gingivitis individuals using Affymetrix’s expression microarrays. The top 10 differentially expressed exRNAs were tested in a clinical cohort to determine whether the discovered salivary exRNA markers for gingivitis were associated with clinical gingivitis and disease regression. For this purpose, unstimulated saliva was collected from 30 randomly selected gingivitis subjects, the gingival and plaque indexes scores were taken at baseline, 3 and 6 weeks and salivary exRNAs were assayed by means of reverse transcription quantitative polymerase chain reaction.ResultsEight salivary exRNA biomarkers developed for gingivitis were statistically significantly changed over time, consistent with disease regression. A panel of four salivary exRNAs [SPRR1A, lncâ TET3â 2:1, FAM25A, CRCT1] can detect gingivitis with a clinical performance of 0.91 area under the curve, with 71% sensitivity and 100% specificity.ConclusionsThe clinical values of the developed salivary exRNA biomarkers are associated with gingivitis regression. They offer strong potential to be advanced for definitive validation and clinical laboratory development test.
dc.publisherR Foundation for Statistical Computing
dc.publisherWiley Periodicals, Inc.
dc.subject.otherbiomarkers
dc.subject.otherexRNA
dc.subject.othergingivitis
dc.subject.othermonitoring
dc.subject.othersaliva
dc.titleSalivary exRNA biomarkers to detect gingivitis and monitor disease regression
dc.typeArticleen_US
dc.rights.robotsIndexNoFollow
dc.subject.hlbsecondlevelDentistry
dc.subject.hlbtoplevelHealth Sciences
dc.description.peerreviewedPeer Reviewed
dc.description.bitstreamurlhttps://deepblue.lib.umich.edu/bitstream/2027.42/144647/1/jcpe12930.pdf
dc.description.bitstreamurlhttps://deepblue.lib.umich.edu/bitstream/2027.42/144647/2/jcpe12930_am.pdf
dc.identifier.doi10.1111/jcpe.12930
dc.identifier.sourceJournal of Clinical Periodontology
dc.identifier.citedreferenceNelson, P., Kiriakidou, M., Sharma, A., Maniataki, E., & Mourelatos, Z. ( 2003 ). The microRNA world: Small is mighty. Trends in Biochemical Sciences, 28, 534 â 540. https://doi.org/10.1016/j.tibs.2003.08.005
dc.identifier.citedreferenceHu, Z., Zimmermann, B. G., Zhou, H., Wang, J., Henson, B. S., Yu, W., â ¦ Wong, D. T. ( 2008 ). Exonâ level expression profiling: A comprehensive transcriptome analysis of oral fluids. Clinical Chemistry, 54, 824 â 832. https://doi.org/10.1373/clinchem.2007.096164
dc.identifier.citedreferenceJuusola, J., & Ballantyne, J. ( 2005 ). Multiplex mRNA profiling for the identification of body fluids. Forensic Science International, 152, 1 â 12. https://doi.org/10.1016/j.forsciint.2005.02.020
dc.identifier.citedreferenceKaczorâ Urbanowicz, K. E., Martin Carrerasâ Presas, C., Aro, K., Tu, M., Garciaâ Godoy, F., & Wong, D. T. ( 2017 ). Saliva diagnosticsâ Current views and directions. Experimental Biology and Medicine (Maywood, N.J.), 242, 459 â 472. https://doi.org/10.1177/1535370216681550
dc.identifier.citedreferenceKagiya, T. ( 2016 ). MicroRNAs: Potential biomarkers and therapeutic targets for alveolar bone loss in periodontal disease. International Journal of Molecular Sciences, 17, 1317. https://doi.org/10.3390/ijms17081317
dc.identifier.citedreferenceKajita, K., Honda, T., Amanuma, R., Domon, H., Okui, T., Ito, H., â ¦ Yamazaki, K. ( 2007 ). Quantitative messenger RNA expression of Tollâ like receptors and interferonâ alpha1 in gingivitis and periodontitis. Oral Microbiology and Immunology, 22, 398 â 402. https://doi.org/10.1111/j.1399-302X.2007.00377.x
dc.identifier.citedreferenceKassebaum, N. J., Smith, A. G. C., Bernabe, E., Fleming, T. D., Reynolds, A. E., Vos, T., â ¦ GBD 2015 Oral Health Collaborators. ( 2017 ). Global, regional, and national prevalence, incidence, and disabilityâ adjusted life years for oral conditions for 195 countries, 1990â 2015: A systematic analysis for the global burden of diseases, injuries, and risk factors. Journal of Dental Research, 96, 380 â 387. https://doi.org/10.1177/0022034517693566
dc.identifier.citedreferenceKim, J. J., Kim, C. J., & Camargo, P. M. ( 2013 ). Salivary biomarkers in the diagnosis of periodontal diseases. Journal of the California Dental Association, 41, 119 â 124.
dc.identifier.citedreferenceKinney, J. S., Morelli, T., Braun, T., Ramseier, C. A., Herr, A. E., Sugai, J. V., â ¦ Giannobile, W. V. ( 2011 ). Saliva/pathogen biomarker signatures and periodontal disease progression. Journal of Dental Research, 90, 752 â 758. https://doi.org/10.1177/0022034511399908
dc.identifier.citedreferenceKung, J. T., Colognori, D., & Lee, J. T. ( 2013 ). Long noncoding RNAs: Past, present, and future. Genetics, 193, 651 â 669. https://doi.org/10.1534/genetics.112.146704
dc.identifier.citedreferenceKuwahara, M., Yamashita, M., Shinoda, K., Tofukuji, S., Onodera, A., Shinnakasu, R., â ¦ Nakayama, T. ( 2012 ). The transcription factor Sox4 is a downstream target of signaling by the cytokine TGFâ beta and suppresses T(H)2 differentiation. Nature Immunology, 13, 778 â 786. https://doi.org/10.1038/ni.2362
dc.identifier.citedreferenceLangemeijer, S. M., Aslanyan, M. G., & Jansen, J. H. ( 2009 ). TET proteins in malignant hematopoiesis. Cell Cycle, 8, 4044 â 4048. https://doi.org/10.4161/cc.8.24.10239
dc.identifier.citedreferenceLee, A., Ghaname, C. B., Braun, T. M., Sugai, J. V., Teles, R. P., Loesche, W. J., â ¦ Kinney, J. S. ( 2012 ). Bacterial and salivary biomarkers predict the gingival inflammatory profile. Journal of Periodontology, 83, 79 â 89. https://doi.org/10.1902/jop.2011.110060
dc.identifier.citedreferenceLee, Y. H., Zhou, H., Reiss, J. K., Yan, X., Zhang, L., Chia, D., & Wong, D. T. ( 2011 ). Direct saliva transcriptome analysis. Clinical Chemistry, 57, 1295 â 1302. https://doi.org/10.1373/clinchem.2010.159210
dc.identifier.citedreferenceLi, Y., Zhou, X., St John, M. A., & Wong, D. T. ( 2004 ). RNA profiling of cellâ free saliva using microarray technology. Journal of Dental Research, 83, 199 â 203. https://doi.org/10.1177/154405910408300303
dc.identifier.citedreferenceLoe, H. ( 1967 ). The Gingival Index, the Plaque Index and the Retention Index Systems. Journal of Periodontology, 38 ( Suppl ), 610 â 616. https://doi.org/10.1902/jop.1967.38.6_part2.610
dc.identifier.citedreferenceMasterson, L., Sorgeloos, F., Winder, D., Lechner, M., Marker, A., Malhotra, S., â ¦ Sterling, J. ( 2015 ). Deregulation of SYCP2 predicts early stage human papillomavirusâ positive oropharyngeal carcinoma: A prospective whole transcriptome analysis. Cancer Science, 106, 1568 â 1575. https://doi.org/10.1111/cas.12809
dc.identifier.citedreferenceMauritz, J. M., Tiffert, T., Seear, R., Lautenschlager, F., Esposito, A., Lew, V. L., â ¦ Kaminski, C. F. ( 2010 ). Detection of Plasmodium falciparum â infected red blood cells by optical stretching. Journal of Biomedial Optics, 15, 030517. https://doi.org/10.1117/1.3458919
dc.identifier.citedreferenceMitsuhashi, K., Nosho, K., Sukawa, Y., Matsunaga, Y., Ito, M., Kurihara, H., â ¦ Shinomura, Y. ( 2015 ). Association of Fusobacterium species in pancreatic cancer tissues with molecular features and prognosis. Oncotarget, 6, 7209 â 7220.
dc.identifier.citedreferenceMorelli, T., Stella, M., Barros, S. P., Marchesan, J. T., Moss, K. L., Kim, S. J., â ¦ Offenbacher, S. ( 2014 ). Salivary biomarkers in a biofilm overgrowth model. Journal of Periodontology, 85, 1770 â 1778. https://doi.org/10.1902/jop.2014.140180
dc.identifier.citedreferenceMuhlemann, H. R., & Son, S. ( 1971 ). Gingival sulcus bleedingâ A leading symptom in initial gingivitis. Helvetica Odontologica Acta, 15, 107 â 113.
dc.identifier.citedreferenceNazar Majeed, Z., Philip, K., Alabsi, A. M., Pushparajan, S., & Swaminathan, D. ( 2016 ). Identification of gingival crevicular fluid sampling, analytical methods, and oral biomarkers for the diagnosis and monitoring of periodontal diseases: A systematic review. Disease Markers, 2016, 1804727.
dc.identifier.citedreferenceNussbaumer, C., Gharehbaghiâ Schnell, E., & Korschineck, I. ( 2006 ). Messenger RNA profiling: A novel method for body fluid identification by realâ time PCR. Forensic Science International, 157, 181 â 186. https://doi.org/10.1016/j.forsciint.2005.10.009
dc.identifier.citedreferenceOgata, Y., Matsui, S., Kato, A., Zhou, L., Nakayama, Y., & Takai, H. ( 2014 ). MicroRNA expression in inflamed and noninflamed gingival tissues from Japanese patients. Journal of Oral Science, 56, 253 â 260. https://doi.org/10.2334/josnusd.56.253
dc.identifier.citedreferenceParraâ Damas, A., Valero, J., Chen, M., Espana, J., Martin, E., Ferrer, I., â ¦ Saura, C. A. ( 2014 ). Crtc1 activates a transcriptional program deregulated at early Alzheimer’s diseaseâ related stages. Journal of Neuroscience, 34, 5776 â 5787. https://doi.org/10.1523/JNEUROSCI.5288-13.2014
dc.identifier.citedreferencePepe, M. S., Feng, Z., Janes, H., Bossuyt, P. M., & Potter, J. D. ( 2008 ). Pivotal evaluation of the accuracy of a biomarker used for classification or prediction: Standards for study design. Journal of the National Cancer Institute, 100, 1432 â 1438. https://doi.org/10.1093/jnci/djn326
dc.identifier.citedreferenceQuigley, G. A., & Hein, J. W. ( 1962 ). Comparative cleansing efficiency of manual and power brushing. Journal of the American Dental Association, 65, 26 â 29. https://doi.org/10.14219/jada.archive.1962.0184
dc.identifier.citedreferenceR Core Team. ( 2014 ). R: A language and environment for statistical computing. Vienna, Austria: R Foundation for Statistical Computing.
dc.identifier.citedreferenceRagvin, A., Moro, E., Fredman, D., Navratilova, P., Drivenes, O., Engstrom, P. G., â ¦ Becker, T. S. ( 2010 ). Longâ range gene regulation links genomic type 2 diabetes and obesity risk regions to HHEX, SOX4, and IRX3. Proceedings of the National Academy of Sciences of the United States of America, 107, 775 â 780. https://doi.org/10.1073/pnas.0911591107
dc.identifier.citedreferenceRajesh, K. S., Thomas, D., Hegde, S., & Kumar, M. S. ( 2013 ). Poor periodontal health: A cancer risk? Journal of Indian Society of Periodontology, 17, 706 â 710.
dc.identifier.citedreferenceRamfjord, S. P. ( 1959 ). Indices for prevalence and incidence of periodontal disease. Journal of Periodontology, 30, 51 â 59. https://doi.org/10.1902/jop.1959.30.1.51
dc.identifier.citedreferenceRaz, A., Carmi, P., Raz, T., Hogan, V., Mohamed, A., & Wolman, S. R. ( 1991 ). Molecular cloning and chromosomal mapping of a human galactosideâ binding protein. Cancer Research, 51, 2173 â 2178.
dc.identifier.citedreferenceSchmalz, G., Li, S., Burkhardt, R., Rinke, S., Krause, F., Haak, R., & Ziebolz, D. ( 2016 ). MicroRNAs as salivary markers for periodontal diseases: A new diagnostic approach? BioMed Research International, 2016, 1027525.
dc.identifier.citedreferenceSexton, W. M., Lin, Y., Kryscio, R. J., Dawson, 3rd, D. R., Ebersole, J. L., & Miller, C. S. ( 2011 ). Salivary biomarkers of periodontal disease in response to treatment. Journal of Clinical Periodontology, 38, 434 â 441. https://doi.org/10.1111/j.1600-051X.2011.01706.x
dc.identifier.citedreferenceShaila, M., Pai, G. P., & Shetty, P. ( 2013 ). Salivary protein concentration, flow rate, buffer capacity and pH estimation: A comparative study among young and elderly subjects, both normal and with gingivitis and periodontitis. Journal of Indian Society of Periodontology, 17, 42 â 46. https://doi.org/10.4103/0972-124X.107473
dc.identifier.citedreferenceStarkey, M. L., Davies, M., Yip, P. K., Carter, L. M., Wong, D. J., Mcmahon, S. B., & Bradbury, E. J. ( 2009 ). Expression of the regenerationâ associated protein SPRR1A in primary sensory neurons and spinal cord of the adult mouse following peripheral and central injury. The Journal of Comparative Neurology, 513, 51 â 68. https://doi.org/10.1002/cne.21944
dc.identifier.citedreferenceStemmler, S., Nothnagel, M., Parwez, Q., Petraschâ Parwez, E., Epplen, J. T., & Hoffjan, S. ( 2009 ). Variation in genes of the epidermal differentiation complex in German atopic dermatitis patients. International Journal of Immunogenetics, 36, 217 â 222. https://doi.org/10.1111/j.1744-313X.2009.00858.x
dc.identifier.citedreferenceStoecklinâ Wasmer, C., Guarnieri, P., Celenti, R., Demmer, R. T., Kebschull, M., & Papapanou, P. N. ( 2012 ). MicroRNAs and their target genes in gingival tissues. Journal of Dental Research, 91, 934 â 940. https://doi.org/10.1177/0022034512456551
dc.identifier.citedreferenceTomar, S. L., & Asma, S. ( 2000 ). Smokingâ attributable periodontitis in the United States: Findings from NHANES III. National Health and Nutrition Examination Survey. Journal of Periodontology, 71, 743 â 751. https://doi.org/10.1902/jop.2000.71.5.743
dc.identifier.citedreferenceTuresky, S., Gilmore, N. D., & Glickman, I. ( 1970 ). Reduced plaque formation by the chloromethyl analogue of victamine C. Journal of Periodontology, 41, 41 â 43. https://doi.org/10.1902/jop.1970.41.41.41
dc.identifier.citedreferenceVardarâ Sengul, S., Demirci, T., Sen, B. H., Erkizan, V., Kurulgan, E., & Baylas, H. ( 2007 ). Human beta defensinâ 1 and â 2 expression in the gingiva of patients with specific periodontal diseases. Journal of Periodontal Research, 42, 429 â 437. https://doi.org/10.1111/j.1600-0765.2006.00964.x
dc.identifier.citedreferenceWang, Y., Kou, Y., Wang, X., Cederbaum, A., & Wang, R. ( 2014 ). Multifactorial comparative proteomic study of cytochrome P450 2E1 function in chronic alcohol administration. PLoS ONE, 9, e92504. https://doi.org/10.1371/journal.pone.0092504
dc.identifier.citedreferenceWong, D. T. ( 2015 ). Salivary extracellular noncoding RNA: Emerging biomarkers for molecular diagnostics. Clinical Therapeutics, 37, 540 â 551. https://doi.org/10.1016/j.clinthera.2015.02.017
dc.identifier.citedreferenceWu, N., Song, Y., Pang, L., & Chen, Z. ( 2016 ). CRCT1 regulated by microRNAâ 520 g inhibits proliferation and induces apoptosis in esophageal squamous cell cancer. Tumour Biology, 37, 8271 â 8279. https://doi.org/10.1007/s13277-015-4730-2
dc.identifier.citedreferenceChapple, I. L., Bouchard, P., Cagetti, M. G., Campus, G., Carra, M. C., Cocco, F., â ¦ Schulte, A. G. ( 2017 ). Interaction of lifestyle, behaviour or systemic diseases with dental caries and periodontal diseases: Consensus report of group 2 of the joint EFP/ORCA workshop on the boundaries between caries and periodontal diseases. Journal of Clinical Periodontology, 44 ( Suppl 18 ), S39 â S51. https://doi.org/10.1111/jcpe.12685
dc.identifier.citedreferenceDeloukas, P., Earthrowl, M. E., Grafham, D. V., Rubenfield, M., French, L., Steward, C. A., â ¦ Rogers, J. ( 2004 ). The DNA sequence and comparative analysis of human chromosome 10. Nature, 429, 375 â 381. https://doi.org/10.1038/nature02462
dc.identifier.citedreferenceEbersole, J. L., Nagarajan, R., Akers, D., & Miller, C. S. ( 2015 ). Targeted salivary biomarkers for discrimination of periodontal health and disease(s). Frontiers in Cellular and Infection Microbiology, 5, 62.
dc.identifier.citedreferenceAinsztein, A. M., Brooks, P. J., Dugan, V. G., Ganguly, A., Guo, M., Howcroft, T. K., â ¦ Venkatachalam, S. ( 2015 ). The NIH Extracellular RNA Communication Consortium. Journal of Extracellular Vesicles, 4, 27493. https://doi.org/10.3402/jev.v4.27493
dc.identifier.citedreferenceAlbandar, J. M., & Kingman, A. ( 1999 ). Gingival recession, gingival bleeding, and dental calculus in adults 30 years of age and older in the United States, 1988â 1994. Journal of Periodontology, 70, 30 â 43. https://doi.org/10.1902/jop.1999.70.1.30
dc.identifier.citedreferenceAlâ Sabbagh, M., Alladah, A., Lin, Y., Kryscio, R. J., Thomas, M. V., Ebersole, J. L., & Miller, C. S. ( 2012 ). Bone remodelingâ associated salivary biomarker MIPâ 1alpha distinguishes periodontal disease from health. Journal of Periodontal Research, 47, 389 â 395. https://doi.org/10.1111/j.1600-0765.2011.01445.x
dc.identifier.citedreferenceAtabaki, M., Hashemi, M., Daneshvar, H., & Alijani, E. ( 2017 ). Lectin, galactosideâ binding, soluble, 3 rs4652 A/C gene variation and the risk for rheumatoid arthritis. Biomedical Reports, 6, 251 â 255. https://doi.org/10.3892/br.2017.838
dc.identifier.citedreferenceBinder Gallimidi, A., Fischman, S., Revach, B., Bulvik, R., Maliutina, A., Rubinstein, A. M., â ¦ Elkin, M. ( 2015 ). Periodontal pathogens Porphyromonas gingivalis and Fusobacterium nucleatum promote tumor progression in an oralâ specific chemical carcinogenesis model. Oncotarget, 6, 22613 â 22623.
dc.identifier.citedreferenceBochenek, G., Hasler, R., El Mokhtari, N. E., Konig, I. R., Loos, B. G., Jepsen, S., â ¦ Schaefer, A. S. ( 2013 ). The large nonâ coding RNA ANRIL, which is associated with atherosclerosis, periodontitis and several forms of cancer, regulates ADIPOR1, VAMP3 and C11ORF10. Human Molecular Genetics, 22, 4516 â 4527. https://doi.org/10.1093/hmg/ddt299
dc.identifier.citedreferenceBoultwood, J., Fidler, C., Strickson, A. J., Watkins, F., Kostrzewa, M., Jaju, R. J., â ¦ Wainscoat, J. S. ( 2000 ). Transcription mapping of the 5qâ syndrome critical region: Cloning of two novel genes and sequencing, expression, and mapping of a further six novel cDNAs. Genomics, 66, 26 â 34. https://doi.org/10.1006/geno.2000.6193
dc.identifier.citedreferenceFine, D. H., Markowitz, K., Furgang, D., Fairlie, K., Ferrandiz, J., Nasri, C., â ¦ Gunsolley, J. ( 2009 ). Macrophage inflammatory proteinâ 1alpha: A salivary biomarker of bone loss in a longitudinal cohort study of children at risk for aggressive periodontal disease? Journal of Periodontology, 80, 106 â 113.
dc.identifier.citedreferenceGhaderi, H., Kiany, F., Razmkhah, M., Dadras, S., Chenari, N., Hosseini, A., â ¦ Ghaderi, A. ( 2014 ). mRNA expression of pattern recognition receptors and their signaling mediators in healthy and diseased gingival tissues. Journal of Indian Society of Periodontology, 18, 150 â 154. https://doi.org/10.4103/0972-124X.131309
dc.identifier.citedreferenceGhallab, N. A. ( 2017 ). Diagnostic potential and future directions of biomarkers in gingival crevicular fluid and saliva of periodontal diseases: Review of the current evidence. Archives of Oral Biology, 87, 115 â 124.
dc.identifier.citedreferenceGiannobile, W. V. ( 2012 ). Salivary diagnostics for periodontal diseases. Journal of the American Dental Association, 143, 6S â 11S. https://doi.org/10.14219/jada.archive.2012.0341
dc.identifier.citedreferenceGiannobile, W. V., Beikler, T., Kinney, J. S., Ramseier, C. A., Morelli, T., & Wong, D. T. ( 2009 ). Saliva as a diagnostic tool for periodontal disease: Current state and future directions. Periodontology 2000, 50, 52 â 64. https://doi.org/10.1111/j.1600-0757.2008.00288.x
dc.identifier.citedreferenceGibbs, S., Fijneman, R., Wiegant, J., Van Kessel, A. G., Van De Putte, P., & Backendorf, C. ( 1993 ). Molecular characterization and evolution of the SPRR family of keratinocyte differentiation markers encoding small prolineâ rich proteins. Genomics, 16, 630 â 637. https://doi.org/10.1006/geno.1993.1240
dc.identifier.citedreferenceGomes, M. A., Rodrigues, F. H., Afonsoâ Cardoso, S. R., Buso, A. M., Silva, A. G., Favoreto, Jr, S., & Souza, M. A. ( 2006 ). Levels of immunoglobulin A1 and messenger RNA for interferon gamma and tumor necrosis factor alpha in total saliva from patients with diabetes mellitus type 2 with chronic periodontal disease. Journal of Periodontal Research, 41, 177 â 183. https://doi.org/10.1111/j.1600-0765.2005.00851.x
dc.identifier.citedreferenceGrau, A. J., Becher, H., Ziegler, C. M., Lichy, C., Buggle, F., Kaiser, C., â ¦ Dorfer, C. E. ( 2004 ). Periodontal disease as a risk factor for ischemic stroke. Stroke, 35, 496 â 501. https://doi.org/10.1161/01.STR.0000110789.20526.9D
dc.identifier.citedreferenceHenskens, Y. M., Van Der Velden, U., Veerman, E. C., & Nieuw Amerongen, A. V. ( 1993 ). Protein, albumin and cystatin concentrations in saliva of healthy subjects and of patients with gingivitis or periodontitis. Journal of Periodontal Research, 28, 43 â 48. https://doi.org/10.1111/j.1600-0765.1993.tb01049.x
dc.identifier.citedreferenceHenson, B. S., & Wong, D. T. ( 2010 ). Collection, storage, and processing of saliva samples for downstream molecular applications. Methods in Molecular Biology, 666, 21 â 30. https://doi.org/10.1007/978-1-60761-820-1
dc.owningcollnameInterdisciplinary and Peer-Reviewed


Files in this item

Show simple item record

Remediation of Harmful Language

The University of Michigan Library aims to describe library materials in a way that respects the people and communities who create, use, and are represented in our collections. Report harmful or offensive language in catalog records, finding aids, or elsewhere in our collections anonymously through our metadata feedback form. More information at Remediation of Harmful Language.

Accessibility

If you are unable to use this file in its current format, please select the Contact Us link and we can modify it to make it more accessible to you.