{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2025,10,12]],"date-time":"2025-10-12T03:23:17Z","timestamp":1760239397982,"version":"build-2065373602"},"reference-count":48,"publisher":"MDPI AG","issue":"11","license":[{"start":{"date-parts":[[2020,11,9]],"date-time":"2020-11-09T00:00:00Z","timestamp":1604880000000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":["JCM"],"abstract":"<jats:p>To compare the expression of the receptor activator of nuclear factor-kappa B (RANK), matrix metalloproteinase 9 (MMP-9) and parathyroid hormone-related protein (PTHrP) in primary chronic apical periodontitis lesions (CAPLs) between people living with HIV (PLWHIV) undergoing antiretroviral therapy (ART) and HIV- individuals, 32 CAPLs (16 lesions from each group) were submitted to histopathological and immunohistochemical analyses and compared between groups. The majority of the PLWHIV group had undetectable plasma viral loads (n = 13; 81.3%). The means of TCD4+ lymphocytes, exposure to HIV-1 and the time of the use of ART were 542.1 cells\/mm3 (SD = 256.4), 6.3 years (SD = 2.9) and 5.0 years (SD = 2.5), respectively. Of all variables studied, only histopathological diagnosis showed a significant difference between groups (LWHIV: granuloma n = 11 (68.0%); cyst n = 5 (31.2%); HIV-: granuloma n = 15 (93.8%); cyst n = 1 (6.2%); p = 0.015). When comparing the expressions of the three inflammatory markers between the groups, no significant differences were seen. There was no difference in the expression of RANK, PTHrP and MMP-9 in primary chronic apical periodontitis lesions between PLWHIV under ART and HIV- individuals.<\/jats:p>","DOI":"10.3390\/jcm9113611","type":"journal-article","created":{"date-parts":[[2020,11,9]],"date-time":"2020-11-09T19:08:29Z","timestamp":1604948909000},"page":"3611","update-policy":"https:\/\/doi.org\/10.3390\/mdpi_crossmark_policy","source":"Crossref","is-referenced-by-count":5,"title":["Expression of Inflammatory Markers RANK, MMP-9 and PTHrP in Chronic Apical Periodontitis from People Living with HIV Undergoing Antiretroviral Therapy"],"prefix":"10.3390","volume":"9","author":[{"given":"Marcio Francisco","family":"Pereira","sequence":"first","affiliation":[{"name":"Postgraduation Program in Dentistry, Est\u00e1cio de S\u00e1 University, Rio de Janeiro 22790-710, Brazil"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"ORCID":"https:\/\/orcid.org\/0000-0003-0317-8878","authenticated-orcid":false,"given":"Fabio Ramoa","family":"Pires","sequence":"additional","affiliation":[{"name":"Postgraduation Program in Dentistry, Est\u00e1cio de S\u00e1 University, Rio de Janeiro 22790-710, Brazil"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Luciana","family":"Armada","sequence":"additional","affiliation":[{"name":"Postgraduation Program in Dentistry, Est\u00e1cio de S\u00e1 University, Rio de Janeiro 22790-710, Brazil"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Dennis Carvalho","family":"Ferreira","sequence":"additional","affiliation":[{"name":"Postgraduation Program in Dentistry, Est\u00e1cio de S\u00e1 University, Rio de Janeiro 22790-710, Brazil"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-6823-1636","authenticated-orcid":false,"given":"Florence","family":"Carrouel","sequence":"additional","affiliation":[{"name":"Laboratory \u201cHealth Systemic Process\u201d, University Lyon 1, EA4129, 69008 Lyon, France"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"ORCID":"https:\/\/orcid.org\/0000-0003-4754-2512","authenticated-orcid":false,"given":"Denis","family":"Bourgeois","sequence":"additional","affiliation":[{"name":"Laboratory \u201cHealth Systemic Process\u201d, University Lyon 1, EA4129, 69008 Lyon, France"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-4388-6310","authenticated-orcid":false,"given":"Lucio Souza","family":"Gon\u00e7alves","sequence":"additional","affiliation":[{"name":"Postgraduation Program in Dentistry, Est\u00e1cio de S\u00e1 University, Rio de Janeiro 22790-710, Brazil"}],"role":[{"role":"author","vocabulary":"crossref"}]}],"member":"1968","published-online":{"date-parts":[[2020,11,9]]},"reference":[{"key":"ref_1","first-page":"51","article-title":"Prevalence of HIV-related oral manifestations and their association with HAART and CD4+ T cell count: A review","volume":"32","author":"Ottria","year":"2018","journal-title":"J. Biol. Regul. Homeost. Agents"},{"key":"ref_2","doi-asserted-by":"crossref","first-page":"223","DOI":"10.1111\/odi.12220","article-title":"Progress in understanding oral health and HIV\/AIDS","volume":"20","author":"Patton","year":"2014","journal-title":"Oral Dis."},{"key":"ref_3","doi-asserted-by":"crossref","first-page":"388","DOI":"10.5125\/jkaoms.2017.43.6.388","article-title":"Oral lesions associated with human immunodeficiency virus in 75 adult patients: A clinical study","volume":"43","author":"Berberi","year":"2017","journal-title":"J. Korean Assoc. Oral Maxillofac. Surg."},{"key":"ref_4","first-page":"S208","article-title":"Less common oral lesions associated with HIV infection: Prevalence and classification","volume":"3","year":"1997","journal-title":"Oral Dis."},{"key":"ref_5","doi-asserted-by":"crossref","first-page":"1170","DOI":"10.1016\/j.joen.2012.05.023","article-title":"Prevalence of periapical radiolucency and root canal treatment: A systematic review of cross-sectional studies","volume":"38","author":"Pak","year":"2012","journal-title":"J. Endod."},{"key":"ref_6","unstructured":"Lopes, H.P., and Siqueira, J.F. (2010). Endodontia\u2014Biologia e T\u00e9cnica, Saraiva. [3rd ed.]."},{"key":"ref_7","doi-asserted-by":"crossref","first-page":"655","DOI":"10.3389\/fmicb.2019.00655","article-title":"Diverse Large HIV-1 Non-subtype B Clusters Are Spreading Among Men Who Have Sex With Men in Spain","volume":"10","author":"Delgado","year":"2019","journal-title":"Front. Microbiol."},{"key":"ref_8","doi-asserted-by":"crossref","first-page":"1205","DOI":"10.1016\/j.joen.2013.06.014","article-title":"Can apical periodontitis modify systemic levels of inflammatory markers? A systematic review and meta-analysis","volume":"39","author":"Gomes","year":"2013","journal-title":"J. Endod."},{"key":"ref_9","doi-asserted-by":"crossref","first-page":"17","DOI":"10.22456\/2177-0018.7869","article-title":"Les\u00e3o periapical em paciente aid\u00e9tico: Revis\u00e3o da literatura e apresenta\u00e7\u00e3o de caso cl\u00ednico cir\u00fargico","volume":"36","author":"Bercini","year":"1995","journal-title":"Rev. Fac. Odontol. Porto Alegre"},{"key":"ref_10","doi-asserted-by":"crossref","first-page":"e12351","DOI":"10.1111\/jicd.12351","article-title":"Systematic review of the changing pattern of the oral manifestations of HIV","volume":"9","author":"Tappuni","year":"2018","journal-title":"J. Investig. Clin. Dent."},{"key":"ref_11","doi-asserted-by":"crossref","first-page":"20","DOI":"10.1111\/j.1600-9657.1986.tb00119.x","article-title":"The periapical index: A scoring system for radiographic assessment of apical periodontitis","volume":"2","author":"Kerekes","year":"1986","journal-title":"Dent. Traumatol."},{"key":"ref_12","doi-asserted-by":"crossref","first-page":"2374","DOI":"10.3389\/fmicb.2018.02374","article-title":"Root Microbiota in Primary and Secondary Apical Periodontitis","volume":"9","author":"Bouillaguet","year":"2018","journal-title":"Front. Microbiol."},{"key":"ref_13","unstructured":"Sundqvist, G. (1976). Bacteriological Studies of Necrotic Dental Pulps, University of Umea."},{"key":"ref_14","doi-asserted-by":"crossref","first-page":"1400","DOI":"10.1016\/j.joen.2014.03.024","article-title":"Immunoexpression of interleukin 17 in apical periodontitis lesions","volume":"40","author":"Ajuz","year":"2014","journal-title":"J. Endod."},{"key":"ref_15","doi-asserted-by":"crossref","first-page":"1281","DOI":"10.1016\/j.joen.2015.03.025","article-title":"Expression and Distribution of Receptor Activator of Nuclear Factor Kappa B, Receptor Activator of Nuclear Factor Kappa B Ligand, and Osteoprotegerin in Periradicular Cysts","volume":"41","author":"Armada","year":"2015","journal-title":"J. Endod."},{"key":"ref_16","doi-asserted-by":"crossref","first-page":"63","DOI":"10.1016\/j.joen.2013.09.037","article-title":"Distribution of mast cells and macrophages and expression of interleukin-6 in periapical cysts","volume":"40","author":"Bracks","year":"2014","journal-title":"J. Endod."},{"key":"ref_17","unstructured":"Lenhard, W., and Lenhard, A. (2017). Computation of Effect Sizes, Psychometrica."},{"key":"ref_18","doi-asserted-by":"crossref","first-page":"3247","DOI":"10.4103\/jfmpc.jfmpc_767_19","article-title":"Correlation of CD4 counts with oral and systemic manifestations in HIV patients","volume":"8","author":"Vohra","year":"2019","journal-title":"J. Fam. Med. Prim. Care"},{"key":"ref_19","doi-asserted-by":"crossref","first-page":"984","DOI":"10.1080\/09540121.2019.1622631","article-title":"Antiretroviral-na\u00efve HIV-infected patients had lower bone formation markers than HIV-uninfected adults","volume":"32","author":"Wattanachanya","year":"2020","journal-title":"AIDS Care"},{"key":"ref_20","doi-asserted-by":"crossref","unstructured":"Desta, A.A., Wubayehu Woldearegay, T., Berhe, A.A., Futwi, N., Gebremedhn Gebru, G., and Godefay, H. (2019). Immunological recovery, failure and factors associated with CD-4 T-cells progression over time, among adolescents and adults living with HIV on Antiretroviral Therapy in Northern Ethiopia: A retrospective cross sectional study. PLoS ONE, 14.","DOI":"10.1371\/journal.pone.0226293"},{"key":"ref_21","doi-asserted-by":"crossref","first-page":"514","DOI":"10.1016\/j.joen.2016.11.008","article-title":"Association between Systemic Diseases and Endodontic Outcome: A Systematic Review","volume":"43","author":"Aminoshariae","year":"2017","journal-title":"J. Endod."},{"key":"ref_22","doi-asserted-by":"crossref","unstructured":"Minniear, T.D., Girde, S., Angira, F., Mills, L.A., Zeh, C., Peters, P.J., Masaba, R., Lando, R., Thomas, T.K., and Taylor, A.W. (2014). Outcomes in a cohort of women who discontinued maternal triple-antiretroviral regimens initially used to prevent mother-to-child transmission during pregnancy and breastfeeding\u2014Kenya, 2003\u20132009. PLoS ONE, 9.","DOI":"10.1371\/journal.pone.0093556"},{"key":"ref_23","first-page":"322","article-title":"A comparison of endodontic treatment outcomes between HIV-positive and HIV-negative patients","volume":"67","author":"Tootla","year":"2012","journal-title":"SADJ"},{"key":"ref_24","first-page":"155","article-title":"Comparison of the success of root canal therapy in HIV\/AIDS patients and non-infected controls","volume":"56","author":"Alley","year":"2008","journal-title":"Gen. Dent."},{"key":"ref_25","doi-asserted-by":"crossref","first-page":"633","DOI":"10.1097\/01.don.0000157985.88883.81","article-title":"The effect of human immunodeficiency virus on endodontic treatment outcome","volume":"31","author":"Quesnell","year":"2005","journal-title":"J. Endod."},{"key":"ref_26","doi-asserted-by":"crossref","first-page":"921","DOI":"10.1016\/j.joen.2016.03.008","article-title":"Cellular Profile and Expression of Immunologic Markers in Chronic Apical Periodontitis from HIV-infected Patients Undergoing Highly Active Antiretroviral Therapy","volume":"42","author":"Gama","year":"2016","journal-title":"J. Endod."},{"key":"ref_27","doi-asserted-by":"crossref","first-page":"627","DOI":"10.6061\/clinics\/2014(09)09","article-title":"Periradicular lesions in HIV-infected patients attending the faculty of dentistry: Clinical findings, socio-demographics status, habits and laboratory data-seeking an association","volume":"69","author":"Fontes","year":"2014","journal-title":"Clinics"},{"key":"ref_28","doi-asserted-by":"crossref","first-page":"558","DOI":"10.1111\/j.1601-0825.2012.01908.x","article-title":"Microbiologic profile of endodontic infections from HIV- and HIV+ patients using multiple-displacement amplification and checkerboard DNA-DNA hybridization","volume":"18","author":"Brito","year":"2012","journal-title":"Oral Dis."},{"key":"ref_29","doi-asserted-by":"crossref","first-page":"533","DOI":"10.1111\/iej.12345","article-title":"Immunological profile of periapical endodontic infections from HIV- and HIV+ patients","volume":"48","author":"Teles","year":"2015","journal-title":"Int. Endod. J."},{"key":"ref_30","doi-asserted-by":"crossref","unstructured":"Wong, S.K., Mohamad, N.-V., Giaze, T.R., Chin, K.-Y., Mohamed, N., and Ima-Nirwana, S. (2019). Prostate Cancer and Bone Metastases: The Underlying Mechanisms. Int. J. Mol. Sci., 20.","DOI":"10.3390\/ijms20102587"},{"key":"ref_31","doi-asserted-by":"crossref","first-page":"11900","DOI":"10.1002\/jcp.27857","article-title":"Parathyroid hormone-related peptide (1-34) promotes tooth eruption and inhibits osteogenesis of dental follicle cells during tooth development","volume":"234","author":"Zhang","year":"2019","journal-title":"J. Cell. Physiol."},{"key":"ref_32","doi-asserted-by":"crossref","first-page":"575","DOI":"10.1073\/pnas.1810200115","article-title":"Autocrine regulation of mesenchymal progenitor cell fates orchestrates tooth eruption","volume":"116","author":"Takahashi","year":"2019","journal-title":"Proc. Natl. Acad. Sci. USA"},{"key":"ref_33","doi-asserted-by":"crossref","first-page":"411","DOI":"10.1016\/S0092-8674(00)81169-1","article-title":"MMP-9\/gelatinase B is a key regulator of growth plate angiogenesis and apoptosis of hypertrophic chondrocytes","volume":"93","author":"Vu","year":"1998","journal-title":"Cell"},{"key":"ref_34","doi-asserted-by":"crossref","first-page":"1091","DOI":"10.1083\/jcb.124.6.1091","article-title":"High expression of 92-kD type IV collagenase (gelatinase B) in the osteoclast lineage during mouse development","volume":"124","author":"Reponen","year":"1994","journal-title":"J. Cell. Biol."},{"key":"ref_35","doi-asserted-by":"crossref","first-page":"555","DOI":"10.1111\/cea.13108","article-title":"Neutrophilia, gelatinase release and microvascular leakage induced by human mast cell tryptase in a mouse model: Lack of a role of protease-activated receptor 2 (PAR2)","volume":"48","author":"Khedr","year":"2018","journal-title":"Clin. Exp. Allergy"},{"key":"ref_36","doi-asserted-by":"crossref","first-page":"1082","DOI":"10.1016\/j.joen.2016.04.001","article-title":"Clinical Investigation of Matrix Metalloproteinases, Tissue Inhibitors of Matrix Metalloproteinases, and Matrix Metalloproteinase\/Tissue Inhibitors of Matrix Metalloproteinase Complexes and Their Networks in Apical Periodontitis","volume":"42","author":"Martinho","year":"2016","journal-title":"J. Endod."},{"key":"ref_37","doi-asserted-by":"crossref","first-page":"175","DOI":"10.1038\/36593","article-title":"A homologue of the TNF receptor and its ligand enhance T-cell growth and dendritic-cell function","volume":"390","author":"Anderson","year":"1997","journal-title":"Nature"},{"key":"ref_38","doi-asserted-by":"crossref","first-page":"17","DOI":"10.1016\/j.molmed.2005.11.007","article-title":"RANKL-RANK signaling in osteoclastogenesis and bone disease","volume":"12","author":"Wada","year":"2006","journal-title":"Trends Mol. Med."},{"key":"ref_39","doi-asserted-by":"crossref","first-page":"237","DOI":"10.1138\/20110512","article-title":"The many roles of RANKL-RANK signaling in bone, breast and cancer","volume":"8","author":"Schramek","year":"2011","journal-title":"IBMS BoneKEy"},{"key":"ref_40","doi-asserted-by":"crossref","unstructured":"Sigl, V., Jones, L.P., and Penninger, J.M. (2016). RANKL\/RANK: From bone loss to the prevention of breast cancer. Open Biol., 6.","DOI":"10.1098\/rsob.160230"},{"key":"ref_41","doi-asserted-by":"crossref","first-page":"243","DOI":"10.1007\/s001090100226","article-title":"Role of receptor activator of nuclear factor-kappaB ligand and osteoprotegerin in bone cell biology","volume":"79","author":"Hofbauer","year":"2001","journal-title":"J. Mol. Med."},{"key":"ref_42","doi-asserted-by":"crossref","first-page":"534","DOI":"10.1159\/000371845","article-title":"The RANKL-RANK Story","volume":"61","author":"Nagy","year":"2015","journal-title":"Gerontology"},{"key":"ref_43","doi-asserted-by":"crossref","first-page":"498","DOI":"10.1177\/10454411980090040701","article-title":"Periapical inflammatory responses and their modulation","volume":"9","author":"Stashenko","year":"1998","journal-title":"Crit. Rev. Oral Biol. Med."},{"key":"ref_44","doi-asserted-by":"crossref","unstructured":"Esemu, L.F., Yuosembom, E.K., Fang, R., Rasay, S., Fodjo, B.A.Y., Nguasong, J.T., Kidima, W., Ekali, G.L., Chen, J.J., and Ndhlovu, L. (2019). Impact of HIV-1 infection on the IGF-1 axis and angiogenic factors in pregnant Cameroonian women receiving antiretroviral therapy. PLoS ONE, 14.","DOI":"10.1371\/journal.pone.0215825"},{"key":"ref_45","doi-asserted-by":"crossref","first-page":"284","DOI":"10.1093\/infdis\/jiy509","article-title":"Biomarkers of Inflammation Correlate With Clinical Scoring Indices in Human Immunodeficiency Virus-Infected Kenyans","volume":"219","author":"Letizia","year":"2019","journal-title":"J. Infect. Dis."},{"key":"ref_46","doi-asserted-by":"crossref","first-page":"937","DOI":"10.1099\/jgv.0.001075","article-title":"HIV-induced matrix metalloproteinase-9 activation through mitogen-activated protein kinase signalling promotes HSV-1 cell-to-cell spread in oral epithelial cells","volume":"99","author":"Sufiawati","year":"2018","journal-title":"J. Gen. Virol."},{"key":"ref_47","doi-asserted-by":"crossref","first-page":"350","DOI":"10.1310\/hct1306-350","article-title":"Treatment of calcium and vitamin D deficiency in HIV-positive men on tenofovir-containing antiretroviral therapy","volume":"13","author":"Bech","year":"2012","journal-title":"HIV Clin. Trials"},{"key":"ref_48","doi-asserted-by":"crossref","first-page":"1200","DOI":"10.1016\/j.joen.2019.06.014","article-title":"Differences in Inflammation and Bone Resorption between Apical Granulomas, Radicular Cysts, and Dentigerous Cysts","volume":"45","author":"Weber","year":"2019","journal-title":"J. Endod."}],"container-title":["Journal of Clinical Medicine"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/www.mdpi.com\/2077-0383\/9\/11\/3611\/pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2025,10,11]],"date-time":"2025-10-11T10:31:16Z","timestamp":1760178676000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.mdpi.com\/2077-0383\/9\/11\/3611"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2020,11,9]]},"references-count":48,"journal-issue":{"issue":"11","published-online":{"date-parts":[[2020,11]]}},"alternative-id":["jcm9113611"],"URL":"https:\/\/doi.org\/10.3390\/jcm9113611","relation":{},"ISSN":["2077-0383"],"issn-type":[{"type":"electronic","value":"2077-0383"}],"subject":[],"published":{"date-parts":[[2020,11,9]]}}}