{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,6,25]],"date-time":"2026-06-25T14:29:35Z","timestamp":1782397775471,"version":"3.54.5"},"reference-count":34,"publisher":"Springer Science and Business Media LLC","issue":"10","license":[{"start":{"date-parts":[[2021,6,30]],"date-time":"2021-06-30T00:00:00Z","timestamp":1625011200000},"content-version":"tdm","delay-in-days":0,"URL":"https:\/\/www.springer.com\/tdm"},{"start":{"date-parts":[[2021,6,30]],"date-time":"2021-06-30T00:00:00Z","timestamp":1625011200000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/www.springer.com\/tdm"}],"content-domain":{"domain":["link.springer.com"],"crossmark-restriction":false},"short-container-title":["Int Urol Nephrol"],"published-print":{"date-parts":[[2021,10]]},"DOI":"10.1007\/s11255-021-02921-8","type":"journal-article","created":{"date-parts":[[2021,6,30]],"date-time":"2021-06-30T05:05:25Z","timestamp":1625029525000},"page":"1977-1985","update-policy":"https:\/\/doi.org\/10.1007\/springer_crossmark_policy","source":"Crossref","is-referenced-by-count":11,"title":["Diagnosis of advanced prostate cancer at the community level in Rwanda"],"prefix":"10.1007","volume":"53","author":[{"ORCID":"https:\/\/orcid.org\/0000-0002-3359-3338","authenticated-orcid":false,"given":"Innocent","family":"Nzeyimana","sequence":"first","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Alexandre","family":"Nyirimodoka","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Edouard","family":"Ngendahayo","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Alex","family":"Bonane","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Emmanuel","family":"Muhawenimana","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Florence","family":"Umurangwa","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Africa","family":"Gasana","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Alphonse Marie","family":"Sibomana","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Seth","family":"Teplitsky","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Christophe","family":"Rusatira","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Jennifer","family":"Rickard","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Theobald","family":"Hategekimana","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Emile","family":"Rwamasirabo","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"297","published-online":{"date-parts":[[2021,6,30]]},"reference":[{"issue":"1","key":"2921_CR1","doi-asserted-by":"publisher","first-page":"1","DOI":"10.11648\/j.ijcems.20160201.11","volume":"2","author":"S Banerjee","year":"2016","unstructured":"Banerjee S (2016) Worldwide prostate cancer epidemiology: differences between regions, races, and awareness programs. Int J Clin Exp Med Sci. 2(1):1. https:\/\/doi.org\/10.11648\/j.ijcems.20160201.11","journal-title":"Int J Clin Exp Med Sci."},{"key":"2921_CR2","doi-asserted-by":"crossref","unstructured":"Parkin D, Bray F, Devesa S (2001) Cancer burden in the year 2000. The global picture. Eur J Cancer. 37:4\u201366. Available from: http:\/\/linkinghub.elsevier.com\/retrieve\/pii\/S0959804901002672","DOI":"10.1016\/S0959-8049(01)00267-2"},{"issue":"2","key":"2921_CR3","doi-asserted-by":"publisher","first-page":"162","DOI":"10.1046\/j.1464-410X.2002.2822.x","volume":"90","author":"M Quinn","year":"2002","unstructured":"Quinn M, Babb P (2002) Patterns and trends in prostate cancer incidence, survival, prevalence and mortality. Part I: international comparisons. BJU Int 90(2):162\u2013173","journal-title":"BJU Int"},{"issue":"SUPPL. 8","key":"2921_CR4","doi-asserted-by":"publisher","first-page":"15","DOI":"10.1093\/annonc\/mdl983","volume":"17","author":"P Kanavos","year":"2006","unstructured":"Kanavos P (2006) The rising burden of cancer in the developing world. Ann Oncol 17(SUPPL. 8):15\u201323","journal-title":"Ann Oncol"},{"key":"2921_CR5","doi-asserted-by":"publisher","unstructured":"Narod S (1999) Genetic epidemiology of prostate cancer. Biochimica et Biophysica Acta. 1423(1):F1\u201313. https:\/\/doi.org\/10.1016\/s0304-419x(98)00030-4","DOI":"10.1016\/s0304-419x(98)00030-4"},{"issue":"4","key":"2921_CR6","doi-asserted-by":"publisher","first-page":"e0153496","DOI":"10.1371\/journal.pone.0153496","volume":"11","author":"D Adeloye","year":"2016","unstructured":"Adeloye D, David RA, Aderemi AV, Iseolorunkanmi A, Oyedokun A, Iweala EEJ et al (2016) An estimate of the incidence of prostate cancer in africa: a systematic review and meta-analysis. Shore N, editor. PLoS ONE 11(4):e0153496. https:\/\/doi.org\/10.1371\/journal.pone.0153496","journal-title":"PLoS ONE"},{"issue":"5","key":"2921_CR7","doi-asserted-by":"publisher","first-page":"E359","DOI":"10.1002\/ijc.29210","volume":"136","author":"J Ferlay","year":"2015","unstructured":"Ferlay J, Soerjomataram I, Dikshit R, Eser S, Mathers C, Rebelo M et al (2015) Cancer incidence and mortality worldwide: sources, methods and major patterns in GLOBOCAN 2012. Int J Cancer 136(5):E359\u2013E386","journal-title":"Int J Cancer"},{"issue":"4","key":"2921_CR8","doi-asserted-by":"publisher","first-page":"267","DOI":"10.7196\/SAMJ.4420","volume":"101","author":"C Heyns","year":"2011","unstructured":"Heyns C, Fisher M, Lecuona A, van der Merwe A (2011) Prostate cancer among different racial groups in the western cape: presenting features and management. South African Med J 101(4):267\u2013270","journal-title":"South African Med J"},{"key":"2921_CR9","doi-asserted-by":"crossref","unstructured":"Lee RT (2018) Prostate cancer. Integr Med. 790\u2013799.e2. Available from: http:\/\/linkinghub.elsevier.com\/retrieve\/pii\/B9780323358682000803","DOI":"10.1016\/B978-0-323-35868-2.00080-3"},{"key":"2921_CR10","doi-asserted-by":"publisher","DOI":"10.1016\/j.eururo.2018.06.018","author":"A Nabid","year":"2018","unstructured":"Nabid A, Carrier N, Martin A-G, Bahary J-P, Lemaire C, Vass S et al (2018) Duration of androgen deprivation therapy in high-risk prostate cancer: a randomized phase III trial. Eur Urol. https:\/\/doi.org\/10.1016\/j.eururo.2018.06.018","journal-title":"Eur Urol"},{"issue":"2","key":"2921_CR11","doi-asserted-by":"publisher","first-page":"89","DOI":"10.1177\/1875974212465549","volume":"6","author":"R Rajasundaram","year":"2013","unstructured":"Rajasundaram R, Gunendran T, George N (2013) Surgical castration for androgen-deprivation therapy of prostate cancer\u2014relevance in current practice. J Clin Urol 6(2):89\u201393","journal-title":"J Clin Urol"},{"key":"2921_CR12","doi-asserted-by":"crossref","unstructured":"McMurtry CT, McMurtry JM (2003) Metastatic prostate cancer: complications and treatment. J Am Geriatr Soc. 51(8):1136\u201342. Available from: http:\/\/www.ncbi.nlm.nih.gov\/pubmed\/12890079","DOI":"10.1046\/j.1532-5415.2003.51367.x"},{"key":"2921_CR13","doi-asserted-by":"crossref","unstructured":"Smith JA, Soloway MS, Young MJ (1999) Complications of advanced prostate cancer. Urology. 54(6A Suppl):8\u201314. Available from: http:\/\/www.ncbi.nlm.nih.gov\/pubmed\/10606278","DOI":"10.1016\/S0090-4295(99)00448-3"},{"key":"2921_CR14","unstructured":"Common bone complications in advanced prostate cancer patients lead to increased medical costs\u2014NewYork-Presbyterian (2019). Available from: https:\/\/www.nyp.org\/news\/Common-Bone-Complications-in-Advanced-Prostate-Cancer-Patients"},{"key":"2921_CR15","doi-asserted-by":"crossref","unstructured":"Luz MA, Aprikian AG (2010) Preventing bone complications in advanced prostate cancer. Curr Oncol. 17 Suppl 2(Suppl 2):S65\u201371. Available from: http:\/\/www.ncbi.nlm.nih.gov\/pubmed\/20882136","DOI":"10.3747\/co.v17i0.722"},{"issue":"2","key":"2921_CR16","doi-asserted-by":"publisher","first-page":"244","DOI":"10.1097\/PAS.0000000000000530","volume":"40","author":"JI Epstein","year":"2016","unstructured":"Epstein JI, Egevad L, Amin MB, Delahunt B, Srigley JR, Humphrey PA (2016) The 2014 international society of urological pathology (ISUP) consensus conference on gleason grading of prostatic carcinoma definition of grading patterns and proposal for a new grading system. Am J Surg Pathol 40(2):244\u2013252","journal-title":"Am J Surg Pathol"},{"issue":"11","key":"2921_CR17","doi-asserted-by":"publisher","first-page":"981","DOI":"10.1056\/NEJMoa1113135","volume":"366","author":"FH Schr\u00f6der","year":"2012","unstructured":"Schr\u00f6der FH, Hugosson J, Roobol MJ, Tammela TLJ, Ciatto S, Nelen V et al (2012) Prostate-cancer mortality at 11 years of follow-up. N Engl J Med 366(11):981\u2013990. https:\/\/doi.org\/10.1056\/NEJMoa1113135","journal-title":"N Engl J Med"},{"key":"2921_CR18","unstructured":"Akinremi T, Adeniyi A, Olutunde A, Oduniyi A, Ogo C (2014) Need for and relevance of prostate cancer screening in Nigeria. Ecancermedicalscience. 8:457. Available from: http:\/\/www.ncbi.nlm.nih.gov\/pubmed\/25228913"},{"key":"2921_CR19","doi-asserted-by":"publisher","first-page":"1","DOI":"10.1186\/s12875-017-0677-2","volume":"19","author":"D Jones","year":"2018","unstructured":"Jones D, Friend C, Dreher A, Allgar V, Macleod U (2018) The diagnostic test accuracy of rectal examination for prostate cancer diagnosis in symptomatic patients: a systematic review. BMC Fam Pract 19:1\u20136","journal-title":"BMC Fam Pract"},{"key":"2921_CR20","unstructured":"Ojewola RW, Tijani KH, Jeje EA, Ogunjimi MA, Anunobi CC, Adesanya AO (2013) An evaluation of usefulness of prostate specific antigen and digital rectal examination in the diagnosis of prostate cancer in an unscreened population:experience in a Nigerian teaching hospital. West Afr J Med 32(1):8\u201313. Available from: http:\/\/www.ncbi.nlm.nih.gov\/pubmed\/23613288"},{"key":"2921_CR21","unstructured":"Khalid KE, Brair AI, Elhaj AM, Ali KE (2011) Prostate-specific antigen level and risk of bone metastasis in Sudanese patients with prostate cancer. Saudi J Kidney Dis Transpl 22(5):1041\u20133. Available from: http:\/\/www.ncbi.nlm.nih.gov\/pubmed\/21912047"},{"key":"2921_CR22","doi-asserted-by":"crossref","unstructured":"Kamaleshwaran KK, Mittal BR, Harisankar CNB, Bhattacharya A, Singh SK, Mandal AK (2012) Predictive value of serum prostate specific antigen in detecting bone metastasis in prostate cancer patients using bone scintigraphy. Indian J Nucl Med 27(2):81\u20134. Available from: http:\/\/www.ncbi.nlm.nih.gov\/pubmed\/23723577","DOI":"10.4103\/0972-3919.110683"},{"issue":"4","key":"2921_CR23","doi-asserted-by":"publisher","first-page":"1011","DOI":"10.1016\/S0022-5347(17)38972-3","volume":"142","author":"MLA Hudson","year":"1989","unstructured":"Hudson MLA, Bahnson RR, Catalona WJ (1989) With prostate cancer. J Urol 142(4):1011\u20131017. https:\/\/doi.org\/10.1016\/S0022-5347(17)38972-3","journal-title":"J Urol"},{"issue":"1","key":"2921_CR24","first-page":"4","volume":"15","author":"D Ojuka","year":"2018","unstructured":"Ojuka D, Majicha S, Ngugi P (2018) Can PSA predict bone metastasis amongst newly diagnosed prostate cancer patients\u202f? Ann African Surg 15(1):4\u20137","journal-title":"Ann African Surg"},{"key":"2921_CR25","unstructured":"Zaman MU, Fatima N, Sajjad Z (2011) Metastasis on bone scan with low prostate specific antigen (\u226420 ng\/ml) and Gleason\u2019s score. Asian Pac J Cancer Prev 12(6):1529\u201332. Available from: http:\/\/www.ncbi.nlm.nih.gov\/pubmed\/22126493"},{"key":"2921_CR26","doi-asserted-by":"crossref","unstructured":"Ishizuka O, Tanabe T, Nakayama T, Kawakami M, Kinebuchi Y, Nishizawa O (2005) Prostate-specific antigen, Gleason sum and clinical T stage for predicting the need for radionuclide bone scan for prostate cancer patients in Japan. Int J Urol 12(8):728\u201332. Available from: http:\/\/www.ncbi.nlm.nih.gov\/pubmed\/16174046","DOI":"10.1111\/j.1442-2042.2005.01118.x"},{"key":"2921_CR27","doi-asserted-by":"publisher","DOI":"10.4111\/kju.2012.53.2.82","author":"J Jang","year":"2012","unstructured":"Jang J, Kim Y (2012) Is prostate biopsy essential to diagnose prostate cancer in the older patient with extremely high prostate-specific antigen? Korean J Urol. https:\/\/doi.org\/10.4111\/kju.2012.53.2.82","journal-title":"Korean J Urol"},{"key":"2921_CR28","doi-asserted-by":"crossref","unstructured":"Chen Y, Lin Y, Nie P, Jiang W, Liu Y, Yuan R, et al (2017) Associations of Prostate-Specific Antigen, Prostate Carcinoma Tissue Gleason Score, and Androgen Receptor Expression with Bone Metastasis in Patients with Prostate Carcinoma. Med Sci Monit 23:1768\u201374. Available from: http:\/\/www.ncbi.nlm.nih.gov\/pubmed\/28400549","DOI":"10.12659\/MSM.900977"},{"key":"2921_CR29","unstructured":"Heyns CF, Naude AM, Ahmed G, Stopforth HB, Stellmacher GA, Visser AJ (2001) Serum prostate-specific antigen as surrogate for the histological diagnosis of prostate cancer. South African Med J 91(8):685\u20139. Available from: https:\/\/www.ajol.info\/index.php\/samj\/article\/view\/140044"},{"issue":"5","key":"2921_CR30","doi-asserted-by":"publisher","first-page":"1283","DOI":"10.1016\/S0022-5347(17)35233-3","volume":"151","author":"WJ Catalona","year":"1994","unstructured":"Catalona WJ, Richie JP, Ahmann FR, Hudson MLA, Scardino PT, Flanigan RC et al (1994) Comparison of digital rectal examination and serum prostate specific antigen in the early detection of prostate cancer\u202f: results of a multicenter clinical trial of 6, 630 men. J Urol 151(5):1283\u20131290. https:\/\/doi.org\/10.1016\/S0022-5347(17)35233-3","journal-title":"J Urol"},{"key":"2921_CR31","doi-asserted-by":"crossref","unstructured":"Malati T, Kumari GR, Murthy PVLN, Reddy CR, Prakash BS (2006) Prostate specific antigen in patients of benign prostate hypertrophy and carcinoma prostate. Indian J Clin Biochem 21. Available from: http:\/\/medind.nic.in\/iaf\/t06\/i1\/iaft06i1p34.pdf","DOI":"10.1007\/BF02913064"},{"key":"2921_CR32","doi-asserted-by":"crossref","unstructured":"Amayo A, Obara W (2004) Serum prostate specific antigen levels in men with benign prostatic hyperplasia and cancer of prostate. East Afr Med J 81(1):22\u20136. Available from: http:\/\/www.ncbi.nlm.nih.gov\/pubmed\/15080511","DOI":"10.4314\/eamj.v81i1.8790"},{"key":"2921_CR33","doi-asserted-by":"crossref","unstructured":"Stamey TA, Yang N, Hay AR, McNeal JE, Freiha FS, Redwine E (1987) Prostate-specific antigen as a serum marker for adenocarcinoma of the prostate. N Engl J Med 317(15):909\u201316. Available from: http:\/\/www.ncbi.nlm.nih.gov\/pubmed\/2442609","DOI":"10.1056\/NEJM198710083171501"},{"key":"2921_CR34","first-page":"114","volume":"5","author":"D Iya","year":"2011","unstructured":"Iya D, Chanchani S, Belmonte J, Morris D, Glew R, Van der Jagt D (2011) Prostate specific antigen in Africans: a study in Nigerian men. Nigerian Journal of Surgical Research 5(3):114\u2013119","journal-title":"Nigerian Journal of Surgical Research"}],"container-title":["International Urology and Nephrology"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/link.springer.com\/content\/pdf\/10.1007\/s11255-021-02921-8.pdf","content-type":"application\/pdf","content-version":"vor","intended-application":"text-mining"},{"URL":"https:\/\/link.springer.com\/article\/10.1007\/s11255-021-02921-8\/fulltext.html","content-type":"text\/html","content-version":"vor","intended-application":"text-mining"},{"URL":"https:\/\/link.springer.com\/content\/pdf\/10.1007\/s11255-021-02921-8.pdf","content-type":"application\/pdf","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2021,9,24]],"date-time":"2021-09-24T21:19:11Z","timestamp":1632518351000},"score":1,"resource":{"primary":{"URL":"https:\/\/link.springer.com\/10.1007\/s11255-021-02921-8"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2021,6,30]]},"references-count":34,"journal-issue":{"issue":"10","published-print":{"date-parts":[[2021,10]]}},"alternative-id":["2921"],"URL":"https:\/\/doi.org\/10.1007\/s11255-021-02921-8","relation":{},"ISSN":["0301-1623","1573-2584"],"issn-type":[{"value":"0301-1623","type":"print"},{"value":"1573-2584","type":"electronic"}],"subject":[],"published":{"date-parts":[[2021,6,30]]},"assertion":[{"value":"22 May 2021","order":1,"name":"received","label":"Received","group":{"name":"ArticleHistory","label":"Article History"}},{"value":"6 June 2021","order":2,"name":"accepted","label":"Accepted","group":{"name":"ArticleHistory","label":"Article History"}},{"value":"30 June 2021","order":3,"name":"first_online","label":"First Online","group":{"name":"ArticleHistory","label":"Article History"}},{"order":1,"name":"Ethics","group":{"name":"EthicsHeading","label":"Declarations"}},{"value":"The authors declare that they have no competing interest.","order":2,"name":"Ethics","group":{"name":"EthicsHeading","label":"Conflict of interest"}},{"value":"Ethical approval was obtained from the Internal Review Board of the University of Rwanda\/College of Medicine and Health sciences and the Ethic committees of each referral hospital where the study was conducted. Reference numbers: UR\/CMHS IRB: 246\/CMHS_IRB\/2018. RMH: RMH\/IRB\/019\/2018. CHUK: Not available. KFH: Not available (no reference number was put on the approval).","order":3,"name":"Ethics","group":{"name":"EthicsHeading","label":"Ethical approval"}},{"value":"All participants received verbal and written information and signed consents to participate.","order":4,"name":"Ethics","group":{"name":"EthicsHeading","label":"Consent to participate"}},{"value":"Not applicable.","order":5,"name":"Ethics","group":{"name":"EthicsHeading","label":"Consent for publication"}}]}}