Association between obesity and frequency of high‑grade prostate cancer on biopsy in men: A single‑center retrospective study

Baio,Raffaele; Napodano,Giorgio; Caruana,Christian; Molisso,Giovanni; Di Mauro,Umberto; Intilla,Olivier; Pane,Umberto; D'Angelo,Costantino; Francavilla,Antonella Bianca; Guarnaccia,Claudio; Pentimalli,Francesca; Sanseverino,Roberto

doi:10.3892/mco.2022.2560

Association between obesity and frequency of high‑grade prostate cancer on biopsy in men: A single‑center retrospective study

Authors:
- Raffaele Baio
- Giorgio Napodano
- Christian Caruana
- Giovanni Molisso
- Umberto Di Mauro
- Olivier Intilla
- Umberto Pane
- Costantino D'Angelo
- Antonella Bianca Francavilla
- Claudio Guarnaccia
- Francesca Pentimalli
- Roberto Sanseverino
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Affiliations: Department of Medicine and Surgery ‘Scuola Medica Salernitana’, University of Salerno, Baronissi, I‑84081 Salerno, Italy, Department of Urology, Ospedale del Mare, I‑80147 Naples, Italy, Department of Chemistry, University of Malta, Msida MSD2080, Malta, Department of Urology, Umberto I Hospital, Nocera, Inferiore, I‑84014 Salerno, Italy, Department of Medical Biotechnologies, University of Siena, I‑53100 Siena, Italy, Department of Civil Engineering, University of Salerno, Fisciano, I‑84084 Salerno, Italy, Department of Medicine and Surgery, LUM University, I‑70010 Bari, Italy
Published online on: June 20, 2022 https://doi.org/10.3892/mco.2022.2560
Article Number: 127
Copyright: © Baio et al. This is an open access article distributed under the terms of Creative Commons Attribution License.

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Abstract

The present study aimed to investigate the relationship between BMI and the prostate cancer (PCa) risk at biopsy in Italian men. Retrospective analyses of the clinical data of 2,372 consecutive men undergoing ultrasound‑guided multicore (≥10) prostate biopsy transrectally between May 2010 and December 2018 were performed. BMIs were categorized, according to Western countries' classification of obesity, as follows: <18.5 kg/m² (underweight), 18.5‑24.99 kg/m² (normal weight), 25‑30 kg/m² (overweight) and >30 kg/m² (obese). The distribution of patients undergoing biopsy was compared with a model population from the official survey data. Patient characteristics and the relationships between characteristics were investigated using correlation analysis, ANOVA, Kruskal‑Wallis and Dunn's tests. The present study estimated the influence on cancer incidence not only of BMI but also of other patient characteristics using multi‑variable logistic modelling and compared, using the models, the expected outcomes for patients who differed only in BMI. From a sample of 2,372 men, the present study enrolled 1,079 men due to a lack of clinical data [such as prostate specific antigen (PSA) and BMI data] in the other patients undergoing prostate biopsy. Their distribution was significantly different from the model distribution with the probability of undergoing biopsy increasing with increasing BMI. The median age was 69.4 years. The median BMI was 26.4 kg/m², while the median PSA level was 7.60 ng/ml. In total, the biopsies detected PCa in 320 men (29.7%) and high‑grade PCa (HGPCa) in 218 men (20.2%). Upon applying the aforementioned Western countries' criteria for BMI categories, there were 4 (0.4%) underweight, 318 (29.5%) of normal weight, 546 (50.6%) overweight, and 211 (19.6%) obese patients. ANOVA/Kruskal‑Wallis tests revealed that overweight and obese men were younger than the normal‑weight men, while there was no statistical difference in their PSA values. Furthermore, 29.3% of normal‑weight men, 29.5% of overweight men and 29.9% of obese men were diagnosed with PCa, while 19.5% of normal‑weight men, 20.1% of overweight men and 21.8% of obese men were affected by severe cancer. BMI was found to be positively correlated with PCa risk and negatively correlated with both age and PSA level. Age and PSA level were both positively correlated with PCa risk, while digital rectal examination (DRE) outcome was strongly indicative of PCa discovery if the test outcome was positive. Logistics models attributed a positive coefficient to BMI when evaluated against both PCa risk and HGPCa risk. In patients having a negative DRE outcome who differed only in BMI, logistic regression showed a 60% increased risk of PCa diagnosis in obese patients compared with in normal‑weight patients. This risk difference increased when other characteristics were less indicative of PCa (younger age/lower PSA), while it decreased when patient characteristics were more indicative (older age/higher PSA, positive DRE). In conclusion, the present study demonstrated that, in men with higher BMIs, the risk of PCa is higher. The relative difference in risk between low and high BMI is most pronounced in younger patients having a lower PSA level and a negative DRE outcome.

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1	Bell KJ, Del Mar C, Wright G, Dickinson J and Glasziou P: Prevalence of incidental prostate cancer: A systematic review of autopsy studies. Int J Cancer. 137:1749–1757. 2015.PubMed/NCBI View Article : Google Scholar
2	Ferlay J, Soerjomataram I, Dikshit R, Eser S, Mathers C, Rebelo M, Parkin DM, Forman D and Bray F: Cancer incidence and mortality worldwide: Sources, methods and major patterns in GLOBOCAN 2012. Int J Cancer. 136:E359–E386. 2015.PubMed/NCBI View Article : Google Scholar
3	Haas GP, Delongchamps N, Brawley OW, Wang CY and de la Roza G: The worldwide epidemiology of prostate cancer: Perspectives from autopsy studies. Can J Urol. 15:3866–3871. 2008.PubMed/NCBI
4	Jansson KF, Akre O, Garmo H, Bill-Axelson A, Adolfsson J, Stattin P and Bratt O: Concordance of tumor differentiation among brothers with prostate cancer. Eur Urol. 62:656–561. 2012.PubMed/NCBI View Article : Google Scholar
5	Hemminki K: Familial risk and familial survival in prostate cancer. World J Urol. 30:143–148. 2012.PubMed/NCBI View Article : Google Scholar
6	Randazzo M, Müller A, Carlsson S, Eberli D, Huber A, Grobholz R, Manka L, Mortezavi A, Sulser T, Recker F and Kwiatkowski M: A positive family history as a risk factor for prostate cancer in a population-based study with organised prostate-specific antigen screening: Results of the Swiss European randomised study of screening for prostate cancer (ERSPC, Aarau). BJU Int. 117:576–583. 2016.PubMed/NCBI View Article : Google Scholar
7	Tan DS, Mok TS and Rebbeck TR: Cancer genomics: Diversity and disparity across ethnicity and geography. J Clin Oncol. 34:91–101. 2016.PubMed/NCBI View Article : Google Scholar
8	Eeles RA, Olama AA, Benlloch S, Saunders EJ, Leongamornlert DA, Tymrakiewicz M, Ghoussaini M, Luccarini C, Dennis J, Jugurnauth-Little S, et al: Identification of 23 new prostate cancer susceptibility loci using the iCOGS custom genotyping array. Nat Genet. 45:385–391, 391e1-e2. 2013.PubMed/NCBI View Article : Google Scholar
9	Amin Al Olama A, Dadaev T, Hazelett DJ, Li Q, Leongamornlert D, Saunders EJ, Stephens S, Cieza-Borrella C, Whitmore I, Benlloch Garcia S, et al: Multiple novel prostate cancer susceptibility signals identified by fine-mapping of known risk loci among Europeans. Hum Mol Genet. 24:5589–5602. 2015.PubMed/NCBI View Article : Google Scholar
10	Pritchard CC, Mateo J, Walsh MF, De Sarkar N, Abida W, Beltran H, Garofalo A, Gulati R, Carreira S, Eeles R, et al: Inherited DNA-repair gene mutations in men with metastatic prostate cancer. N Engl J Med. 375:443–453. 2016.PubMed/NCBI View Article : Google Scholar
11	Lynch HT, Kosoko-Lasaki O, Leslie SW, Rendell M, Shaw T, Snyder C, D'Amico AV, Buxbaum S, Isaacs WB, Loeb S, et al: Screening for familial and hereditary prostate cancer. Int J Cancer. 138:2579–2591. 2016.PubMed/NCBI View Article : Google Scholar
12	Ewing CM, Ray AM, Lange EM, Zuhlke KA, Robbins CM, Tembe WD, Wiley KE, Isaacs SD, Johng D, Wang Y, et al: Germline mutations in HOXB13 and prostate-cancer risk. N Engl J Med. 366:141–149. 2012.PubMed/NCBI View Article : Google Scholar
13	Leitzmann MF and Rohrmann S: Risk factors for the onset of prostatic cancer: Age, location, and behavioral correlates. Clin Epidemiol. 4:1–11. 2012.PubMed/NCBI View Article : Google Scholar
14	Breslow N, Chan CW, Dhom G, Drury RA, Franks LM, Gellei B, Lee YS, Lundberg S, Sparke B, Sternby NH and Tulinius H: Latent carcinoma of prostate at autopsy in seven areas. The international agency for research on cancer, Lyons, France. Int J Cancer. 20:680–688. 1977.PubMed/NCBI View Article : Google Scholar
15	Global Health Risks: Mortality and burden of disease attributable to selected major risks. World Health Organisation: Geneva, Switzerland, 2019.
16	Kaaks R and Kühn T: Epidemiology: Obesity and cancer-the evidence is fattening up. Nat Rev Endocrinol. 10:644–645. 2014.PubMed/NCBI View Article : Google Scholar
17	Bhaskaran K, Douglas I, Forbes H, dos-Santos-Silva I, Leon DA and Smeeth L: Body-mass index and risk of 22 specific cancers: A population-based cohort study of 5·24 million UK adults. Lancet. 384:755–765. 2014.PubMed/NCBI View Article : Google Scholar
18	American Cancer Society: Cancer facts and figures. American Cancer Society: Atlanta, GA, USA, 2012.
19	Buschemeyer WC III and Freedland SJ: Obesity and prostate cancer: Epidemiology and clinical implications. Eur Urol. 52:331–343. 2007.PubMed/NCBI View Article : Google Scholar
20	Culp S and Porter M: The effect of obesity and lower serum prostate-specific antigen levels on prostate-cancer screening results in American men. BJU Int. 104:1457–1461. 2009.PubMed/NCBI View Article : Google Scholar
21	Baillargeon J, Pollock BH, Kristal AR, Bradshaw P, Hernandez J, Basler J, Higgins B, Lynch S, Rozanski T, Troyer D and Thompson I: The association of body mass index and prostate-specific antigen in a population-based study. Cancer. 103:1092–1095. 2005.PubMed/NCBI View Article : Google Scholar
22	Freedland SJ, Terris MK, Platz EA and Presti JC Jr: Body mass index as a predictor of prostate cancer: Development versus detection on biopsy. Urology. 66:108–113. 2005.PubMed/NCBI View Article : Google Scholar
23	Fowke JH, Signorello LB, Chang SS, Matthews CE, Buchowski MS, Cookson MS, Ukoli FM and Blot WJ: Effects of obesity and height on prostate-specific antigen (PSA) and percentage of free PSA levels among African-American and Caucasian men. Cancer. 107:2361–2367. 2006.PubMed/NCBI View Article : Google Scholar
24	Beebe-Dimmer JL, Faerber GJ, Morgenstern H, Werny D, Wojno K, Halstead-Nussloch B and Cooney KA: Body composition and serum prostate-specific antigen: Review and findings from Flint men's health study. Urology. 71:554–560. 2008.PubMed/NCBI View Article : Google Scholar
25	Rundle A and Neugut AI: Obesity and screening PSA levels among men undergoing an annual physical exam. Prostate. 68:373–380. 2008.PubMed/NCBI View Article : Google Scholar
26	Grubb RL III, Black A, Izmirlian G, Hickey TP, Pinsky PF, Mabie JE, Riley TL, Ragard LR, Prorok PC, Berg CD, et al: Serum prostate-specific antigen hemodilution among obese men undergoing screening in the prostate, lung, colorectal, and ovarian cancer screening trial. Cancer Epidemiol Biomarkers Prev. 18:748–751. 2009.PubMed/NCBI View Article : Google Scholar
27	Barqawi AB, Golden BK, O'Donnell C, Brawer MK and Crawford ED: Observed effect of age and body mass index on total and complexed PSA: Analysis from a national screening program. Urology. 65:708–712. 2005.PubMed/NCBI View Article : Google Scholar
28	Price MM, Hamilton RJ, Robertson CN, Butts MC and Freedland SJ: Body mass index, prostate-specific antigen, and digital rectal examination findings among participants in a prostate cancer screening clinic. Urology. 71:787–791. 2008.PubMed/NCBI View Article : Google Scholar
29	Bañez LL, Hamilton RJ, Partin AW, Vollmer RT, Sun L, Rodriguez C, Wang Y, Terris MK, Aronson WJ, Presti JC Jr, et al: Obesity-related plasma hemodilution and PSA concentration among men with prostate cancer. JAMA. 298:2275–2280. 2007.PubMed/NCBI View Article : Google Scholar
30	Fontaine KR, Heo M and Allison DB: Obesity and prostate cancer screening in the USA. Public Health. 119:694–698. 2005.PubMed/NCBI View Article : Google Scholar
31	Fowke JH, Signorello LB, Underwood W III, Ukoli FA and Blot WJ: Obesity and prostate cancer screening among African-American and Caucasian men. Prostate. 66:1371–1380. 2006.PubMed/NCBI View Article : Google Scholar
32	Scales CD Jr, Curtis LH, Norris RD, Schulman KA, Dahm P and Moul JW: Relationship between body mass index and prostate cancer screening in the United States. J Urol. 177:493–498. 2007.PubMed/NCBI View Article : Google Scholar
33	Engeland A, Tretli S and Bjørge T: Height, body mass index, and prostate cancer: A follow-up of 950000 Norwegian men. Br J Cancer. 89:1237–1242. 2003.PubMed/NCBI View Article : Google Scholar
34	Andersson SO, Wolk A, Bergström R, Adami HO, Engholm G, Englund A and Nyrén O: Body size and prostate cancer: A 20-year follow-up study among 135006 Swedish construction workers. J Natl Cancer Inst. 89:385–389. 1997.PubMed/NCBI View Article : Google Scholar
35	Jemal A, Bray F, Center MM, Ferlay J, Ward E and Forman D: Global cancer statistics. CA Cancer J Clin. 61:69–90. 2011.PubMed/NCBI View Article : Google Scholar
36	Freedland SJ, Bañez LL, Sun LL, Fitzsimons NJ and Moul JW: Obese men have higher-grade and larger tumors: An analysis of the duke prostate center database. Prostate Cancer Prostatic Dis. 12:259–263. 2009.PubMed/NCBI View Article : Google Scholar
37	Hu MB, Xu H, Bai PD, Jiang HW and Ding Q: Obesity has multifaceted impact on biochemical recurrence of prostate cancer: A dose-response meta-analysis of 36,927 patients. Med Oncol. 31(829)2014.PubMed/NCBI View Article : Google Scholar
38	Hutterer G, Perrotte P, Gallina A, Walz J, Jeldres C, Traumann M, Suardi N, Saad F, Bénard F, Valiquette L, et al: Body mass index does not predict prostate-specific antigen or percent free prostate-specific antigen in men undergoing prostate cancer screening. Eur J Cancer. 43:1180–1187. 2007.PubMed/NCBI View Article : Google Scholar
39	Capitanio U, Perrotte P, Hutterer GC, Suardi N, Jeldres C, Shariat SF, Duclos A, Arjane P, Montorsi F and Karakiewicz PI: Effect of body mass index on prostate-specific antigen and percentage free prostate-specific antigen: Results from a prostate cancer screening cohort of 1490 men. Int J Urol. 16:91–95. 2009.PubMed/NCBI View Article : Google Scholar
40	Freedland SJ, Platz EA, Presti JC Jr, Aronson WJ, Amling CL, Kane CJ and Terris MK: Obesity, serum prostate specific antigen and prostate size: Implications for prostate cancer detection. J Urol. 175:500–504. 2006.PubMed/NCBI View Article : Google Scholar
41	Hu MB, Liu SH, Jiang HW, Bai PD and Ding Q: Obesity affects the biopsy-mediated detection of prostate cancer, particularly high-grade prostate cancer: A dose-response meta-analysis of 29,464 Patients. PLoS One. 9(e106677)2014.PubMed/NCBI View Article : Google Scholar
42	MacInnis RJ and English DR: Body size and composition and prostate cancer risk: Systematic review and meta-regression analysis. Cancer Causes Control. 17:989–1003. 2006.PubMed/NCBI View Article : Google Scholar
43	Kobayashi T, Mitsumori K, Nishizawa K, Kawahara T, Ogura K and Ide Y: Association between body mass index and prostate cancer detection rates in Japanese urologic patients. Urology. 66:130–134. 2005.PubMed/NCBI View Article : Google Scholar
44	Masuda H, Kagawa M, Kawakami S, Numao N, Matsuoka Y, Yokoyama M, Yamamoto S, Yonese J, Fukui I and Kihara K: Body mass index influences prostate cancer risk at biopsy in Japanese men. Int J Urol. 20:701–707. 2013.PubMed/NCBI View Article : Google Scholar
45	Park J, Cho SY, Lee SB, Son H and Jeong H: Obesity is associated with higher risk of prostate cancer detection in a biopsy population in Korea. BJU Int. 114:891–895. 2014.PubMed/NCBI View Article : Google Scholar
46	Lee SE, Hong SK, Park HZ, Chang JS, Yoon CY, Byun SS and Abdullajanov M: Higher body mass index is associated with lower risk of prostate cancer detection via multi (≥12)-core prostate biopsy in Korean men. Urology. 76:1063–1066. 2010.PubMed/NCBI View Article : Google Scholar
47	Oh JJ, Jeong SJ, Lee BK, Jeong CW, Byun SS, Hong SK and Lee SE: Does obesity affect the accuracy of prostate-specific antigen (PSA) for predicting prostate cancer among men undergoing prostate biopsy. BJU Int. 112:E265–E271. 2013.PubMed/NCBI View Article : Google Scholar
48	Lavalette C, Cordina Duverger E, Artaud F, Rébillard X, Lamy PJ, Trétarre B, Cénée S and Menegaux F: Body mass index trajectories and prostate cancer risk: Results from the EPICAP study. Cancer Med. 9:6421–6429. 2020.PubMed/NCBI View Article : Google Scholar
49	Michael J, Oyekunle T, Howard L, De Hoedt A, Hoyo C, Grant D and Freedland S: Interplay between exercise and BMI; results from an equal access, racially diverse biopsy study. Cancer Causes Control. 30:13–20. 2019.PubMed/NCBI View Article : Google Scholar
50	Werny DM, Thompson T, Saraiya M, Freedman D, Kottiri BJ, German RR and Wener M: Obesity is negatively associated with prostate-specific antigen in U.S. men, 2001-2004. Cancer Epidemiol Biomarkers Prev. 16:70–76. 2007.PubMed/NCBI View Article : Google Scholar
51	Kim YJ, Han BK, Hong SK, Byun SS, Kim WJ and Lee SE: Body mass index influences prostate-specific antigen in men younger than 60 years of age. Int J Urol. 14:1009–1012. 2007.PubMed/NCBI View Article : Google Scholar
52	Isom-Batz G, Bianco FJ Jr, Kattan MW, Mulhall JP, Lilja H and Eastham JA: Testosterone as a predictor of pathological stage in clinically localized prostate cancer. J Urol. 173:1935–1937. 2005.PubMed/NCBI View Article : Google Scholar
53	Nwadi UV, Nwofor AME, Oranusi CK, Orakwe JC, Obiesie EA, Mbaeri TU, Abiahu JA and Mbonu OO: Correlation between body mass index and gleason score in men with prostate cancer in Southeastern Nigeria. Niger J Surg. 27:22–27. 2021.PubMed/NCBI View Article : Google Scholar
54	Price RS, Cavazos DA, De Angel RE, Hursting SD and deGraffenried LA: Obesity-related systemic factors promote an invasive phenotype in prostate cancer cells. Prostate Cancer Prostatic Dis. 15:135–143. 2012.PubMed/NCBI View Article : Google Scholar
55	Nandeesha H: Insulin: A novel agent in the pathogenesis of prostate cancer. Int Urol Nephrol. 41:267–272. 2009.PubMed/NCBI View Article : Google Scholar
56	Fowke JH, Motley SS, Cookson MS, Concepcion R, Chang SS, Wills ML and Smith JA Jr: The association between body size, prostate volume and prostate-specific antigen. Prostate Cancer Prostatic Dis. 10:137–142. 2007.PubMed/NCBI View Article : Google Scholar
57	Park JH, Cho BL, Kwon HT, Lee CM and Han HJ: Effect of body mass index and waist circumference on prostate specific antigen and prostate volume in a generally healthy Korean population. J Urol. 182:106–111. 2009.PubMed/NCBI View Article : Google Scholar
58	Yang CY, Peng CY, Liu YC, Chen WZ and Chiou WK: Surface anthropometric indices in obesity-related metabolic diseases and cancers. Chang Gung Med J. 34:1–22. 2011.PubMed/NCBI
59	Qu YY, Dai B, Kong YY, Chang K, Ye DW, Yao XD, Zhang SL, Zhang HL and Yang WY: Influence of obesity on localized prostate cancer patients treated with radical prostatectomy. Asian J Androl. 15:747–752. 2013.PubMed/NCBI View Article : Google Scholar
60	Choi JB, Myong JP, Lee Y, Kim I, Kim JH, Hong SH and Ha US: Does increased body mass index lead to elevated prostate cancer risk? It depends on waist circumference. BMC Cancer. 20(589)2020.PubMed/NCBI View Article : Google Scholar