Tropical Medicine and International Health volume 9 no 4 pp 520525 april 2004

Urinary tract infections and genitourinary abnormalities in Cameroonian men

Matthew F. Yuyun1, Fru F. Angwafo III2, Sinata Koulla-Shiro3 and Jimmy Zoung-Kanyi2
1 Department of Public Health and Primary Care, School of Clinical Medicine, University of Cambridge, UK 2 Department of Surgery, Faculty of Medicine and Biomedical Sciences, University of Yaounde, Cameroon 3 Department of Infectious Diseases, Faculty of Medicine and Biomedical Sciences, University of Yaounde, Cameroon

Summary

objective To compare the prevalence of genitourinary abnormalities in men diagnosed with urinary tract infection (UTI) in a Cameroonian hospital and those without. patients and methods Consecutive adult men aged 1875 years, whose midstream urine samples were received for microscopy, culture and sensitivity at the microbiology laboratory of the Yaounde University Teaching Hospital, Cameroon, constituted the study population. Genitourinary abnormalities were diagnosed from history, physical examination, abdominal and transrectal ultrasonography, plain abdominal X-ray, and if indicated urethrocystoscopy and biopsy. results Of the 206 patients who qualied, 179 completed the study and 63 (35.2%) were found to have UTI. A total of 41 (65.1%) patients with UTI (mean age 69.2 years) had at least one genitourinary abnormality, compared to 13 (11.2%) of those without UTI (mean age 61.9 years) (P < 0.001). The age-adjusted prevalence of genitourinary abnormalities was 59.4% in the UTI group and 12.1% in the non-UTI group (P < 0.001). The most frequent genitourinary abnormality in men with UTI was benign prostatic enlargement, followed by urethral stricture. The crude odds ratio (95% condence intervals) for UTI associated with genitourinary abnormality was 14.77 (6.8032.05), and the adjusted odds ratio 11.51 (7.0829.46). conclusion Urological evaluation of Cameroonian men with UTI, using simple history taking, physical examination, ultrasound examination and plain abdominal X-ray, could have signicant clinical benets in this tropical African region. keywords urinary tract infections, prostatic hyperplasia, urethral stricture, urinary calculi, neoplasms

Introduction After the post-infancy drop, the prevalence of urinary tract infection (UTI) increases with age, and is signicantly higher in women (520% depending on age group) than in men (0.110%) (Kunin 1997; Lindert & Shortliffe 1999). Most of the UTIs seen in women are uncomplicated (occurring in otherwise healthy individuals without any metabolic, functional or anatomic abnormality of the urinary tract) (Anderson 1999). However, after middle age, the prevalence and incidence of UTI increase progressively in men, with a concomitant and progressive decrease in the female-to-male prevalence ratio (Schaeffer 1996; Kunin 1997). Studies conducted in developed countries have shown that 4080% of adult men with UTI have an underlying genitourinary abnormality (Schaeffer 1996; Kunin 1997; Ulleryd et al. 2001; Andrews et al. 2002). Today, there 520

appears to be a general consensus that UTI in men of any age should be considered as complicated, and that urological evaluation of these patients should be mandatory (Lipsky 1989; Kunin 1997; Lindert & Shortliffe 1999). However, this practice is based only on the high prevalence of obstructive abnormalities observed in descriptive case series studies of men with UTI. Analytical studies involving comparison of the distribution of genitourinary abnormalities in men without UTI are lacking. Descriptive statistics of genitourinary abnormalities in men with UTI in sub-Saharan African are still unknown. In this region, where infectious diseases still account for the overall highest rate of morbidity and mortality (WHO 2000), it remains unclear whether UTIs in men are complicated by underlying urinary tract abnormalities as is the case in western countries or whether they arise as a result of the same general risk factors (malnutrition,

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poverty, lack of portable water supply, poor hygiene and sanitation), which account for the high occurrence of other infectious diseases. We therefore undertook this study to compare the prevalence of genitourinary abnormalities in men with and those without UTI. We thought it would also be useful to evaluate the risk of UTI associated with an underlying genitourinary abnormality in men.

37 C, was considered signicant and thus diagnostic of UTI (Kass & Finland 1956). Germs were identied through Gram-stain and biochemical tests. Positive cultures were sensitivity-tested using the Mueller Hinton medium and a list of antibiotic discs. Uroculture and sensitivity tests were conducted according the National Committee for Clinical Laboratory Standards (NCCLS) guidelines. Dipstick (Multitx) urinalyses were also done. Diagnosis of genitourinary abnormalities Men were invited to the Urology Clinic for history and physical examination, including a digital rectal examination. The International Prostate Symptom Score (I-PSS) questionnaire was also administered to all patients. The I-PSS is based on the answers to seven questions concerning lower urinary tract symptoms and the total score ranges from 0 to 35 (I-PSS 1993). They also had an abdominal ultrasound, transrectal ultrasound (some) and plain abdominal X-ray. Abdominal ultrasound was done using the B-mode ultrasonography (3.5 MHz transducer), with a hand-held probe, and post-void residual urine volume (PVR) was calculated from the formula for an ellipsoid [p/6 (width) (height) (depth)] (Roehrborn & Peters 1988). Post-void residual urine volume measurements were positively skewed and results are presented as the median, 25th and 75th percentiles. A smooth, non-tender prostate volume >30 ml was considered as benign prostatic hyperplasia (Jakobsen et al. 1988). If indicated, urethrocystoscopy was done by an urologist. Biopsies were also advised and done if indicated. Venous blood samples were collected and serum prostatic-specic antigen (PSA), urea and creatinine assayed. If PSA exceeded 10 ng/ml, then further investigation was carried out because of the high probability of prostate cancer (Oesterling et al. 1993). Ultrasonography and plain abdominal X-ray were carried out as routine investigations by radiologists who were blinded to the UTI status of the patients. Based on ndings from history, physical examination and investigations, patients were classied into two binary categories, namely presence or absence of genitourinary abnormalities. Ethical approval for this study was obtained from the research-guiding Ethics Committee of the Faculty of Medicine and Biomedical Science, University of Yaounde, Cameroon. Urological assessment was conducted after obtaining informed consent from the patients. Statistical analyses Comparison of characteristics between men with UTI and those without was by the Students t-test for quantitative variables and the chi-squared test for qualitative variables. 521

Patients and methods Study population Adult men aged 18 years and above, whose urine samples were consecutively received in the microbiology laboratory of the Yaounde Central Hospital (teaching hospital of the University of Yaounde), Cameroon, for microscopy, culture and sensitivity constituted the study population. Recruitment began in April 1996, and ended in October 1997. Excluded were patients with risk factors for UTI, such as catheterized men and any instrumentation, patients with physician diagnosis of diabetes, diagnosed AIDS patients, stulae, post-operative patients, patients with a recent history of antimicrobial therapy (within the preceding 2 weeks of urine collection), non-ambulating patients and patients with psychiatric disorders. A total of 206 male patients who had a urine culture were retained for the study after the exclusion criteria were applied. They were invited for investigation for genitourinary abnormalities. Twenty-four patients declined, and of those who consented, two died from myocardial infarction and one from ruptured oesophageal varices, before investigations had been conducted, leaving a total of 179 as the nal study population. The ages of patients ranged from 18 to 75 years, with more than 90% aged 50 years or more. Diagnosis of UTI Early morning clean-catch midstream urine was collected in a 20-ml sterile screw-capped container, and immediately taken to the microbiology laboratory for microscopy, culture and sensitivity. In situations where collection of early morning urine was impossible, urine was collected at least 4 h after the last micturition. If a delay of more than 1 h was anticipated after urine microscopy, then the urine specimen was refrigerated at 4 C, awaiting culture. Uroculture was done on two media: Debrinated Human Blood Agar and Eosin Methylene Blue (selective for Gramnegative uropathogens). A bacterial colony count of 105 CFU/ml of midstream urine, after an overnight culture of the inoculated plates incubated aerobically at

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Adopting the cross-sectional casecontrol design, logistic regression analyses were used to determine the risk of UTI given the presence of genitourinary abnormality. Men with UTI were considered as cases and those without UTI were considered as controls. The Wald test was used for testing hypothesis about individual coefcients in the regression analyses, and in all hypotheses testing the risk of Type 1 error was set a priori at P < 0.05. The statistical package used for these analyses was stata 6.

Results Characteristics of the study population Of the 179 men who completed the study, 63 (35.2%) were found to have UTI on uroculture, while 116 (64.8%) did not. Table 1 shows the characteristics of men with proven UTI compared to those without. The median age in men with UTI was 67.9 years, and in those without UTI 63.3 (P 0.012). The mean I-PSS in patients with UTI was 13.7, compared to 5.9 in those without UTI (P < 0.001). Mean total serum creatinine and urea, which are biochemical signals of renal failure, were signicantly higher in UTI cases, as well as the presence of dipstick haematuria or proteinuria. Risk of UTI associated with presence of genitourinary abnormalities A total of 41 (65.1%) patients with UTI had at least one genitourinary abnormality, compared to 13 (11.2%) in those without UTI, P < 0.001 (Table 2 and Figure 1). The age-adjusted prevalence of genitourinary abnormalities was 59.4% (for UTI group) and 12.1% (for non-UTI group), P < 0.001. The most frequent type of genitourinary

abnormality was benign prostatic enlargement (BPE), followed by urethral stricture and prostate cancer in both men with UTI and those without. The less frequent types of genitourinary abnormalities were grouped together as other causes. These were urinary calculus, bladder cancer, hydronephrosis, hydroureter, spinal disease, colorectal carcinoma and kidney carcinoma. Some patients had more than one urinary tract abnormality (e.g. urolithiasis and BPE occurring together). The crude odds ratio (95% condence intervals) for UTI associated with genitourinary abnormality was 14.77 (6.8032.05). Adjusting for age, the values became 11.51 (7.0829.46). Comparison of clinical characteristics of men with UTI with and without genitourinary abnormalities Characteristics of men with UTI carrying an underlying genitourinary abnormality, and those with UTI but without a genitourinary abnormality, are compared in Table 3. Uropathogens Gram-negative bacilli of the group Enterobacteriaceae were the principal uropathogens identied. The most frequent amongst them was Escherichia coli, which accounted for 58.6% of all UTIs, followed by Proteus mirabilis (18.2%), Klebsiella pnuemoniae (9.4%), Pseudomonas auriginosa (3.0%). Gram-positive cocci accounted for 10.8% of all UTIs (Staphylococcus saprophyticus, Staphylococcus aureus, Streptococcus pyogenes and Enterococcus faecalis). About 98.7% of the germs identied were sensitive to uoroquinolones, 94.2% to third-generation cephalosporines, 86.1% to amoxillin/ clavulanate, 74.0% to aminoglycosides, 65.2% to cotrimoxazole and lower sensitivities for other antibiotics. One

UTI absent, n 116 Median age (years)* Mean I-PSS Dysuria, n (%) Haematuria, n (%) Proteinuria, n (%) Mean serum creatinine (lmol/l) Mean serum urea (mmol/l) Mean PSA (ng/ml) Median PVR (ml)* Mean prostate volume (ml) 63.3 (54.2, 71.8) 5.9 (2.2) 1 (0.9%) 4 (3.4%) 4 (3.4%) 112.9 (7.8) 4.7 (0.7) 3.1 (0.5) 13.6 (4.9, 43.7) 18.7 (7.7)

UTI present, n 63 67.9 (58.0, 74.1) 13.7 (6.3) 10 (15.9%) 18 (28.6%) 46 (73.0%) 139.0 (16.6) 6.9 (1.1) 6.9 (2.1) 49.4 (25.1, 129.2) 26.5 (13.6)

P value 0.012 <0.001 <0.001 <0.001 <0.001 <0.001 0.006 0.004 <0.001 <0.001

Table 1 Characteristics of men with urinary tract infection and men without (n 179)

* Median (25th, 75th percentile). Data are mean (standard deviation) or number (percentage). I-PSS, International Prostate Symptom Score; PVR, post-void residual urine volume; PSA, prostate-specic antigen.

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Table 2 Prevalence of genitourinary abnormalities in men with urinary tract infection compared to those without (n 179) UTI absent, n 116 All genitourinary abnormalities Benign prostatic enlargement Urethral stricture Prostate cancer Others 13 (11.2%) 9 (7.8%) 1 (0.9%) 2 (1.7%) 3 (2.5%) UTI present, n 63 41 (65.1%) 26 (41.3%) 5 (7.9%) 4 (6.3%) 9 (14.3%)

Renal insufciency Nine patients (14.3%) with UTI had renal failure dened as serum creatinine levels >150 lmol/l compared to three (2.6%) in the group without UTI (P < 0.001). Among the nine cases of renal failure in the UTI group, six had an underlying functional of anatomical genitourinary abnormality and three were without (two had glomerulonephritis and one had no other clinically detectable abnormality apart from UTI, using the clinical investigations at our disposal). Four patients with UTI had renal scarring/small kidney on combined abdominal ultrasound and plain abdominal X-ray. Among the three non-UTI men with abnormally raised serum creatinine levels, two were imputable to obstructive uropathy and one to renovascular atherosclerotic disease (Table 1). Discussion Obstructive urinary tract abnormalities may lead to stagnation of urine and distension of the urinary tract wall proximal to the obstruction. A larger volume of stagnated urine serves as an excellent culture medium for bacteria to persist and multiply (Neal 1999). Bacteria adherence to the urothelium is an essential early step in the initiation of UTI. Under normal urinary ow, bacteria virulence factors like pili or mbrae, which are used to adhere to the epithelial cells lining the urinary tract are less effective, as the continuous urine current sweeps bacteria down the tract. In the absence of a good mechanical action of urine ow during an obstruction, bacteria easily adhere and multiply (Neal 1999). If the obstruction is severe, reux of infected urine to the renal pelvis and renal parenchyma can lead to pyelonephritis, renal abscess, urosepsis and death (Conrad et al. 1991).

P value <0.001 <0.001 <0.001 <0.001 <0.001

Data are number of genitourinary abnormalities (prevalence). Some patients had more than one genitourinary abnormality.

Prevalence of genitourinary abnormalities (%)

70 60 50 40 30 20 10 0

65.10%

P < 0.001
11.20%

UTI absent

UTI present

Urinary tract infection

Figure 1 Prevalence of genitourinary abnormalities in men with urinary tract infection compared to those without (n 179).

patient had a multi-drug resistant E. faecalis, and on interview was found to have received incomplete doses of many antibiotics prescribed empirically.

Table 3 Comparative assessment of clinical characteristics of men with urinary tract infection (UTI) carrying an underlying genitourinary abnormality (GUA), and those with UTI but without GUA (n 63)

UTI without GUA, n 22 UTI with GUA, n 41 P value Median age (years)* 66.3 (58.2, 71.8) Mean I-PSS 6.5 (4.0) Dysuria, n (%) 4 (18.1%) Haematuria, n (%) 5 (22.7 %) Proteinuria, n (%) 15 (68.2%) Mean creatinine (lmol/l) 119.9 (10.6) Mean urea (mmol/l) 5.3 (0.7) Mean PSA (ng/ml) 6.7 (2.2) Median PVR (ml)* 21.1 (10.0, 88.7) Mean prostate volume (ml) 20.8 (9.6) 68.9 (57.0, 74.7) 19.4 (7.1) 5 (12.2%) 13 (31.7%) 31 (75.6%) 143.2 (17.7) 7.2 (1.3) 7.0 (1.9) 62.6 (29.1, 173.5) 29.7 (14.2) 0.162 <0.001 0.030 0.194 0.227 0.005 0.026 0.323 <0.001 <0.001

* Median (25th, 75th percentile). Data are mean (standard deviation) or number (percentage). I-PSS, International Prostate Symptom Score; PVR, post-void residual urine volume; PSA, prostate specic antigen.

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In this study, benign prostatic enlargement was the most frequent genitourinary abnormality, followed by urethral stricture and prostate cancer. This is similar to the earlier ndings of others in tropical Africa (Zoung Kanyi et al. 1989; Ogbonna et al. 1997; Dawam et al. 2000), who observed high hospital incidences of benign prostatic hyperplasia and identied it as the principal cause of consultation in men with lower urinary tract symptoms. In Sub-Saharan descriptive statistics about urethral strictures are scant in the literature. About 70% of urethral strictures seen in this region are attributable to venereal urethritis, while approximately 30% result from trauma (Ouattara et al. 1990; Ahmed & Kalayi 1998). Recent studies in this geographical region have observed a high hospital incidence of prostate cancer comparable to incidence rates observed in African Americans, and have highlighted the lack of the availability and access to diagnostic techniques and trained man power as probable reasons for the low incidence rates reported earlier in Sub-Saharan Africa (Osegbe 1997; Angwafo 1998). In developed countries, BPE is the most common cause of urinary tract obstruction in men, with urinary calculi surpassing urethral stricture as the second most frequent cause of obstruction (Ulleryd et al. 2001; Andrews et al. 2002). The prevalence of UTI in these Cameroonian men of 35.2% was higher than the 510% observed in clinicbased or community studies of men within a similar age range in the western world (Schaeffer 1996; Kunin 1997). This might be reective of the fact that in this hospital, as is the case in most hospitals in this region, investigations are most often requested only when there is a high index of suspicion from history and physical examination, for economic reasons. Unlike in industrialized countries where it has been observed that 4080% of adult men with UTI have an underlying genitourinary abnormality (Schaeffer 1996; Kunin 1997; Ulleryd et al. 2001; Andrews et al. 2002), data on the association between urinary tract infection and genitourinary abnormalities in adult men are lacking in the developing world. Our ndings indicate that 65.1% of Cameroonian men with UTI have at least a genitourinary abnormality. A signicantly lower prevalence of these abnormalities is observed in men without UTI (11.2%). In addition, we observed that patients with genitourinary abnormalities had approximately 12 times the risk of UTI compared to those without. These ndings indicate that urological evaluation of men with signicant UTI should be mandatory. The most common uropathogen cultured from patient with UTI was Escherichia coli, which is similar to the ndings of others (Schaeffer 1996; Kunin 1997). 524

We dened renal failure as serum creatinine levels >150 lmol/l, which was signicantly more prevalent in patients with UTI compared to those without. It has been observed that UTIs bring about renal scarring (Conrad et al. 1991; Lindert and Shortliffe 1999). The synergistic effect of urinary tract obstruction and UTI may be operational in the genesis of renal insufciency (Klahr et al. 1986). In our study sample, mean level of PSA was signicantly raised in men with UTI compared to those without. Although more prostate cancers cases were seen in the UTI group, PSA might also be elevated due to UTI with prostatitis and might be independent of the prevalence of prostate cancer (van Iersel et al. 1995). This nding is supported by our data, given that there was no signicant difference in mean PSA levels between men with UTI and an underlying genitourinary abnormality, and those with UTI but without a genitourinary abnormality. The selection of controls in this study is, however, a cause for concern, as the prevalence of genitourinary abnormalities in the control group might not necessarily reect the true prevalence of these abnormalities in an average population. If among some of the controls, the request for urine microscopy and culture was part of a work-up for diagnosed or strongly suspected genitourinary abnormality, then the prevalence of genitourinary abnormalities in the control group would be higher than it would have been in an unselected population and the odds ratio would therefore be biased towards null. This implies that if our control group was randomly selected from the community, for example, the odds ratios would be even higher than what we found in our sample. Conclusions This study has shown a signicantly high prevalence of underlying anatomical and functional abnormalities in Cameroonian men with urinary tract infection compared to those without. Urological evaluation of men with UTI, using simple history taking, physical examination, ultrasound examination and plain abdominal X-ray, is of great clinical value and could have signicant clinical benets in this tropical African region. Acknowledgements We are very grateful to the Roche Laboratory for donating culture media and antibiotic discs for sensitivity testing used in this study. We thank Prof. Sow Mamadou and Dr Fouda Joseph Pierre (urologists), and Prof. Gonsu-Fotsin ` Joseph (radiologist) of the Yaounde Central Hospital for their clinical assistance during this study. We are grateful

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to Mrs Mvondo J. Matip and all the laboratory technicians of the microbiology laboratory unit of the Yaounde Central Hospital for the time they devoted to assist us in this work. References
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Authors Dr Matthew F. Yuyun, Department of Public Health and Primary Care, University of Cambridge School of Clinical Medicine, Institute of Public Health, Robinson Way, Cambridge CB2 2SR, UK. Tel.: +44 1223 330309; Fax: +44 1223 330330; E-mail: mfy20@medschl.cam.ac.uk or myuyun20@hotmail.com (corresponding author). Fru F. Angwafo III and Jimmy Zoung-Kanyi, Department of Surgery, Faculty of Medicine and Biomedical Sciences, University of Yaounde, PO Box 1364, Yaounde, Cameroon. E-mail: asanj25@hotmail.com, fobuzshi@yahoo.com Sinata Koulla-Shiro, Department of Infectious Diseases, Faculty of Medicine and Biomedical Sciences, University of Yaounde, PO Box 1364, Yaounde, Cameroon.

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