ORIGINAL ARTICLE

Ultrasonographic evaluation of patients with male accessory gland infection

S La Vignera, A.E. Calogero, R.A. Condorelli, L.O. Vicari, M. Catanuso, R. DAgata & E. Vicari
Section of Endocrinology, Andrology and Internal Medicine and Master in Andrological, Human Reproduction and Biotechnology Sciences, Department of Internal Medicine and Systemic Diseases, Catania University, Catania, Italy

Keywords Male accessory gland infectionmale infertilitytransrectal ultrasonography Correspondence Sandro La Vignera, Section of Endocrinology, Andrology and Internal Medicine, Department of Biomedical Sciences, Catania University, Policlinico G. Rodolico, Via S. Soa 78, Building 4, Room 2C19, Catania 95123, Italy. Tel.: +39 95 378 1180; Fax: +39 95 378 1180; E-mail: sandrolavignera@email.it Accepted: September 7, 2010 doi: 10.1111/j.1439-0272.2010.01132.x

Summary MAGI is the inammation of the accessory male glands that notoriously exerts a negative inuence on male fertility. The diagnosis is integrated by clinical, laboratory and ultrasound evaluation. In particular, the ultrasound criteria were published in 1999. The aim of this study was to analyse the sensitivity and specicity of additional diagnostic ultrasound criteria as well as of conventional criteria in a selected category of infertile patients with MAGI. To accomplish this, 100 patients with MAGI were evaluated by scrotal and transrectal ultrasound by three different operators. The control group consisted of 100 agematched healthy men. Statistical analysis was performed to evaluate sensitivity, specicity, positive and negative predictive values, and ROC curve analysis. The results showed that additional ultrasound criteria had a diagnostic accuracy similar to traditional criteria. The threshold value of two criteria for each diagnostic category (traditional and additional criteria) obtained high values of sensitivity and specicity. In conclusion, this study conrms the validity of the ultrasound criteria of MAGI previously published; in addition, it suggests the clinical utility of other indicators in clinical practice with good diagnostic accuracy and nally it establishes a clear threshold ultrasonographic value for the diagnosis of MAGI.

Introduction MAGI stands for male (sex) accessory gland inammation. There are two main denitions. The rst is that proposed by the WHO (1993) and the other by the NIH in 1995 (Krieger et al., 1999). According to the WHO criteria, the diagnosis of MAGI is based on the presence of sperm alterations (oligo, astheno and/or teratospermia) associated with two or more of the following factors: (i) a history of urogenital infection, sexually transmitted infection and/or presence of postinammatory alterations in the physical examination of testicular and epididymal region and/or anorectal digital exploration of prostate and seminal vesicles; (ii) cytological signs and/or microbiological infection and/or inammation on the secretion obtained after prostatic massage; (iii) signs of infection in ejaculate (leucocytospermia < 1 106 ml)1; spermioculture positive for
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signicant presence of pathogenic bacteria; alterations in physicalchemical properties and/or biochemistry of seminal plasma). According to the NIH Chronic Prostatitis Collaborative Research Network, which produced the classication NIDDK/NIH 1995, published by Krieger et al. (1999), prostatitis includes acute infections of the prostate (category I) and chronic (category II); inammation of the prostate (category IIIa) symptomatic or without symptoms; symptoms/signs attributable to laboratory prostate inammation (category IV) or without inammation (category IIIb). Although WHO recognises MAGI as a cause of male infertility, various studies to determine the extent of the negative impact of these clinical conditions on the reproductive performance show a prevalence ranging from 1.5% to 16%. The wide range of prevalence reported in the literature reects several issues: (i) incomplete and not well characterised diagnosis; (ii) higher prevalence reported in
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cohorts of infertile patients or persistent infection (poorresponder to antibiotic treatment) and/or (iii) past failures of in vitro fertilisation (IVF) programmes. (Comhaire et al., 1980; Andreeben et al., 1993; Diemer et al., 2003; Vicari et al., 2004a). Ultrasonographic evaluation of testes, epididymis, prostate and seminal vesicles is an important tool to evaluate the extension of MAGI. We have found that the negative impact of the inammatory process on sperm quality and, consequently, fertility is higher in clinical forms that simultaneously involve prostate, seminal vesicles and epididymis, compared to clinical forms limited only to the prostate. Recently, we have also reported that only ultrasonographic evaluation is able to discriminate bilateral forms of MAGI from the unilateral forms (Vicari et al., 2006). Thus, we have proposed the following criteria for ultrasonographic diagnosis of MAGI: Prostatitis (Fig. 1) is suspected in the presence of two or more of the following ultrasonographic signs: (a) asymmetry of the gland volume; (b) areas of low echogenicity; (c) areas of high echogenicity; (d) dilatation of peri-prostatic venous plexus. Vesciculitis (Fig. 2) is suspected in the presence of two or more of the following ultrasonographic signs: (a) increased (>14 mm) antero-posterior diameter, mono- or

Fig. 3 Epididymitis: Enlargement of the cephalic tract.

Fig. 1 Prostatitis: hyperechoic area in the right lobe.

Fig. 2 Vesciculitis: increased diameter and polycyclic areas.

bilateral; (b) asymmetry >2.5 mm (normal 714 mm) compared with the controlateral vesicle; (c) reduced (<7 mm) antero-posterior diameter, mono- or bilateral; (d) thickened and/or calcied glandular epithelium; (e) polycyclic areas separated by hyperechoic septa in one or both vesicles. Epididymitis (Fig. 3) is suspected in the presence of two or more of the following ultrasonographic signs: (a) increase in size of the head (cranio-caudal diameter >12 mm) and/or of the tail (cranio-caudal diameter >6 mm) (nding single or bilateral); (b) presence of multiple microcystis in the head and/or tail (nding single or bilateral); (c) low echogenicity or high echogenicity, mono- or bilateral; (d) large hydrocele, mono- or bilateral (Vicari, 1999, 2000; Vicari et al., 2006). After several years from the publication of these criteria, there are no studies about their reproducibility and no other possible ultrasound signs have been proposed. We have tested additional criteria detected with high frequency in these patients. These ultrasound signs are as follows: for prostate: (a) single or multiple internal similar cystic areas and (b) area(s) of moderate increase in vascularity (focal or multiple); for seminal vesicles: (a) fundus/ body ratio >2.5, (b) fundus/body ratio <1; (c) anteroposterior diameter unchanged after recent immediate ejaculation; for epididymis: (a) enlargement in superior part of the cephalic tract and superior/inferior part ratio >1; (b) unchanged antero-posterior diameter of tail after ejaculation (La Vignera et al., 2008a,b). The aim of this study was to evaluate the sensitivity (S) and specicity (Sp) of additional ultrasound signs detected in patients with MAGI and their comparison with conventional ultrasound signs. In addition, S, Sp, positive predictive value (PPV) and negative predictive value (NPV) of each ultrasound nding (traditional and additional) were evaluated. Finally, the best threshold for an ultrasound diagnosis of prostatitis, vesciculitis and epididymitis was evaluated.
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Patients and methods Patient selection The study was conducted on 100 consecutive patients consulting our Andrology outpatient clinic. Their median age was 27 3 years (range 2432 years). The diagnosis of MAGI was performed according to WHO criteria 1993. One hundred fertile healthy men aged 31 2 years (range 2534 years) represented the control group. Exclusion criteria included endocrine disease, history of genitourinary surgery, previous sexual dysfunction, acute urogenital inammation. In detail, all patients were administered a specic questionnaire for MAGI (La Vignera et al., 2008a,b), and underwent a physical examination with digital rectal exploration, sperm analysis with particular evaluation of biochemical markers and leucocytes, cytological and bacteriological examination of prostatic secretion, in addition to microbiological examination of sperm and, nally, ultrasound examination. The presence of MAGI was considered in the presence of oligospermia or oligoasthenospermia or oligoasthenoteratospermia associated with following combinations: 1 factor A (altered anamnesis and/or physical examination) + 1 factor B (altered prostatic secretion); or 1 factor A + 1 factor C (inammatory signs of seminal plasma); or 1 factor B + 1 factor C, or presence of 2 factors C. The protocol was approved by the internal Institutional Review Board and an informed written consent was obtained from each men. Ultrasound evaluation All patients underwent scrotal ultrasound evaluation with a linear probe (7.511 MHz) and prostato-vescicular ultrasound evaluation with an end-re transrectal probe (7.5 MHz). The ultrasound equipment used was Esaote Megas GPX (Genoa, Italy). The ultrasound scans were conducted randomly by three operators. The scores collected were gradually incorporated into an electronic database for subsequent statistical processing. The study was approved by the internal committee of the institute. Statistical analysis S, Sp, PPV, NPV and receiver operating characteristics (ROC) curve were calculated in the three groups. (Pepe, 2003). To measure the accuracy of diagnostic tests, the area under the ROC curve (AUC) is used (Swets, 1996). Classication of the discriminative ability of a test proposed by Swets was used in the interpretation of the AUC. This proposal is based on the following schedule: test is not informative if 0.5 AUC; test is not very
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accurate if 0.5 < AUC < 0.7; test is moderately accurate if 0.7 < AUC < 0.9; test is highly accurate if 0.9 < AUC < 1; test is perfect if AUC = 1. To estimate the standard error of the AUC, we used the method of DeLong et al. (1988), while the estimated condence intervals at 95% were used the binomial distribution. Results A total of 200 ultrasound examinations were performed. Altogether, 20 ultrasonographic signs suggestive of MAGI were detected: six for the diagnosis of prostatitis (two additional and four conventional), eight for the diagnosis of vesciculitis (three additional and ve conventional), six for the diagnosis of epididymitis (two additional and four conventional). Table 1 shows the sensitivity, specicity, positive predictive value and negative predictive value of all ultrasound signs detected (conventional and additional). The search for an overall threshold for a diagnosis shows the following results: the ultrasound diagnosis of prostatitis with more than two signs (conventional and additional) showed a sensitivity of 0.90 (CI 95% = 0.780.97), specicity of 1.00 (CI 95% = 0.961.00), positive predictive value of 1.00 (CI 95% = 0.921.00) and negative predictive value of 1.00 (CI 95% = 0.890.98). The ultrasound diagnosis of vesciculitis with more than two signs (conventional and additional) showed a sensitivity of 1.00 (CI 95% = 0.93 1.00), specicity of 0.98 (CI 95% = 0.930.99), positive predictive value of 0.96 (CI 95% = 0.860.99) and negative predictive value of 1.00 (CI 95% = 0.961.00). Finally, the ultrasound diagnosis of epididymitis with more than two signs (conventional and additional) showed a sensitivity of 1.00 (CI 95% = 0.931.00), specicity of 1.00 (CI 95% = 0.961.00), positive predictive value of 1.00 (CI 95% = 0.931.00) and negative predictive value of 1.00 (CI 95% = 0.961.00). Table 2 shows the analysis of comparison between conventional and additional ultrasonographic criteria for prostatitis, vesciculitis and epididymitis. Discussion The ultrasound study of MAGI is of recent interest: in a rst evaluation, only calcications and dilatation of the venous plexus were reproducible. Other observed ultrasound abnormalities of the prostate and seminal vesicles were poorly reproducible (Schipper et al., 2001). Dohle (2003) reported that only 10% of patients with a history positive for MAGI had prostate abnormalities by transrectal ultrasound (oedema, dilatation of the seminal vesicles and ejaculatory ducts), intraprostatic calcications and dilatation of the periprostatic venous plexus. Our studies
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Table 1 Sensitivity, specicity, positive predictive value and negative predictive value of all ultrasound signs detected (conventional and additional) Specicity (CI 95%) 0.85 0.93 0.90 0.90 0.96 0.95 0.87 0.93 0.95 0.94 0.92 0.96 0.97 0.96 0.86 0.92 0.95 0.88 0.95 0.99 (0.760.91) (0.860.97) (0.870.98) (0.820.95) (0.900.99) (0.890.99) (0.790.93) (0.860.97) (0.890.98) (0.870.98) (0.850.96) (0.900.99) (0.910.99) (0.900.99) (0.770.92) (0.850.96) (0.890.98) (0.800.94) (0.890.98) (0.940.99) Sensitivity (CI 95%) 0.88 0.88 0.80 0.34 0.90 0.90 0.78 0.68 0.90 0.78 0.56 0.90 0.78 0.90 0.90 0.58 0.90 0.54 0.88 0.90 (0.760.95) (0.760.95) (0.660.90) (0.210.49) (0.780.97) (0.780.97) (0.640.88) (0.530.81) (0.780.97) (0.640.88) (0.410.70) (0.780.97) (0.640.85) (0.780.97) (0.780.97) (0.430.72) (0.780.97) (0.390.68) (0.760.95) (0.780.97) Positive predictive value (CI 95%) 0.75 0.86 0.87 0.63 0.92 0.90 0.75 0.83 0.90 0.87 0.78 0.92 0.93 0.92 0.76 0.78 0.90 0.69 0.90 0.98 (0.620.85) (0.740.94) (0.740.95) (0.420.80) (0.800.98) (0.780.97) (0.610.86) (0.680.93) (0.780.97) (0.730.95) (0.610.89) (0.800.98) (0.810.99) (0.800.98) (0.630.86) (0.620.90) (0.780.97) (0.520.83) (0.780.97) (0.880.99) Negative predictive value (CI 95%) 0.93 0.94 0.90 0.73 0.95 0.95 0.89 0.85 0.95 0.89 0.81 0.95 0.90 0.95 0.94 0.81 0.95 0.79 0.94 0.95 (0.860.98) (0.870.98) (0.830.95) (0.640.81) (0.890.98) (0.890.98) (0.810.94) (0.770.91) (0.890.98) (0.820.85) (0.720.87) (0.890.98) (0.820.95) (0.890.98) (0.880.98) (0.730.88) (0.890.98) (0.700.86) (0.870.98) (0.890.98)

US criteria P conventional sign a P conventional sign b P conventional sign c P conventional sign d P additional sign a P additional sign a V conventional sign a V conventional sign b V conventional sign c V conventional sign d V conventional sign e V additional sign a V additional sign b V additional sign c E conventional sign a E conventional sign b E conventional sign c E conventional sign d E additional sign a E additional sign b

P, prostatitis; V, vesciculitis; E, epididymitis.

show that the scrotal and transrectal prostate-vesicular ultrasound scans are able to detect three diagnostic categories: prostatitis, prostato-vesciculitis and prostatovesciculo-epididymitis and, in addition, unilateral or bilateral forms (Vicari, 1999; Vicari et al., 2006). The present study compared the ultrasound characterisation of patients with male accessory gland infections with that of healthy fertile men. Traditional ultrasound criteria, previously published, have been described, for evaluation of their diagnostic specicity and sensitivity, in addition to verifying the reliability of other possible diagnostic ultrasound signs, indicated as additional signs. First, a statistical evaluation of sensitivity, specicity, positive predictive value and negative predictive value was conducted. This initial assessment showed that among the traditional signs of prostatitis, the sign with greater diagnostic accuracy is the presence of hypoechoic areas within the prostate parenchyma, while among the additional signs of prostatitis, both the presence of single or multiple internal cystis in similar areas and area(s) of moderately increased vascularity (focal or multiple) showed the same diagnostic accuracy. Overall, both traditional and additional signs for the study of prostatitis are shown to be highly accurate for diagnosis. Relative to the traditional ultrasonographic signs of vesciculitis, the sign with greater diagnostic accuracy is the presence of reduced (<7 mm) antero-posterior diameter mono- or bilateral, while
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among the additional criteria, it is the presence of fundus/body ratio less than 1 and anteriorposterior diameter unchanged after ejaculation. Overall, both traditional and additional signs for the study of vesciculitis are shown to be highly accurate for diagnosis. As far as the traditional ultrasound signs of epididymitis, the sign with the greatest diagnostic accuracy was the presence of ipoechogenicity or iperechogenicity mono- or bilateral, while among the additional criteria, the presence of enlargement in superior part of the cephalic tract and superior/ inferior part ratio > 1 and unchanged tail antero-posterior diameter after ejaculation showed the same diagnostic accuracy. Overall, both traditional and additional signs for the study of epididymitis are shown to be highly accurate for diagnosis. Finally, the presence of more than two ultrasound signs for each diagnostic category, including both the traditional and additional criteria, makes a very reliable diagnosis with high levels of specicity and sensitivity. Therefore, this study conrms the diagnostic accuracy of ultrasound criteria proposed (Vicari, 1999, 2000; Vicari et al., 2006); in addition it indicates the presence of new criteria which may be added to the previous ones to increase the sensitivity and specicity of the diagnosis with greater objectivity. The scrotal ultrasound evaluation is considered critical in the assessment and clinical management of male infertility (Zahalsky & Nagler, 2001; Vicari et al., 2004a). The role of scrotal ultrasound is aimed mainly at nding non-palpable lesions or the
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Table 2 Comparison of statistical accuracy between all traditional and additional ultrasound signs of prostatitis, vesciculitis and epididymitis US Sign Prostatitis a b c d e f T. signs A. signs Vesciculitis a b c d e f g h T. signs A. signs Epididymitis a b c d e f T. signs A. signs AUC SE 95% CI Accuracy

0.864 0.905 0.870 0.619 0.930 0.925 0.987 0.945 0.824 0.805 0.925 0.860 0.740 0.930 0.875 0.930 0.994 0.993 0.879 0.750 0.925 0.709 0.915 0.945 0.979 0.993

0.0294 0.0266 0.0310 0.0371 0.0236 0.0241 0.00572 0.0234 0.0342 0.0357 0.0241 0.0319 0.0380 0.0236 0.0308 0.0236 0.00295 0.00345 0.0277 0.0378 0.0241 0.0392 0.0257 0.0220 0.00732 0.00320

0.7990.915 0.8460.947 0.8050.919 0.5360.698 0.8760.965 0.8700.962 0.9520.998 0.8960.976 0.7540.882 0.7320.865 0.8700.962 0.7930.911 0.6610.808 0.8760.965 0.8110.923 0.8760.965 0.9651.000 0.9631.000 0.8160.927 0.6720.817 0.8700.962 0.6290.781 0.8580.954 0.8950.976 0.9410.995 0.9631.000

Highly accurate test Highly accurate test Moderately accurate test Low accurate test Highly accurate test Highly accurate test Highly accurate test Highly accurate test Moderately accurate Moderately accurate Highly accurate test Moderately accurate Moderately accurate Highly accurate test Moderately accurate Highly accurate test Highly accurate test Highly accurate test test test test test test

infertility (Jarow, 1993; Brunereau et al., 2000; Yassa & Keesara, 2001). The post-testicular causes include inammation of the male accessory glands and ejaculatory disorders such as anejaculation, hematospermia (Vicari et al., 2004b,c) and painful ejaculation. Since inammation of the prostate and seminal vesicles often tend to be persistent (La Vignera et al., 2008a,b), with consequent impacts on reproductive health and symptoms, it will be of interest to evaluate the ultrasound characteristics once cure has been achieved. References
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AUC, area under curve; SE, error standard; CI, condence interval.

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