Urogenital Tuberculosis

ANDRÉ A. FIGUEIREDO,1 ANTÔNIO M. LUCON,2 and

MIGUEL SROUGI2
1
Núcleo Interdisciplinar de Pesquisa em Urologia and Department of Surgery/Urology,
Federal University of Juiz de Fora, Minas Gerais—Brazil; 2Division of Urology,
University of São Paulo Medical School, São Paulo, Brazil

ABSTRACT Urogenital tuberculosis is the second most frequent spread to the kidneys, prostate, and epididymis; through
form of extrapulmonary tuberculosis. Starting with a pulmonary the descending collecting system to the ureters, blad-
focus, 2 to 20% of patients develop urogenital tuberculosis
der, and urethra; and through the ejaculatory ducts to
through hematogenous spread to the kidneys, prostate,
and epididymis; through the descending collecting system to the
the genital organs (1, 2). Urogenital tuberculosis occurs
ureters, bladder, and urethra; and through the ejaculatory ducts at all age ranges, but it is predominant in males in their
to the genital organs. Urogenital tuberculosis occurs at all age fourth and fifth decades (3). It is a serious, insidious
ranges, but it is predominant in males in their fourth and fifth disease, generally developing symptoms only at a late
decades. It is a serious, insidious disease, generally developing stage, which leads to a diagnostic delay with consequent
symptoms only at a late stage, which leads to a diagnostic delay urogenital organ destruction; there are reports of pa-
with consequent urogenital organ destruction; there are reports tients with renal failure as their initial clinical presenta-
of patients with renal failure as their initial clinical presentation.
tion (3).
Although the condition has been long recognized by
nephrologists, urologists, and infectious disease specialists, Although the condition has been long recognized by
urogenital tuberculosis is still largely unknown. Even when nephrologists, urologists, and infectious disease special-
suggestive findings such as hematuria, sterile pyuria, and ists, urogenital tuberculosis is still largely unknown.

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recurrent urinary infections are present, we rarely remember Even when suggestive findings such as hematuria, sterile
this diagnostic possibility. Greater knowledge of the features pyuria, and recurrent urinary infections are present,
of urogenital tuberculosis then becomes relevant and should we rarely remember this diagnostic possibility. Greater
emphasize the importance of an early diagnosis.
knowledge of the features of urogenital tuberculosis then
becomes relevant and should emphasize the importance
of an early diagnosis.
INTRODUCTION
Tuberculosis has a worldwide distribution, without cy-
clical or seasonal variations and with greater prevalence EPIDEMIOLOGY
in regions of high population densities and poor socio- Extrapulmonary tuberculosis occurs in 10% of tuber-
economic and sanitary status. It is estimated that 30% of culosis cases. Urogenital tuberculosis is responsible for
the world’s population (1.7 billion people) are carriers of 30 to 40% of extrapulmonary tuberculosis cases, second
Mycobacterium tuberculosis (1). In spite of the avail-
ability of pharmacological treatment and of technological Received: 2 October 2016, Accepted: 9 November 2016,
breakthroughs, the last 3 decades have witnessed a re- Published: 13 January 2017
crudescence of the infection due to the emergence of re- Editor: David Schlossberg, Philadelphia Health Department,
Philadelphia, PA
sistant bacilli, human migration, and the AIDS epidemic. Citation: Figueiredo AA, Lucon AM, Srougi M. 2017. Urogenital
In fact, tuberculosis is still a serious challenge to the world tuberculosis. Microbiol Spectrum 5(1):TNMI7-0015-2016.
public health, chiefly in developing countries (2). doi:10.1128/microbiolspec.TNMI7-0015-2016.
Correspondence: André A. Figueiredo, andreavaresef@gmail.com
Starting with a pulmonary focus, 2 to 20% of patients
© 2017 American Society for Microbiology. All rights reserved.
develop urogenital tuberculosis through hematogenous

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Figueiredo et al.

only to lymph node involvement (2, 4–6). Urogenital ensues, unless there is immunodeficiency and systemi-
tuberculosis occurs in 2 to 20% of patients with pul- cally symptomatic miliary tuberculosis develops, with
monary tuberculosis (5, 7–10). While in developed constitutional symptoms and multiple renal abscesses, as
countries the urogenital cases constitute 2 to 10% of has been seen in AIDS patients (Fig. 1) (1, 7). In fact, 25
cases of pulmonary tuberculosis, the figures are 15 to to 62% of patients with miliary tuberculosis have renal
20% in developing countries (5, 7–9). lesions with multiple bilateral foci (12, 14). The latent
period between pulmonary infection with bacillemia
and clinical urogenital tuberculosis is 22 years on aver-
ETIOPATHOGENESIS age, ranging from 1 to 46 years, according to the mo-
Mycobacterium tuberculosis, an acid-fast aerobic ba- ment when immunity falls and the latent renal foci are
cillus, is the most virulent mycobacterial pathogen in reactivated (8).
humans. Its slow replication accounts for the insidious After reactivation of the renal foci, infection prog-
nature of the infection and its resistance to ordinary resses from a single focus, affecting one kidney and
antibiotics, since the latter work during bacterial divi- sparing the other (13). This accounts for the greater
sion. Although the bacillus can stay dormant in the host, frequency of unilateral renal tuberculosis (Fig. 2) (8, 15).
not producing symptoms for a long time, reactivation Contiguous involvement of the collecting system leads to
may follow impairment of immunity (2). Other myco- bacilluria and descending unilateral spread to the ureter
bacteria, such as Mycobacterium bovis, important where and bladder. In ureteral tuberculosis, multiple stenoses
unpasteurized milk is consumed (4), are less virulent to develop throughout the ureter, with ureteral obstruc-
humans and are only rarely responsible for urogenital tion, ureterohydronephrosis, and consequent risk of re-
lesions. nal functional loss. With infection progression, there is
Once inhaled, the bacilli multiply in the pulmonary bladder damage with progressive fibrosis characterizing
alveoli, with primary granuloma formation (1, 2). As a more advanced form known as contracted bladder
few as one to five bacilli in the alveolus may result in (Fig. 3 and 4) (16). Progression of bladder tuberculosis
infection. Primary pulmonary tuberculosis is usually reduces bladder capacity and compliance, with distor-
clinically silent and self-limited. From this pulmonary tion of the ureterovesical junctions and development
focus, bacillemia ensues and leads to bacillus implants of vesicoureteral reflux; the reflux almost always in-
in other organs. At this point, colonization of the renal volves only the initially spared kidney, since ureteral
and prostate parenchyma may occur. After 6 months, stenosis protects against the radiological manifestation
spontaneous cicatrization of primary pulmonary tuber- of reflux. Reflux which is secondary to a contracted
culosis occurs, and the patient enters a latent phase, bladder transforms the collecting system (ureter and

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with a 5% likelihood of disease reactivation in the fol-
lowing 2 years and a 5% additional likelihood of re-
activation thereafter. In most active cases of both FIGURE 1 Post-contrast phase of abdominal computed to-
pulmonary and extrapulmonary disease, latent foci are mography (CT) in an AIDS patient, with bilateral renal ab-
reactivated by malnutrition, diabetes mellitus, steroid scesses and dilatation of the collecting system on the right.
and immunosuppressant use, and immunodeficiency (1, Retroperitoneal lymph node enlargement with central ne-
11). crosis is apparent (arrow). From reference 27, with permission.
In the pathophysiology of urogenital tuberculosis,
there is gradual development of the initial forms, from
minimal urogenital damage and few symptoms to severe
disease with contracted bladder, bilateral renal injury,
and possible end-stage renal failure (3). A clear under-
standing of this course is paramount to highlight the
importance of early diagnosis. After hematogenous
spread from the pulmonary focus, there is colonization
of the renal parenchyma, with initially bilateral, corti-
cal, glomerular, and pericapillary renal lesions that are
concomitant with other hematogenic foci in the prostate
and other organs beyond the urogenital system (12,
13). These foci generally cicatrize, and a latent period

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FIGURE 2 Magnetic resonance imaging (A) and CT (B and C) of patients with unilateral
renal tuberculosis, with dilatation of the collecting system (caliectasis) and thinning of
the renal parenchyma. There is no dilatation of the renal pelvis. From reference 27, with
permission.

pyelocaliceal junction) into an extension of the capacity (first kidney to be involved) and by high-degree vesico-
of the contracted bladder, with ascending transmission ureteral reflux on the other (second kidney to be in-
of intravesical pressure (16). Unidentified and untreated volved), pointing to secondary loss of function of one
reflux damages the kidney through infection or trans- of the kidneys because of vesicoureteral reflux (Fig. 3
mission of intravesical pressure, leading to end-stage and 4). Thus, if diagnosis and treatment do not occur at
renal failure. In a study of 25 cases of tuberculosis- the initial stages of the infection, urogenital tuberculosis
related contracted bladder (16), the patients with may severely damage the urogenital organs, from uni-
bilateral renal tuberculosis had bilateral ureterohydro- lateral renal loss to contracted bladder-related end-stage
nephrosis caused by ureteral obstruction on one side renal failure.

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FIGURE 3 Sequential exams of patient with urogenital tuberculosis. (A) Initial intravenous urography (IU) with right kidney
dysfunction and normal left kidney and bladder. (B) IU after 10 months, with development of contracted bladder and
ureterohydronephrosis on the left. (C) Voiding cystography showing high-grade vesicoureteral reflux on the left as a cause of
dilatation of the collecting system. From reference 27, with permission.

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FIGURE 4 Sequential exams of a patient with urogenital tuberculosis. (A) Initial IU with normal right kidney and left kidney with
ureterohydronephrosis due to stenosis of the middle ureter (arrow) and intrarenal stenoses without pelvic dilatation (typical
tuberculosis feature). (B) Cystography with normal bladder and no reflux. (C and D) IU and voiding cystography after 6 months
without treatment, showing renal dysfunction on the left and ureterohydronephrosis on the right, with contracted bladder
and bilateral vesicoureteral reflux (high grade on the right) as a cause of ureterohydronephrosis. From reference 27, with
permission.

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AFFECTED ORGANS tuberculosis. (iii) The third is unilateral renal involve-

Tuberculosis may affect the entire male urinary and ment, with descending spread to the ipsilateral ureter
genital tracts. Table 1 shows the frequencies of male and bladder and then retrograde spread to the contra-
urinary and genital tract involvement (8, 15, 17). lateral kidney through reflux (16). The last is the main
Urogenital tuberculosis most frequently affects the mechanism of bilateral renal damage in tuberculosis.
kidneys, renal infection being slowly progressive, Accordingly, bilateral renal damage in tuberculosis
asymptomatic, and highly destructive, with instances is generally asymmetric, with one of the kidneys more
of unilateral renal loss of function and renal failure severely damaged (multiple stenoses of the collecting
on diagnosis (18). Kidney destruction might be due to system and asymmetric calyceal dilatation), whereas the
progression of a focal lesion, with caseous granuloma other kidney is less involved, with reflux-related ure-
formation, fibrosis, and renal cavitation. Yet obstruction terohydronephrosis (16). There is a rare subset of pa-
of the collecting system, which may be distal when due tients with bilateral renal tuberculosis who may develop
to ureteral stenosis or proximal when there are intra- acute or chronic renal failure with histological findings
renal stenoses, is the main cause of tuberculosis-related of diffuse interstitial nephritis, with or without granu-
renal dysfunction (6, 19, 20). loma formation but without radiological findings sug-
Although unilateral renal involvement predominates gestive of tuberculosis, except for renal atrophy in some
in tuberculosis (8, 15), bilateral damage may occur, with cases. These cases differ from the classic clinical and
risk of renal failure. Bilateral renal tuberculosis may be radiological presentations of urogenital tuberculosis,
due to three mechanisms. (i) The first is exacerbation of since voiding symptoms and radiological alterations are
the hematogenous spread period, with the formation of not prominent, and the bacillus can rarely be found in
multiple predominantly bilateral parenchymatous foci, the urine. Diagnosis is generally made on histopathology
seen in patients with immunodeficiency and miliary tu- of a sample obtained through renal biopsy (23, 24).
berculosis (Fig. 1) (12). (ii) The second is bilateral focus Ureteral and bladder tuberculosis involvement is
reactivation with progressive descending spread to the secondary to renal disease and consequent descending
collecting system and bilateral ureteral stenoses, without infection through the collecting or lymphatic system.
the presence of a contracted bladder. This presentation Descending lymphatic spread was demonstrated in pigs
is extremely rare: Conte et al. (21) describe a patient which received direct renal inoculation of the bacillus
with postrenal renal failure due to tuberculosis-related and developed ureteral tuberculosis even after total
bilateral stenosis of the collecting system, which resolved occlusion of the ureter (25). In ureteral tuberculosis,
after specific treatment, and Chattopadhyay et al. (22) multiple stenoses develop throughout the ureter, with
describe a case of right autonephrectomy due to ob- predominance of the anatomical narrowings such as the

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struction associated with infundibular stenosis of the vesicoureteral junction and, to a lesser extent, the ure-
contralateral kidney. In both cases, there was no bladder terorenal junction and the mid-ureter (4, 18). Ureteral

TABLE 1 Frequency of affected urogenital organs

Findings in indicated study

Christensen, 1974, García-Rodríguez et al., Mochalova and Starikov,

Affected organ United States (8) 1994, Spain (15) 1997, Russia (17)
Total no. (no. of men) 102 (72) 81 (51) 4,298 (2,888)
Kidney (%) 60.8 93.8 100
Bilateral (%) 29 14.5 83.4
Unilateral (%) 71 85.5 16.6
Ureter (%) 18.6 40.7 NRa
Bladder (%) 15.7 21 10.6
Prostateb (%) 26.4 2 49.5
Epididymisb (%) 22.2 11.8 55.5
Seminal vesicles (%) 6.9 0 NR
Urethra (%) 1.4 2 21.4

NR, not reported.

a

In relation to male patients.

b

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stenosis is the main cause of renal dysfunction in tu- regions of rabbits was observed to lead to tuberculous
berculosis, occurring in up to 93.7% of all cases (4). prostate foci concomitant with foci in other organs,
As previously stated, bladder tuberculosis is second- and discrete renal foci without communication with the
ary to kidney tuberculosis through descendant urinary urinary collecting system. In the clinical cases, the pros-
dissemination. Although urogenital tuberculosis has no tate lesion was not accompanied by mucosal or sub-
initial specific symptoms or radiological findings, blad- mucosal impairment of the prostatic urethra, being
der tuberculosis has a highly specific clinical and radio- situated instead in the lateral and peripheral regions,
logical finding: the contracted bladder. In a review of while urethral ulcerative lesions with prostate involve-
published series of urogenital tuberculosis, contracted ment were seen only in more advanced cases with vesical
bladder was found in 8.9% of urogenital tuberculosis tuberculosis (Fig. 5) (32). In prostatic tuberculosis, there
cases, but at differing rates in developed (4.0%) and is caseous necrosis with calcification and development
developing (13.6%) countries (26). Radiologically, con- of fibrosis with gland hardening (33). Prostatic tuber-
tracted bladder presents with diffuse thickening of the culosis is usually asymptomatic and diagnosed as an
bladder wall, without trabeculations or diverticulous incidental prostatectomy finding in patients older than
bladder. The vesicoureteral junction is located in the those with urogenital tuberculosis (33–35). Prostatic
lateral upper part of the bladder, and it looks like all abscesses are rare but occur in AIDS patients (36).
bladder has contracted but the bladder trigone (27) The epididymis is affected in 10 to 55% of men with
(Fig. 4). Clinically, the patient presents with high uri- urogenital tuberculosis, and scrotal changes are the main
nary frequency, with average urinary diurnal frequency sign on physical examination (8, 11, 15, 17). Epididymal
less than 20 min and bladder capacity of less than tuberculosis is bilateral in 34% of the cases, presenting
100 ml. Sometimes incontinence develops. The presence as a nodule or scrotal hardening in all patients, scrotal
of contracted bladder represents an advanced urogenital fistula in half the cases, and hydrocele in only 5% (37).
tuberculosis infection (16). The presence of a scrotal fistula is a telltale sign of tu-
In spite of constant urethral exposure to the urinary berculosis.
bacilli, urethral tuberculosis occurs in only 1.9 to 4.5% Because of ejaculatory duct obstruction with oligo-
of all cases of urogenital tuberculosis, and never as an azoospermia and low-volume ejaculate due to obstruc-
isolated entity. Acute urethritis and urethral discharge tion of the ejaculatory ducts, infertility may be the first
with associated prostatic tuberculosis, or chronically symptom of tuberculosis. Multiple stenoses in the ejac-
developing urethral stenosis and fistulae, are the most ulatory duct system make reconstruction impossible and
common clinical presentations (28, 29). are an indication for assisted reproduction (4, 30, 38).
Tuberculosis affects the entire male genital tract, with Leukospermia is a less frequent and earlier mechanism

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lesions in the prostate, seminal vesicles, vas deferens, underlying tuberculosis-related infertility (30).
epididymis, Cooper glands, penis, and testicles, the last
through contiguity with the epididymis, since the blood-
testicle barrier plays a protective role. Genital tuber- FIGURE 5 Voiding urethrocystography showing contracted
bladder, no vesicoureteral reflux, and prostate tuberculosis,
culosis occurs through hematogenous spread to the
with dilatation and irregularities of the prostatic urethra. From
prostate and epididymis or through the urinary system reference 27, with permission.
to the prostate and spread from the ejaculatory ducts
to the seminal vesicles, vas deferens, and epididymis (30,
31). Genital tuberculosis may be accompanied by renal
lesions, but it may manifest in isolation (3). The fre-
quency of genital organ involvement varies according to
the criteria used. The prostate is histologically involved
in 39.5 to 50% of subjects with urogenital tuberculosis,
while epididymitis is the most common clinical mani-
festation, because prostate tuberculosis is usually sub-
clinical (12, 14, 17).
In prostate contamination, hematogenous spread is
more frequent than through the urinary system (32). In
an experimental and clinical observational study, bacil-
lus injection in the subcapsular and intracortical renal

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Penile tuberculosis is rare, developing after direct Pharmacotherapy is the mainstay of treatment for
contact or secondary to another urogenital focus, with female genital tuberculosis, surgery being reserved for
the appearance of an erythematous papule that may voluminous tubo-ovarian abscesses. Pharmacotherapy
ulcerate. Infiltration of the cavernous bodies may lead to and tubal surgery do not restore fertility; assisted re-
penis deformity and urethral fistulae, a situation that production, chiefly in vitro fertilization with embryo
may be confused with penile carcinoma (39, 40). transfer, is indicated in such cases. Yet there is anecdotal
evidence of parity after treatment of tubal tuberculosis
(41, 42).
FEMALE GENITAL TUBERCULOSIS Vertical transmission of tuberculosis is very rare, with
The incidence of female genital tuberculosis ranges from 358 cases described until 1995 and only 18 cases de-
0.002 to 0.56% among hospitalized women and from scribed between 2001 and 2005. It may occur through
0.2% to a relevant 21% among those with infertility. transplacental transmission, through umbilical veins to
The condition affects women of childbearing age, with a the fetal liver and lungs, or by aspiration or swallowing
predominance in the 20- to 40-year age range (41, 42). of infected amniotic fluid. The exact risk of vertical
Female genital tuberculosis is secondary to hema- transmission in female tuberculosis is not known; how-
togenous spread from a primary focus, generally in the ever, meningeal, extrapulmonary, and miliary tubercu-
lungs or, less commonly, through lymphatic spread from losis are high risk factors. Mothers who have completed
tuberculosis of abdominal organs. However, primary antitubercular treatment and even those with at least 2
genital tuberculosis might develop after sexual inter- weeks’ duration before delivery are less likely to transmit
course with a man with tuberculosis of the penis or ep- the disease to the newborn than are untreated mothers.
ididymis. After initial involvement of the fallopian tube, Therefore, isoniazid prophylaxis to the neonate is re-
the infection may involve the endometrium and, more commended if the mother has received treatment for less
rarely, the myometrium, reaching the ovarian cortex than 2 weeks (43).
through contiguity. The fallopian tubes are affected in
90 to 100% of the cases, normally in a bilateral fashion,
with a predominance of lesions in the ampulla (greater CLINICAL FEATURES
vascular supply), followed by the isthmus. In 50 to 70% In a recent review (26) of 9,178 patients described in
of the cases, there is a uterine lesion with a predomi- 39 case series (6 in Latin America, 7 in Africa, 14 in Asia,
nance of endometrial lesions, the myometrium being 4 in the United States, and 8 in Europe), urogenital tu-
more rarely affected. Ovarian tuberculosis is usually a berculosis was seen to affect two males to each female,
sequela of tubal tuberculosis, when tubo-ovarian masses with a mean age of 40.7 years (range, 5 to 90 years).

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develop. Vulvar or vaginal tuberculosis is exceedingly In only 36.5% of the cases was there clinical history or
rare (41, 42). radiological evidence of previous tuberculosis. There-
Genital tuberculosis generally presents clinically as fore, in most cases, urogenital tuberculosis cannot be
infertility (40 to 76%), pelvic or abdominal pain (50 suspected on the basis of a history of previous pul-
to 55%), and menstrual disorders (20 to 25%). Infer- monary disease. Symptoms arise when there is bladder
tility is the main manifestation of the disease, resulting impairment, once, as far as tuberculosis is concerned, the
from tubal obstruction or the presence of adhesions kidneys are mute while the bladder plays the role of the
and synechiae of the uterine cavity. On radiology, hys- vocal cords (9). Storage symptoms (frequency, nocturia,
terosalpingography may show findings suggestive of tu- and urgency) are thus the most common manifestations,
berculosis: obstruction of the fallopian tube, multiple followed by hematuria and low back pain, occurring in
constrictions along the fallopian tube, and adhesion, 50.5, 35.6, and 34.4% of cases, respectively. On phys-
deformity, and obliteration of the uterine cavity without ical examination, up to 48.9% of subjects have some
previous history of curettage. A pelvic mass mimicking scrotal abnormality, with a lump, epididymal hardening,
an ovarian tumor may develop in genital tuberculo- or fistula, which points to the importance of these signs
sis. Histopathological diagnosis may be made after (Table 2).
uterine curettage or biopsy of the fallopian tube. Culture Autopsy studies revealed that only 50% of the pa-
of menstrual fluid is also feasible. Yet, when there is a tients with renal tuberculosis were symptomatic, with
suspicion of tuberculosis on clinical and radiological only 18% having received a clinical diagnosis (12). This
grounds alone, treatment may be started, even without diagnostic delay is due to the insidious progression of
histological or bacteriological confirmation (41, 42). the disease, paucity and nonspecificity of symptoms,

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TABLE 2 Comparison of patients from developed and developing countriesb

Value for developed Value for developing

Feature or parameter Total value countries countries P valuea
No. of patients 9,178 3,048 1,832
% Men 64.8 62.9 60.6 0.02
% Women 35.2 37.1 39.4 0.02
Age (yrs)
Median 40.7 42.7 39.8
Range 5–90 7–90 5–83
% with previous tuberculosis 36.5 37.9 49.1 <0.01
% with symptoms and signs
Storage symptoms 50.5 44.3 55.2 <0.01
Hematuria 35.6 24.5 44.3 <0.01
Lumbar pain 34.4 28.7 42.3 <0.01
Scrotal mass 48.9 20.6 25.0 0.19
Fever and malaise 21.9 23.2 19.9 0.28
No urinary symptoms 6.4 8.4 0 <0.01
% with diagnosis by the following
Urine 64.2 79.0 55.4 <0.01
Histopathology 21.9 7.8 38.3 <0.01
Clinico-radiographic 10.4 9.6 11.3 0.36
% with normal kidneys 15.2 18.9 13.2 <0.01
% with unilateral nonfunctioning kidney 26.9 22.7 33.3 <0.01
% with renal failure 7.4 1.9 13.6 <0.01
% with contracted bladder 8.6 4.0 13.6 <0.01
% with surgery 54.9 56.6 50.0 <0.01
% with ablative surgery 27.2 35.0 43.7 <0.01
aP, significance level through chi-square test.
bFrom reference 26, with permission.

lack of physicians’ awareness, poor care-seeking be- pyuria with negative urine cultures (sterile pyuria), he-
havior, and difficult bacteriological diagnosis because maturia, and epididymo-orchitis are findings suggestive
of sporadic bacilluria with few organisms (6, 10). of urogenital tuberculosis in the pediatric population
Therefore, diagnosis is rarely made before severe uro- (22).

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genital lesions develop (3). A total of 7.4% of patients
with urogenital tuberculosis develop end-stage chronic
renal failure (Table 2). IMMUNOSUPPRESSION
Comparison of the disease features between develop- Immunosuppression favors the development of tuber-
ing countries and developed ones (with the exception of culosis, which, in these cases, has a unique course, with
Russia, which has intermediate characteristics) shows greater risk of hematogenous spread and extrapulmo-
significant differences. Patients from developing countries nary tuberculosis (44). AIDS is now the main factor
are more likely to have specific symptoms and receive leading to tuberculosis development. Besides reactivating
late histological diagnoses. In such countries, tuberculosis latent foci, human immunodeficiency virus (HIV)-related
is consequently more severe, with a greater frequency of immunosuppression may lead to rapid progression of
renal failure, unilateral renal obstruction, ablative sur- a new infection or reinfection (44). Between 20 and 50%
geries, and contracted bladder and a lower frequency of HIV-infected patients worldwide have active tuber-
of normal upper collecting systems (Table 2). These data culosis (45, 46). Urogenital tuberculosis seems to be very
underlie the relationship between the severity of uro- important in AIDS patients. In the United States, of
genital tuberculosis and the timing of the diagnosis. 1,282 tuberculosis patients seen between 1991 and 1997
Although urogenital tuberculosis affects all age ranges, in an inner-city hospital, 46% were coinfected with HIV,
there are few cases in children because of the long interval and, among the patients with urogenital tuberculosis,
between pulmonary infection and renal tuberculosis (3). two-thirds had AIDS (47). In autopsy studies of 46 AIDS
Recurrent urinary tract infection or urinary tract infec- patients in Brazil, 54.3% had tuberculosis, with the
tion that does not respond to conventional antibiotics, disseminated form as the most frequent presentation,

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whereas an astounding 23.9% of AIDS patients had comparison of 72 nonimmunosuppressed patients with
bilateral renal granulomas (45). HIV-positive patients urogenital tuberculosis and eight immunosuppressed
with tuberculosis are younger, have more constitutional patients (four with AIDS and four post-renal transplant),
symptoms (fever, bacteremia, and fatigue), show more the latter had a predominance of constitutional symp-
diffuse pulmonary involvement, develop lymph node toms, disseminated tuberculosis, and multiple parenchy-
enlargement and disseminated tuberculosis more fre- matous renal foci, with a lower frequency of involvement
quently, and have higher mortality rates than do HIV- of the collecting system (Table 3). Therefore, immu-
negative subjects (44). Regarding urogenital tuberculo- nosuppressed patients develop a form of urogenital tu-
sis, HIV-positive patients are younger and more prone berculosis that has distinctive clinical and radiological
to developing kidney and prostate abscesses (47). features, resembling severe bacterial infection, with bac-
From 0.5 to 4.0% of patients with post-renal trans- teremia and visceral metastatic foci (50).
plant immunosuppression develop tuberculosis in de-
veloped countries; these figures rise to 3.8 to 11.8% in
developing countries (48, 49). In transplant patients, LABORATORY AND
pleuropulmonary and disseminated tuberculosis are RADIOLOGICAL WORKUP
more common, although urogenital tuberculosis may For around 10.4% of patients with urogenital tubercu-
predominate in developing countries (48, 49). Post-renal losis, diagnosis is presumptive and based on suggestive
transplant patients with urogenital tuberculosis present clinical, laboratory, and radiological data, without mi-
clinically with fever and without voiding symptoms in crobiological or histological confirmation (26).
two-thirds of cases, and without typical radiological Identification of the tuberculosis bacillus in the urine
findings in the renal graft. Contrasting with the classic is achieved through Ziehl-Neelsen’s acid-fast staining
cases of urogenital tuberculosis, only around 20% of technique or through urine culture in Lowenstein-Jensen
these patients have voiding symptoms (48, 49). In a medium (24, 45). The former is quick, with 96.7%

TABLE 3 Features of immunocompromised and nonimmunocompromised patients with urogenital tuberculosisa

Value for immunocompromised

Value for patients with the following:
nonimmunocompromised
Feature patients AIDS Transplantation P value
No. 72 4 4

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Median age (yrs) 35 26 51.5
% with symptoms and signs
Storage symptoms 76.4 37.5 0.033
Hematuria 58.3 37.5 0.288
Lumbar pain 30.6 25.0 1.000
Fever 43.1 87.5 0.024
Scrotal mass 22.0 0.0 0.591
No urological symptoms 5.6 37.5 0.019
% with duration of symptoms of <6 mo 2.8 87.5 <0.001
% with previous tuberculosis 26.4 25.0 1.00
% with disseminated tuberculosis 18.1 62.5 0.012
% with diagnosis by the following
Urine 50.0 50.0 1.000
Histopathology 33.3 50.0 0.441
Clinico-radiographic 16.7 0.0 0.599
% with cortical kidney lesions 6.2 87.5 <0.001
Bilateral 3.1 37.5 0.008
Unilateral/grafted 3.1 50.0 0.001
% with excretory kidney lesions 93.8 12.5 <0.001
Bilateral 37.5 12.5 0.248
Unilateral 56.3 0.0 0.005
% with contracted bladder 65.3 12.5 0.001
Mortality (%) 4.2 12.5 0.350
aFrom reference 50, with permission.

10 ASMscience.org/MicrobiolSpectrum
 Urogenital Tuberculosis

specificity but only 42.1 to 52.1% sensitivity (51, 52). Cystoscopy with biopsy is a low-morbidity proce-
Culture is the diagnostic gold standard for urogenital dure that may be performed when there is clinical
tuberculosis. Because bacilluria is sporadic and faint, suspicion of tuberculosis and bacillus-negative urine
three to six early morning midstream samples are re- culture, being more useful in the acute phase. The most
quired. Sensitivity varies widely, from 10.7 to 90%, frequent findings are local hyperemia, mucosal erosion
and the results can take 6 to 8 weeks to be obtained (3, and ulceration, tubercle formation, and irregularity of
10). the ureteral meatuses. Vesical biopsy is only 18.5 to
Some findings in urine examination, such as pyuria, 52% sensitive, though (10, 55).
hematuria, acid urine, and negative culture, suggest that Imaging techniques are up to 91.4% sensitive for uro-
urogenital tuberculosis may be present in up to 93% of genital tuberculosis diagnosis, with intravenous uro-
patients (3). Yet the suspicion of tuberculosis should not graphy and abdominal computerized tomography being
be based on these findings alone, because alterations in used more (10). Findings suggestive of urogenital tuber-
the urine have been described in only 22 to 27.6% of culosis are calyceal irregularities; infundibular stenosis;
cases (42, 53). Usual pathogens are yielded by urine pseudotumor or renal scarring; renal loss of function;
culture for 20 to 40% of urogenital tuberculosis cases renal cavitation; urinary tract calcification (present in
and for up to 50% of females (3). 7 to 19% of the cases); collecting system thickening,
PCR for Mycobacterium tuberculosis identification stenosis, or dilatation; contracted bladder; and lesions
in the urine, a highly sensitive and specific technique in in other sites beyond the urinary tract, such as lymph
which small bits of genetic material are amplified, has nodes, spleen, liver, and vertebrae (3, 10, 27). The
become the ideal diagnostic tool, as it gives results in simultaneous finding of kidney and bladder lesions is
24 to 48 h and allows for the diagnosis to be made characteristic of tuberculosis, and the earliest findings
even when there are few bacilli, features that make it a are outline irregularity and calyceal dilatation due to
potentially ideal method for the diagnosis of urogeni- infundibular stenosis (10).
tal tuberculosis (10, 52). Compared to culture, it was Multiple stenoses of the collecting urinary system
95.6% sensitive and 98.1% specific (52). Compared to from the renal pelvis to the ureterovesical junction are
bacteriological, histological, or clinico-radiological di- the findings most suggestive of urogenital tuberculosis,
agnoses, it was 94.3% sensitive and 85.7% specific (10). occurring in 60 to 84% of cases (27). In spite of this
Yet in a systematic review including the analysis of variability, urogenital tuberculosis involves the urinary
new PCR tests for the diagnosis of urogenital tubercu- tract in a sequential pattern as described above. After
losis, specificity was high but sensitivity was variable. unilateral renal and ureteral involvement, with thicken-
In spite of the potential role of PCR in the diagnosis ing and stenosis of the collecting system leading to

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of urogenital tuberculosis, there is no present evidence hydronephrosis and renal parenchyma atrophy, there
supporting the diagnosis of the condition without cul- may be bladder damage, with diffuse thickening of the
ture confirmation (54). bladder walls and development of vesicoureteral reflux,
Intradermal injection of tuberculin, a tuberculosis usually unilaterally to the as-yet-undamaged kidney.
bacillus-derived purified protein, leads to a late hyper- High-grade reflux may lead to ureterohydronephrosis,
sensitivity-like local inflammatory reaction with hard reflux nephropathy, and end-stage renal failure (16).
nodular formation after 48 to 72 h. Patients are classi- Phases in the urogenital involvement of tuberculosis
fied according to the induration diameter as nonreactors can then be characterized. Radiological investigation of
(below 5 mm), weak reactors (between 5 and 10 mm), 20 patients with urogenital tuberculosis showed four
and strong reactors (over 10 mm). The exam is not di- types of presentation (27): (i) bilateral renal tuberculosis
agnostic, though, once M. bovis BCG-vaccinated sub- with predominance of parenchymatous involvement
jects are reactors; further, when a nonvaccinated subject (Fig. 1); (ii) unilateral renal tuberculosis without vesical
reacts, this merely indicates previous contact with the or contralateral renal involvement (Fig. 2); (iii) unilateral
bacillus. Yet when a previously weak reactor becomes renal tuberculosis and contracted bladder, with a ra-
a strong one, it indicates recent infection (1, 2). The diologically normal contralateral kidney; and (iv) bi-
tuberculin test may contribute to the diagnosis of uro- lateral renal tuberculosis and contracted bladder, with
genital tuberculosis in countries without widespread unilateral renal dysfunction and ureterohydronephrosis
BCG vaccination, a situation in which the test is positive of the contralateral kidney due to high-grade reflux.
in 85 to 95% of patients with urogenital tuberculosis In two of these patients disease progress was radiologi-
(5, 14). cally demonstrated (Fig. 3 and 4). Understanding these

ASMscience.org/MicrobiolSpectrum 11
Figueiredo et al.

phases is important for early diagnosis, when such com- asymptomatic phase of relapse (9, 62–64). The devel-
plications and more complex reconstructive surgery may opment of antimicrobial resistance, caused by too short
be avoided. a treatment regimen (up to 60% of the patients), is one
Epididymal tuberculosis presents on ultrasonography of the factors responsible for tuberculosis recrudescence
as a hypoechoic lesion involving the whole epididymis (2).
or just its head, with a heterogeneous texture and con- Pharmacological treatment may cure small renal foci
comitant testicular involvement in 38.9% of the cases and unblock the collecting system (3, 62). Nevertheless,
(56). it has been known since the 1970s that pharmacological
treatment may aggravate the renal lesions just a few
weeks after its start, with fibrosis leading to obstruc-
PHARMACOLOGICAL TREATMENT tion of the collecting system and vesical contraction and
The pharmacological treatment of urogenital tuberculo- with worsening of frequency and development of renal
sis should be started after microbiological or histological dysfunction (5, 18, 63). Therefore, the placement of a
diagnosis has been made and even before diagnostic double J stent, to prevent worsening obstruction and
confirmation, when clinical, laboratory, and radiological consequent renal dysfunction, must be considered dur-
data warrant a presumptive diagnosis (57). Bactericidal ing the pharmacological treatment of patients with
(e.g., isoniazid, rifampin, pyrazinamide, and strepto- ureteral stenosis.
mycin) and bacteriostatic (e.g., ethambutol and ethion-
amide) drugs are used (1–3). Since there is 80% relapse
with a single drug, 25% with two drugs, and 10% with SURGICAL TREATMENT
a triple regimen (5), the most conservative approach is Over half (54.9%) the patients with urogenital tuber-
to initiate a four-drug regimen, i.e., isoniazid, rifampin, culosis undergo surgery, a figure that ranges from
pyrazinamide, and ethambutol or streptomycin. After 8 to 95%, according to the timing of diagnosis (26). In
2 weeks of treatment, no bacilli can be identified in the the series where surgery was less frequent, the patients
urine (2). Although the optimal treatment duration has were diagnosed when still asymptomatic, with lower
not been defined, shorter-term treatments have replaced rates of renal lesions (26). On the other hand, when the
the traditional 18- and 24-month treatments formerly diagnosis is delayed, the silent progression of the disease
recommended, and infection with susceptible organisms leads to organ destruction, with a greater frequency of
can usually be managed with regimens suitable for pul- surgical interventions (26).
monary tuberculosis as discussed elsewhere. Shorter- Surgery may be ablative, with removal of the
term regimens are justified because of the good renal tuberculosis-destroyed kidney or epididymis, or recon-

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vascularization, high urinary concentration of the drugs structive for unblocking the collecting system or aug-
used, low bacillary load in the urine, lower cost and menting the contracted bladder (2, 65). The last decades
toxicity, higher compliance, and efficacy similar to that have witnessed a decrease in the number of ablative
of longer-duration regimens (47, 58). Four- to six-month surgeries and an increase in the number of reconstructive
treatments with nephrectomy of the excluded kidney ones (66). The patient should be operated on after at
have afforded relapse rates lower than 1% (57, 59, 60). least 4 to 6 weeks of pharmacological treatment (2, 3,
Malnutrition and poor social conditions warrant treat- 63).
ment for longer than 9 months, as relapse rates may be Most authors recommend nephrectomy without ure-
as high as 22% after a 6-month regimen and 19% after terectomy in cases of unilateral renal dysfunction to
1 year (9, 61). avoid relapse, eliminate irritative voiding symptoms,
Microbiological relapse of urogenital tuberculosis treat hypertension, and avoid abscess formation (18, 35,
may occur after initial urine sterilization, even after 57, 62, 63). Systemic arterial hypertension is more fre-
prolonged treatment and nephrectomy of the excluded quent in patients with urogenital tuberculosis in whom
kidneys (9, 62, 63). Relapses occur in up to 6.3% of the unilateral renal dysfunction develops; nephrectomy can
cases after a mean of 5.3 years of treatment (range, 11 be curative of this condition in up to 64.7% of the cases
months to 27 years) with bacilli that are sensitive to the (62). Relapse is more likely when a nonfunctioning kid-
drugs initially used (61, 64). Most authors recommend a ney is not removed, because the pharmacological treat-
10-year follow-up period after pharmacological treat- ment may not sterilize all tuberculous foci, viable bacilli
ment, because of the possibility of late relapse and the having been identified in kidneys from 8 weeks to 9
advantage of early treatment of initial lesions in the months of treatment (6, 62, 63). Conversely, after moni-

12 ASMscience.org/MicrobiolSpectrum
 Urogenital Tuberculosis

toring 35 patients for up to 22 years without any com- self-catheterization. In 85.8% of cases, patients can void
plication, some authors recommend kidney preservation after surgery, and this figure improves to 94.2% after
if there is no pain, infection, or bleeding (53, 67). another surgery for desobstruction, such as transure-
Urinary collecting system obstruction is the main thral prostate resection. In two series (16, 73), uro-
cause of kidney loss of function, the likelihood of renal dynamic evaluation after surgery was performed. The
function recovery in this situation being low (53). In pressure flow studies have shown that all patients void
selected cases of severe renal function reduction, how- through the voluntary increase of abdominal pressure
ever, urinary diversion may preserve these kidneys for (Valsalva’s maneuver). However, in some cases Valsalva’s
later reconstruction (6). The positive prognostic factors maneuver occurred during the involuntary contraction
for functional recovery of obstructed kidneys are distal and the patient used this contraction to void. In cysto-
ureteral stenosis, cortical thickness greater than 5 mm, metry, involuntary contractions occur in 72% of cases
and glomerular filtration rate above 15 ml/min, as as- and are not associated with worsening capacity (16).
sessed by the nephrostomy output or renal scintigraphy Rhythmic bowel contractions are triggered by wall dis-
(6, 63). On the other hand, intrarenal stenoses almost tension and seem to persist after bladder augmentation.
always lead to renal dysfunction (18). In the rare in- Worse results were associated with reservoir with small
stances in which an early diagnosis is made, percutane- capacity but not with the presence of involuntary con-
ous nephrostomy is 80% successful, and a segment of tractions (16).
ileum may be interposed between the bladder and the In an impressively large urogenital tuberculosis series
dilated calices (68, 69). with description of 4,298 patients in Russia (17) pub-
Ureteral stenosis is treated with dilatation or endo- lished in 1997, bladder augmentation with sigmoid had
scopic incision, with a 50 to 90% success rate, or with been performed in 426 patients since 1960. The authors
reconstructive surgery (2, 18). propose, after describing frequent stenosis of intestine-
bladder anastomoses, the realization of cystoprosta-
Surgery for Contracted Bladder tectomy with orthotopic neobladder with cecum with
Among 316 patients in 11 series of surgery for tuber- uretero-ileal anastomosis and invagination of the ap-
culous contracted bladder (16–18, 70–78), 64% were pendix into the remaining part of the urethra. Due to a
men and the median age was between 30 and 40 years. lack of more detailed data, no conclusion can be made
Bladder augmentation was performed in 90% of the with regard to that proposal.
cases and orthotopic neobladder in 10%. In only three In conclusion, the aims of contracted bladder surgical
exceptional cases, a cutaneous urethrostomy was done treatment are (i) improvement of quality of life through
(71). Among bladder augmentation, ileum was used in incontinence treatment and restoration of a reasonable

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35.4% of cases, with detubularization in all but in some urinary interval and (ii) preservation of the upper uri-
cases from the two oldest series in 1969 and 1970. Sig- nary tract by lowering the bladder pressure. Therefore,
moid was used in 38.9%, with detubularization in al- a low-pressure, high-capacity reservoir must be created
most all cases and the ileocecal segment used in 25.8%, through a bladder augmentation or an orthotopic neo-
however, in the tubularized original form in almost all bladder. In both cases, the bowel segment used does not
cases. The frequent use of sigmoid and ileocecal segment affect the results and its detubularization provides higher
is explained by the need for ureteral reimplantation in capacity and compliance of the reservoir, although the
cases of ureteral stenosis or high-grade reflux. In neo- cecum may be used successfully with its original tubular
bladder surgery, the same intestinal segments were used, configuration. There are no randomized comparative
but the Studer procedure was used in 73.3%. The suc- studies between these segments in tuberculosis patients,
cess criteria were not uniform among the series, but suc- but there is one nonrandomized retrospective compar-
cess was usually defined by improvement of urinary ative study between detubularized ileocecal and sigmoid
frequency and preservation of upper urinary tract. The segment and nondetubularized sigmoid. Worse results
former was achieved in 80 to 100% of the cases. How- were associated with the nondetubularized sigmoid
ever, there were cases with progression to terminal renal (16). The detubularization allows a greater reservoir
failure in same series (16, 18, 71, 72, 75) despite an volume, from 18% to 425% improvement, proportional
absence of postvoiding residue and no stenosis or re- to the length of the segment to be detubularized and
flux of uretero-vesical anastomosis/junction. Different inversely proportional to the radius. The cecum pos-
from bladder augmentation due to neurogenic bladder, sesses a greater radius and volume than the sigmoid and
most patients can void spontaneously with no need of ileum at initial configuration; therefore, the volumetric

ASMscience.org/MicrobiolSpectrum 13
Figueiredo et al.

improvement after the detubularization is unnecessary subject of future studies. We propose that any patient
and may explain the good outcome associated with the presenting with gross hematuria, persistent microscopic
tubularized cecum (16). Ureteral reimplantation should hematuria or pyuria, recurrent urinary tract infection,
be made in cases of stenosis but is not necessary in reflux and persistent irritative micturition symptoms be inves-
(77). The choice between bladder augmentation and tigated for urogenital tuberculosis, with six urine sam-
orthotopic neobladder is not well established, and there ples collected for culture or PCR. We also propose a
are no comparative studies. Neobladder is advised with periodic urine examination for hematuria or pyuria in
a very small bladder (less than 15 to 20 ml) or in the patients with previous pulmonary tuberculosis or immu-
presence of pain (suprapubic or perineal) (17, 74, 77). nosuppressed subjects (AIDS or posttransplantation).
Pain may not improve after augmentation and may be
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