Abstract
The objective of this study was to determine the effect of circumcision on the frequency of urinary tract infection (UTI), growth development, and the nutrition status in infants with antenatal hydronephrosis (AH). The data were collected prospectively between 1998 and 2010. Infants with a fetal pelvis diameter of >5 mm identified with antenatal ultrasound were followed-up. Body height and weight were expressed as HZ scores (observed height − median height/standard deviation) and WZ scores (observed weight − median weight/Standard deviation). The nutritional status was evaluated and the body weight was transformed to a weight-for-height index (WHI = weight/median weight for the height age × 100). The HZ and WZ scores or WHI were calculated for each patient at the first and last visits. The chi-square and Student’s t tests were used for statistical analysis. A p value <0.05 was considered significant. The study included 178 (134 males, 44 females) patients. Of these, 29 were diagnosed by vesicoureteral reflux (VUR), 87 by obstructive uropathy, and 54 by normal. Of 134 males, 111 infants were circumcised. The mean monitoring time was 45±24.9 months and the mean age of circumcision was 14 ± 16.06 months. The pre-circumcision UTI frequency (2.97 ± 1.14/y) was significantly higher than post-circumcision period (0.25 ± 0.67/y) (p < 0.05). Also, pre-circumcision UTI frequency (2.97 ± 1.14/y) was significantly higher than the UTI frequency observed in female cases (0.85 ± 0.91/y) and in the overall study group (0.73 ± 0.79/y) (p < 0.05). In all patients, the HZ of the circumcised subjects (0.18 ± 1.01) was statistically higher than uncircumcised subjects (−0.26 ± 0.92) (p < 0.05). Although statistically insignificant, the HZ of the circumcised males (0.13 ± 1.24) with VUR was higher than the uncircumcised patients (0.03 ± 0.55) (p > 0.05). In obstructive uropathy groups, the HZ of the circumcised males (−0.13 ± 0.54) was also found to be higher than uncircumcised males (−0.49 ± 0.66) (p < 0.05). Although nutrition scores were found to be better in circumcised males, no statistically significant effect of circumcision on the nutrition status was detected. In conclusion, postnatal early circumcision of infants with AH seems to prevent frequent UTIs and nutritional disturbances enabling normal growth.
Introduction
Circumcision is a surgical procedure which includes the removal of the circumcision tissue called prepisium and to open up the head of the penis. In addition to being a widely-applied surgical intervention in Turkey and other Muslim countries due to religious beliefs, it is also the most commonly applied surgical procedure in the world. Due to several indications other than these reasons, its application rate increased rapidly in non-Muslim countries in recent years. According to the most recent studies, it is claimed that urinary tract infection (UTI) is related to the circumcision tissue and the frequency of UTI is 10–20 times higher in uncircumcised children compared to others.Citation1,Citation2 Circumcision has been started to be applied in the nineteenth century on a routine basis to be protected from many diseases and it has been quickly accepted in many countries. At least 25% of the men in the world are circumcised due to the aforementioned reasons. On the other hand, no specific studies investigating the effect of circumcision on the frequency of UTI or growth and nutritional status in children with AH are available in the literature. In this study, we aimed to evaluate the effect of circumcision on the frequency of UTI as well as growth and nutrition status in infants with AH.
Materials and methods
The data were collected prospectively from 178 patients with AH in our hospital between 1998 and 2010 and analyzed retrospectively. Hydronephrosis was defined as the dilation of the anterior–posterior pelvic diameter (APPD) of the fetal renal pelvis ≥5 mm after 20 weeks of gestation. Postnatally, all infants with AH were given prophylactic amoxicilin (10 mg/kg/day, single night dose) and were investigated according to our previously proposed protocol.Citation3–5
On admission, body weights and lengths were measured and urinalysis and urine culture tests were performed; measurements and tests were repeated monthly. Patients were followed at 1-month intervals up to the 1st year, then at 3-month intervals until the final examination. Presence of ≥100,000 CFU/mL bacteria in bagged specimens with clinical symptoms were accepted as UTI. In the absence of clinical signs, to diagnose or rule out of UTI, any bacterial growths were confirmed by intravesical catheterization or suprapubic aspiration. Infants with proven UTI were treated with suitable antibiotics. In this study, we only considered the frequency of UTI, irrespective of the localization.
An ultrasound (US) scan (Toshiba SSA-270A Color Doppler) was performed on days 2–3 (or when first seen), days 7–10, and at the first month of life. Irrespective of the postnatal US findings, a voiding cystourethrography (VCUG) (Siemens model 180110 91 × 1060) was performed for all infants at the first month. If both three postnatal US findings and VCUG were normal, the fourth US was performed after 6 months of life. If this last US was normal, further follow-up of the infant was continued. Based on these findings, infants were classified into two categories: normal (isolated hydronephrosis), i.e., children without urinary tract malformations; abnormal, i.e., children with malformations.
All male patients with AH were offered for circumcision. The decision of circumcision and timing were completely dependent on the preferences of the parents. All circumcisions were performed surgically at different institutions and their circumcision times were recorded. The frequency of UTI, height, weight, and nutrition status were assessed in all boys and girls as well as in infants with or without urinary tract abnormality. These parameters were also assessed in pre- and post-circumcision periods in male infants.
Body height and weight were expressed as HZ (=observed height − median height/standart deviation) and WZ scores (=observed weight − median weight/standard deviation). The nutritional status was evaluated and the body weight was transformed to a weight-for-height index (WHI) (=weight/median wieght for the height age × 100). Turkish reference curves for age and gender were taken with in all scores. The lower and upper limits for these parameters were accepted as follows: −2 and +2 for HZ and WZ scores; 90 and 120% for WHI score. The HZ and WZ scores or WHI were calculated for each patient at the first and last visits.
Our hospital ethics committee approved this study and parents were informed by being given explanation of the clinical significance of urinary tract abnormalities as well as the rationale of postnatal follow-up. The chi-square and student’s t tests were used for statistical analysis. A p value <0.05 was considered significant.
Results
Totally 178 infants were diagnosed by AH. Among these, 134 (75.3%) were males and 44 (24.7%) were females and the male/female ratio was 3.04. All the patients were monitored starting from their newborn terms and the mean monitoring time was 45 ± 24.9 months (min 12, max 112 months). Mean intrauterin (IU) diagnosis age and renal pelvic diameter were 30.9 ± 5.6 weeks and 10.1 ± 3.6 mm, respectively.
Of the 178 infants, 124 (69.7%) infants were detected to have urinary tract malformation. Underlying abnormalities were VUR in 29 (16.3%) patients and obstructive uropathy in 87 (48.9%) patients [ureteropelvic junction obstruction (UPJO) in 71 patiens, ureterovesical junction obstruction (UVJO) in 14, UPJO + VUR in 1 and posterior urethral valve (PUV) in 1 patient] ().
Table 1. Postnatal diagnoses (n = 178).
Among 134 male infants, 111 males were circumcised. Mean age of circumcision was 14 ± 16.06 months (range: 1–81 months; median: 7 months). Pre-circumcision UTI frequency of the circumcised infants was found to be higher (2.97 ± 1.14) than female infants (0.85 ± 0.91) and all of the subjects (0.73 ± 0.79) (p < 0.05). Similarly, pre-circumcision UTI frequency (2.97 ± 1.14) was found to be higher than the post-circumcision UTI frequency (0.25 ± 0.67) in the circumcised subjects and this difference was found to be significant (p < 0.05). In the study group, initial HZ, WZ, and WHI score values showed no difference whereas the final HZ of the circumcised subjects (0.18 ± 1.01) was statistically found to be higher than uncircumcised subjects (−0.26 ± 0.92) (p < 0.05). Final WHI scores were not statistically different between circumcised and uncircumcised male infants ().
Table 2. Comparison of UTI frequency, HZ, WZ, and WHI scores in the study group (n = 178).
Of 178 patients, 29 (16.3%) were detected to have VUR; 16 of them were circumcised, 4 of them were uncircumcised and 9 of them were female infants. In the pre-circumcision period, the frequency of UTI in the circumcised males with VUR was found to be higher (3.16 ± 1.93) than females (1.16 ± 1.21) and all of the VUR patients (1.34 ± 1.10) (p < 0.05). Similarly, the frequency of UTI in the pre-circumcision period (3.16 ± 1.93) was higher than in the post-circumcision period (0.73 ± 1.29) in circumcised males with VUR and this difference was also significant (p < 0.05). Final HZ of the circumcised males (0.13 ± 1.24) with VUR was found to be higher than the uncircumcised infants (0.03 ± 0.55), but this difference was not statistically significant (p > 0.05). Similarly, although statistically insignificant, WHI scores improved in the circumcised males after circumcision ().
Table 3. Comparison of UTI frequency, HZ, WZ, and WHI scores in infants with VUR (n = 29).
Of the study group, 87 infants (48.9%) showed obstructive uropathy; 59 of them were circumcised males and 10 of them were uncircumcised males as well as 18 of them were female subjects. In the pre-circumcision period, the frequency of UTI (2.86 ± 1.22) was higher than in the females (1.11 ± 0.91) and all of the patients (0.71 ± 0.70) (p < 0.05). Also, pre-circumcision UTI frequency (2.86 ± 1.22) was higher than the post-circumcision UTI frequency (0.17 ± 0.54) in the circumcised males with obstructive uropathy (p < 0.05). Initial HZ of the circumcised males (−0.13 ± 0.54) with obstructive uropathy was also found to be higher than uncircumcised males (−0.49 ± 0.66) and females (−0.13 ± 0.87) (p < 0.05). Final WHI scores were found to be better than initial, but it was not statistically significant ().
Table 4. Comparison of UTI frequency, HZ, WZ, and WHI scores in infants with obstructive uropathy (UPJO, UVJO, PUV) (n = 87 patients).
Discussion
The most important aspect of this study is the fact that circumcision could decrease the risk of UTI in infants with AH, which is considered as an important risk factor for UTI, and also it could provide a positive contribution to growth development. Moreover, to the best of our knowledge, this is the first study performed to date, investigating the hypothesis whether circumcision, by decreasing the risk of UTI, would effect positively the growth and nutrition status in male infants with AH.
The association between UTI and circumcision was first defined in 1982 by Ginsberg and McCracken.Citation6 Later studies have clearly reported that circumcision decreased the risk of UTI in male children. The risk of UTI in uncircumcised children has been attributed to the increased bacterial colonization under the foreskin and periurethral area, which leads to ascending infections. For this reason, the removal of the circumcision tissue seems to be one of the most logical steps to prevent UTI.Citation7–12 Majority of the recent studies claim that UTI is related to the circumcision tissue and the frequency of UTI is 10–20 times higher in uncircumcised children compared to others.Citation13 Additionally, the rate of hospitalization among children with UTI was also higher being 1/140 and 1/530 in uncircumcised and circumcised children, respectively.Citation14 However, there are controversial studies that are against routine circumcision in such patients.Citation15,Citation16 After these striking results, American Academy of Pediatrics published a report which advised the application of circumcision for kids under 1 year of age to decrease the risk of penis cancer and UTI in the future.Citation17 Although it is a widely applied procedure in Muslim countries due to religious beliefs, with the publication of this report, circumcision applications have also rapidly increased in the non-Muslim societies which happened also due to various indications other than religious beliefs.Citation10,Citation13 Today, it is the most commonly applied surgical procedure in the United States and it has been reported that 80–98% of all the male children get circumcised before their first birthday and over 1,250,000 circumcision procedures are performed in a year.Citation17
The number of studies investigating the relationship between circumcision and UTI in infants with AH is limited. In majority of these studies, however, patients did not have any urological problems. Only one study has demonstrated the effect of circumcision in patient with posterior uretral valve. Mukherjee et al.Citation18 have reported that circumcision decreased the frequency of UTI by 83% compared to pre-circumcision status. No studies investigating the causal relationship between circumcision and growth and nutritional status in children with AH are available in the literature, so far. In our study, early circumcision was advised to all male subjects with AH diagnosis. Infants were also categorized into subgroups among themselves and according to their underlying pathologies. These subgroups (circumcised and uncircumsised male subjects, female subjects and all subjects) were compared in terms of UTI frequency as well as growth and nutritional status. Among 178 monitored subjects, 111 were circumcised males, 23 infants were uncircumcised males and 44 of them were females. Similar to the previous studies, the pre-circumcision UTI frequency in circumcised males was found to be higher than the post-circumcision UTI frequency, suggesting that circumcision prevents UTI in male infants with AH. When the subjects were categorized according to their underlying causes, UTI frequency also significantly decreased in circumcised infants with obstructive uropathy and VUR. Based on our study results, we can speculate that circumcision resulted in a reduction in UTI frequency in male infants with urinary tract malformations.
If urinary tract abnormalities could not be detected by the prenatal US and subsequently managed, many of these urologic abnormalities would manifest later in life as pyelonephritis, growth retardation, hypertension, or even end-stage renal failure due to recurrent UTI. Increased catabolism and loss of appetite caused by tubulointerstitial dysfunction associated with intrauterine hydronephrosis, and frequent UTIs are likely the most important reasons for growth retardation of these children.Citation3,Citation4,Citation19,Citation20
In our study, we found that the frequency of UTI significantly decreased after circumcision. Furthermore, weight Z score showed no significantly improvements during the study period whereas height Z score in the overall study group gradually increased after circumcision. Although statistically insignificant, we found better nutritional scores in circumcised males. These results confirm the idea that circumcision may effect positively the growth and nutritional status in male infants with antenatally detected hydronephrosis.
This study includes several limitations. Firstly, growth during the first months of life is depending on many parameters, such as birth weight, socioeconomic conditions, and the kind of feeding. We cannot rule out that these factors that were not included in our study might have contributed to delayed growth. Secondly, low-number subgroup limited us to conclude the effect of circumcision on UTI as well as growth and nutritional status in VUR patients. Thirdly, since there is a natural decrease in UTI episodes due to spontaneous resolution of VUR or maturation of mucosal defenses in growing children, the reduction of UTI therefore cannot be solely attributed to the intervention performed. Also, the reduction of UTI frequency might be caused by better urine collection upon time due to parental training.
As a result, we can conclude that the low incidence of UTI following circumcision may suggest a causal relationship between circumcision and growth and nutritional status in infants with AH. However, multi-center longitudinal studies are needed to confirm our findings.
Declaration of interest
The authors report no conflicts of interest. The authors alone are responsible for the content and writing of the paper.
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