










































Frequency of Metabolic Abnormalities in Pakistani 
Children With Renal Stones
Muhammad Tanveer Sajid,1 Muhammad Rafiq Zafar,1 Qurat-Ul-Ain Mustafa,2 Rabia Abbas,3  
Sohail Raziq,1 Khurram Mansoor1

1 Armed Forces Institute of Urology, Rawalpindi, Pakistan  2 Army Medical College, Rawalpindi, Pakistan 3 Pak Emirates Military Hospital, Rawalpindi, Pakistan

Abstract

Objective To determine the frequency of various metabolic abnormalities in children with urinary lithiasis.
Methods This cross-sectional study was conducted at the Armed Forces Institute of Urology, Rawalpindi, from 
30 January 2017 to 1 February 2020. A total of 1355 children who were aged 4 to 14 years and who had renal stones 
were included, while those with urinary tract infections, posterior urethral valve, pelvi-ureteric junction obstruction, 
reflux disease, and chronic renal failure were excluded. Twenty-four-hour urine samples were analyzed for urinary 
uric acid, calcium, oxalate, citrate, and magnesium. Demographics and metabolic abnormalities—hypercalciuria, 
hyperoxaluria, hypocitraturia, hyperuricosuria, and hypomagnesuria—were noted and analyzed.

Results The study analysis included 1355 patients. Low urine volume was observed in 465 (34.3%) of the patients. 
Three hundred nine patients (22.8%) had metabolic abnormalities, the most common being hypocitraturia (184, 
59.5%) followed by hypercalciuria (136, 44%) and hypomagnesuria (126, 40.8%). Mean age of presentation, disease 
duration, recurrent bilateral stones were found significantly different in those having metabolic abnormalities 
(7.81±2.25 versus 8.76±2.50 P < 0.001, 7.73±1.50 versus 8.43±1.54 P < 0.001, 19.4 versus 2.4% P < 0.001 respectively). 
No significant difference was found in frequency of abnormal urinary metabolic parameters between boys and girls 
(P > 0.05) or, upon data stratification, on the basis of disease duration, stone laterality, and recurrence.

Conclusions Metabolic abnormalities were found in 22.8% % of children presenting with urinary lithiasis. The 
most frequent abnormality observed was hypocitraturia followed by hypercalciuria and hypomagnesuria. Early 
identification helps manage such patients appropriately, mitigating long-term sequelae.

Introduction

There has been a sharp rise in urinary lithiasis in the pediatric population over the past couple of decades, probably 
due to global warming and the widespread westernization of diet, which has led to the obesity pandemic, as well as 
other environmental factors[1]. Although the true incidence is not known, it is estimated that 6% to 10% of children are 
affected. Although the lifetime risk varies widely among nations, metabolic disorders are found in in approximately 
40% to 50% of children with urolithiasis[2]. The disease is endemic in Pakistan, Turkey, and Saudi Arabia, as well as 
in some South Asian and African countries. Hot climate, poverty, paucity of clean water, and malnourishment are 
contributing factors[3].

Urinary stones are typically classified by their location or by their chemical composition. Pediatric urolithiasis is 
a multifactorial disease, rightly considered by many as a symptom of underlying abnormality, either metabolic 
or anatomical, having poorly understood etiopathogenesis[4]. Supersaturation-crystallization is the most widely 
accepted theory. Most patients present with non-specific symptoms. Late presentation is a norm leading to significant 

Key Words Competing Interests Article Information

Child, calcium oxalate, crystallization, 
hypercalciuria, lithiasis, magnesium,  
uric acid, urinalysis

None declared. Received on July 22, 2020 
Accepted on September 28, 2020

Soc Int Urol J. 2021;2(1):18–24

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delay in the diagnosis. Ultrasonography is the preferred 
preliminary investigation, as it is non-invasive, easily 
available, and repeatable[5]. Thorough metabolic 
evaluation of all children who have renal stones is the 
linchpin if morbidity and long-term renal complications 
are to be prevented. Moreover, stone disease carries 
a high probability of recurrence among children, 
necessitating early identification of those at risk, 
prophylaxis, and lifestyle modifications. The 24-hour 
urine screening test is the most important tool in the 
diagnostic workup of children presenting with urinary 
lithiasis[6].

In adults, treatment options include watchful waiting, 
extracorporeal shock wave lithotripsy, ureterorenoscopy, 
percutaneous nephrolithotomy, and open removal. In 
children, however, extracorporeal shock wave lithotripsy 
and minimal invasive procedures utilizing smaller 
diameter scopes are preferred[7]. Prophylactic treatment 
to prevent recurrence depends upon identification of 
metabolic abnormalities among those at risk.

Studies conducted worldwide have found a very high 
incidence of metabolic abnormalities when children 
presenting with nephrolithiasis were subjected to 
metabolic screening[8]. In recent years, several studies 
have studied metabolic evaluation of stone formers, 
but most deal with adult populations compounded by 
presence of limited local data having small sample size 
and absence of 24-hour urinary metabolic screening[9]. 
In this context, the current study aims to assess the 
frequency of metabolic abnormalities among local 
children presenting with urolithiasis. This is intended 
to help clinicians design management protocols that 
incorporate urine metabolic screening as an integral 
part, with a view to preventing stone recurrence.

Methods
This descriptive cross-sectional study was conducted at 
the Department of Urology and Renal Transplantation, 
AFIU Rawalpindi Pakistan, a quaternary care state-of-
the-art facility, from 30 January 2017 to 1 February 2020. 
Approval was provided by the hospital’s ethical review 
board (Certificate # Uro-Adm-Trg-1/IRB/2017/106), 
an independently organized body adhering to the 
guidelines of the Declaration of Helsinki, the WHO, 
and the International Council on Harmonization and 
Good Practice (ICH-GCP). Over a 3-year period, a 
non-probability consecutive sampling technique was 
used to enroll 1355 patients who met the inclusion 
criteria (children of both sexes, aged 4 to 14 years, with 
a confirmed diagnosis of renal stones), while those who 
had PUJO, urinary tract infections, PUV, vesicoureteral 
reflux, inadequate 24-hour urine samples, and CRF were 
excluded. Written informed consent was obtained from 
the patients and their guardians as deemed appropriate.

All urine samples were obtained from the patients, 
without dietary restrictions, once lithiasis and/or 
associated UTI had been treated. Clean plastic bottles 
having 10 mL of 6M hydrochloric acid as preservative 
were used to collect 24-hour urine samples, and 
additional samples were collected without preservative 
to measure uric acid. Collection adequacy was verified 
by urine creatinine excretion rate. Urinary calcium, 
magnesium, citrate, oxa late, and uric acid were 
determined by a calorimetric method with ADVIA 1800 
Clinical Chemistry System (Siemens Medical Solutions, 
Malvern, US), while pH was measured by the Mission 
Expert urinalysis reagent strips (Acon Laboratories 
Inc., San Diego, US). Presence or absence of metabolic 
abnorma lities ie, hy perca lciuria, hy peroxa luria, 
hypocitraturia, hyperuricosuria and hypomagnesuria 
(as per operational definition), as well as demographic 
details (age, sex, residence, educational status, BMI, urine 
volume, duration of symptoms, clinical presentation, 
family history of urolithiasis, stone laterality, and stone 
recurrence) were recorded on a specially designed 
proforma. Stone recurrence was defined as symptomatic 
stone recurrence diagnosed on ultrasound or CT 
scan a minimum 30 days after complete clearance of 
stones. The following values were used to define 
abnormalities on 24-hour urine: creatinine (12 to 30mg/
kg), hypocitraturia (< 365mg/1.73m2 for boys and < 
310mg/1.73m2 for girls), hypercalciuria (> 4mg/kg), 
hyperoxaluria (> 45mg/1.73m2), hypomagnesuria (< 
1.2mg/kg), hyperuricosuria (> 9.3mg/kg) and low urine 
volume (< 1mL/kg/hr × 24hrs).

Statistical analysis was done using IBM SPSS 
Statistics for Windows, Version 24.0. (Armonk, NY: 
IBM Corp). Descriptive statistics were used to calculate 
means ±standard deviation for quantitative variables, 
while frequencies with percentage were calculated for 
qualitative variables, significance being determined 
by Student t test and chi-square test, respectively. 
Effect modifiers like age, sex, duration of disease, 
stone laterality, and recurrence were controlled by 
stratification. Post-stratification chi-square was applied 
to determine the effect on metabolic abnormalities.  
P ≤ 0.05 was considered significant.

Results
The study analysis included 1355 patients (75.7% of total 
1789 reported; 434 (24.3%) excluded) with mean age 
8.54±2.47 years, and male to female ratio 1.25:1. Low 
urine volume was found in 465 (34.3%) of the patients. 
Three hundred nine patients (22.8%) were found to have 
metabolic abnormalities.

Mean age of presentation was significantly younger 
in those having metabolic abnormalities (7.8±2.3 
versus 8.8±2.5; P < 0.001), and more male than female 

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patients were affected with metabolic derangements 
(1.6:1 versus 1.2:1; P <0.01). Disease duration and BMI 
were significantly lower in patients with metabolic 
abnormalities (P < 0.001), who also exhibited frequent 
bilateral recurrent stones and positive family history  
(in all cases, the difference was statistically significant, 
P < 0.001) (Table 1).

In the 309 patients with metabolic abnormalities, 
hypocitraturia (184, 59.5%) was the most common 
der a ngement , fol lowe d by hy poc a lc iu r ia a nd 
hypomagnesuria (Table 2). When broken down by each 
type of metabolic abnormality individually, there was no 
statistically significant difference between subgroups of 
children stratified by sex, disease duration (± 6 months), 
stone laterality (right, left, or bilateral) and presence or 
absence of recurrence (Table 3).

Discussion
Urinary lithiasis in pediatric populations is relatively 
rare but increasing steadily across the globe[1]. Several 
factors can predispose children to nephrolithiasis, 
notably metabolic and genitourinary abnormalities[4]. 
Recurrence is a hallmark of childhood stone disease, 
imposing considerable morbidity and cost[6]. The 
current study was conducted to determine the frequency 
of metabolic derangement among local children 
presenting with renal stones.

Our results show concordance with national as well 
as international literature, albeit with a different 
study population. In a study by Rizvi et al.[10], the M: 
F  ratio was 2.7:1, the mean age was 7.1±3.8 years, and 
patients and malnutrition in their patients. Metabolic 
evaluation was performed in 1892 children, revealing 
hypovolemia, hypocitraturia, and hyperoxaluria. Our 
findings were similar with respect to age, nutritional 
status, and low urine volume, and hypocitraturia being 
the most common abnormality, but not with respect to 
sex distribution. However, in keeping with our findings, 
other studies have reported a male preponderance in 
children with metabolic abnormalities[3,11]. Children 
in our study who had metabolic abnormalities were 
younger, had earlier presentation, presented more 
frequently with bilateral stones, and were more likely to 
have positive family history.

There is wide variation in the reported frequency of 
metabolic abnormality (33% to 93% of children with 
renal stones), depending upon geographical region of 
the study. Issler et al.[8] in their review carried in the 
UK found a frequency of 34%, similar to our findings, 
while studies by Elmecai et al. in Turkey[12] and Gajengi 
et al. in India[13] reported 83.2% and 64%, respectively. 
Similarly, Bilge et al.[14] in their study analyzed 
children aged 16.8 ± 14.9 months and found metabolic 

abnormalities in 17.8% of cases, hypercalciuria being the 
most common (88.9%). Barata et al.[15] in a retrospective 
analysis of children with nephrolithiasis in Brazil 
reported a 13.6% frequency of metabolic abnormality. 
The most frequent disorders found were hypercalciuria, 
hyperuricosuria, and hypocitraturia. Frequency was 
22.8% in this study. The higher frequency may be 
due to a hot, humid climate, and, in keeping with the 
international literature, bilateral and recurrent stones 
were associated with positive family history. However, in 
contrast to our results, obesity rather than malnutrition 
was associated with metabolic abnormality as also 
indicated by Bandari et al.[16].

Ethnic and geographic differences may account 
for the variations in the reported prevalence of 
abnormalities in children with metabolic disorder. 
Elmecai et al.[12] studied 143 preschool children 
a nd fou nd hy per uricosuria a nd hy pocit raturia 
to be most frequent disorders (24.5% and 23.8% 
respectively). They also found that 16.8% of patients 
had multiple metabolic abnormalities. In a study of 100 
Iranian children with urolithiasis, Sadeghi et al.[17] 
reported hypocitraturia (64%) to be most common 
abnormality followed by hypercalciuria (56%), while 
Velásquez-Forero et al.[18] found hypocitraturia in  
70%, hypomagnesuria in 42%, and hypercalciuria in 
37% of Mexican children evaluated. Van Dervoort et 
al.[19] similarly observed hypocitraturia to be the most 
commonly identified metabolic abnormality in a US 
population, present in 52% of the children, but Rellum 
et al. found hypercalciuria to be most common in a 
Dutch cohort, present in 47%[20]. Our results revealed 
hypocitraturia in 59.5% children, hypocalciuria in 
44%, and hypomagnesuria in 40.8%, while 14.6% had 
hyperuricosuria, and hyperoxaluria was present in 
9.4%, which is consistent with the findings of previous 
reports[6,21]. However, in contrast to our findings, 
Copelovitch et al.[22] reported hypercalciuria in 30% to 
50% of the cases, and Nasseri et al.[23], and Amancio et 
al.[24] reported hyperuricosuria as a frequent metabolic 
change. Similarly, Isler et al.[8] reported hypercalciuria 
in 52%, hyperoxaluria in 21%, and cystinuria in 22%, 
while 27% also had bilateral stones. Children with 
metabolic abnormalities in the current study had 
bilateral stones in 19.4% of cases compared to 2.6% in 
children without metabolic abnormalities (P <  0.001). 
A statistically significant relation was revealed among 
bilateral, recurrent stones, and family history in our 
study, underscoring the importance of metabolic 
assessment in children, as early identification allows 
targeted treatment which mitigates recurrence among 
those with longer life expectancy. As ours is a referral 
institute with a wide catchment area, our cohort of the 
represent all socioeconomic strata of the society, thus 
allowing generalization of the results.

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TABLE 1. 

Demographic features of children presenting with renal stones (n=1355)

Demographic Variable
Patients Without Metabolic 

Abnormalities (n=1046)
Patients with Metabolic 
Abnormalities (n= 309) P Value

Age of the patient (mean±SD) 8.8±2.5 7.8±2.3 <0.001

Gender distribution (M:F) 563:483 191:118 0.013

BMI (kg/m2) 16.3±1.3 15.6±1.5 <0.001

Disease duration (months) 8.4±1.5 7.7±1.5 <0.001

Urine volume (mL /kg)          Normal 686(65.6) 204(66.1)
0.89

Low 360(34.4) 105(33.9)

Residence (n %)

0.36Urban 515(49.2) 143(46.3)

Rural 531(50.8) 156(53.7)

Educational status (n %)

0.19
Not attending school 180(17.2) 53(17.2)

Attending school 670(64.1) 184(59.5)

Disconnected education 196(18.7) 72(23.3)

Recurrent stones (n %)

<0.001Yes 114(10.9) 108(35)

No 932(89.1) 201(65)

Family counselling (n %)

0.13Yes 728(69.6) 229(74.1)

No 318(30.4) 80(25.9)

Stone laterality (n %)

<0.001
Right 490(46.8) 116(37.5)

Left 529(50.6) 133(43)

Bilateral 27(2.6) 60(19.4)

Family history urolithiasis (n %)

<0.001Yes 94(9) 116(37.5)

No 952(91) 193(62.5)

Clinical presentation (n %)

0.93

Incidental 88(8.4) 25(8.1)

Abdominal/flank pain 260(24.9) 73(23.6)

Urinary tract infection 434(41.5) 130(42.1)

Hematuria 154(14.7) 49(15.9)

Vomiting 52(5) 15(4.9)

Enuresis 37(3.5) 08(2.6)

Urgency 21(2) 09(2.9)

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More recent studies conducted in China[25] and the 
UK[26] found hypocitraturia and cystinuria to be the 
most common abnormalities. Cystinuria has a reported 
frequency of 2% to 8%. Our study did not report this 
abnormality as our institution does not have the capacity 
to test for it. Different dietary habits and hereditary 
factors might influence differences in urine chemistry 
results explaining variegated pattern of frequencies 
world over. Stone analysis was performed in various 
studies across the globe finding calcium oxalate and 

phosphate among 77% to 86 % of the patients[9,20], 
however such details were not reported in the studied 
patients so the type of stone cannot be commented upon.

No significant difference was found in the frequency 
of abnormal urinary metabolic parameters between boys 
and girls (P > 0.05), which is consistent with results of 
Elmaci et al.[12]. Similarly, we did not find any difference 
in metabolic abnormalities with respect to age, laterality, 
and recurrence. Our data showed significantly lower 

TABLE 2. 

Frequency of various metabolic abnormalities among children diagnosed with metabolic abnormalities

Metabolic Disorder

Frequency (n %) 

Yes No

Hypocitraturia 184(59.5) 125(40.5)

Hypercalciuria 136(44) 173(56)

Hypomagnesuria 126(40.8) 183(59.2)

Hyperuricosuria 45(14.6) 264(85.4)

Hyperoxaluria 29(9.4) 280(90.6)

TABLE 3. 

Data stratification with respect to disease duration, stone laterality and recurrence in children having metabolic   
abnormalities (n=309)

Variable 

Hypocitraturia
(n %) P 

Value

Hypercalciuria
(n %) P

Value

Hypomagnesuria 
(n %) P 

Value

Hyperuricosuria
(n %) P

Value

Hyperuricosuria
(n %) P 

Value

Yes No Yes No Yes No Yes No Yes No

Disease duration

<06 Months 37(12) 25(8) 0.79 28(9) 34(11) 0.79 27(9) 35(11) 0.25 09(3) 53(17) 0.47 06(2) 56(18) 0.07

>06 Months 147(48) 100(32) 0.84 108(35) 139(45) 0.91 99(32) 148(50) 0.82 36(11) 211(68) 0.75 23(7) 224(72) 0.66

Stone laterality

Right 71(23) 45(15) 0.19 60(19) 56(18) 0.95 41(13) 75(24) 0.44 14(4) 102(33) 0.06 11(4) 105(34) 0.35

Left 80(26) 53(17) 0.16 46(14) 87(28) 0.71 62(20) 71(23) 0.35 23(7) 110(36) 0.48 10(3) 123(40) 0.21

Bilateral 33(11) 27(9) 0.45 30(10) 30(10) 0.77 23(7) 37(12) 0.44 08(3) 52(17) 0.65 08(3) 52(17) 0.65

Stone recurrence

Yes 67(22) 41(13) 0.32 54(17) 54(17) 0.84 46(15) 62(20) 0.16 0.91 09(3) 99(32) 0.68

No 84(27) 117(38) 0.52 82(26) 119(38) 0.90 80(26) 121(39) 0.05 0.38 20(6) 181(59) 0.26

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TABLE 3. 

Data stratification with respect to disease duration, stone laterality and recurrence in children having metabolic   
abnormalities (n=309)

Variable 

Hypocitraturia
(n %) P 

Value

Hypercalciuria
(n %) P

Value

Hypomagnesuria 
(n %) P 

Value

Hyperuricosuria
(n %) P

Value

Hyperuricosuria
(n %) P 

Value

Yes No Yes No Yes No Yes No Yes No

Disease duration

<06 Months 37(12) 25(8) 0.79 28(9) 34(11) 0.79 27(9) 35(11) 0.25 09(3) 53(17) 0.47 06(2) 56(18) 0.07

>06 Months 147(48) 100(32) 0.84 108(35) 139(45) 0.91 99(32) 148(50) 0.82 36(11) 211(68) 0.75 23(7) 224(72) 0.66

Stone laterality

Right 71(23) 45(15) 0.19 60(19) 56(18) 0.95 41(13) 75(24) 0.44 14(4) 102(33) 0.06 11(4) 105(34) 0.35

Left 80(26) 53(17) 0.16 46(14) 87(28) 0.71 62(20) 71(23) 0.35 23(7) 110(36) 0.48 10(3) 123(40) 0.21

Bilateral 33(11) 27(9) 0.45 30(10) 30(10) 0.77 23(7) 37(12) 0.44 08(3) 52(17) 0.65 08(3) 52(17) 0.65

Stone recurrence

Yes 67(22) 41(13) 0.32 54(17) 54(17) 0.84 46(15) 62(20) 0.16 0.91 09(3) 99(32) 0.68

No 84(27) 117(38) 0.52 82(26) 119(38) 0.90 80(26) 121(39) 0.05 0.38 20(6) 181(59) 0.26

BMI in those having metabolic abnormalities similar 
to findings of Isler et al.[8]. Nevertheless, quoted 
literature is divided on whether obesity or malnutrition 
contributes to stone formation. The reason for lower 
BMI in our patients is malnutrition, which is prevalent 
in this part of the world. The reported frequency of 
positive family history varies. Amancio et al.[24] 
reported positive family history in 85% of patients, and 
Barata et al.[15] in 61.3%. In the present study, 37.5% of 
the analyzed patients reported positive family history, 
recurrent stones were present in 35%, and bilateral 
stones in 19.4% of those having metabolic abnormalities. 
The findings are similar to those of Ferraro et al.[27]  
and others. This fact points towards importance of 
metabolic evaluation in children presenting with 
nephrolithiasis so that appropriate strategy may be 
instituted to prevent relapse or recurrence.

Major clinical features were found to be similar in 
both groups of patients studied (P > 0.05). In our study, 
the most common presenting feature was UTI, followed 
by flank or abdominal pain and hematuria. These results 
are consistent with those of other studies[13,28,29]. 
Both visible and non-visible hematuria were relatively 
uncommon in our study compared w it h ot her 
reports[15,19]. These findings point to the close relation 
between UTI and stone disease and to the previously 
noted importance of screening children presenting with 
recurrent UTI. However, 24-hour urine collection in 
children is not always easy. Parents, as well as children, 
need to be educated on the importance of these samples, 

which will help in timely identification and treatment 
of underlying abnormality. If 24-hour collection is 
not feasible, spot urine analysis can provide a useful 
alternative.

Limitations of the study
The results of the present study should be interpreted 
with caution as it involved subjects from a single 
center and had a short follow-up. Further, there was no 
availability of cysteine analysis at our laboratory, which 
limited our ability to draw epidemiological conclusions 
about cystinuria. Moreover, neither metabolic screening 
of blood nor stone analysis was included, missing a 
critical aspect of stone disease in children. Our results 
cannot be extrapolated with certainty to the global 
pediatric population because of significant geographical 
and environmental variations and because our data are 
not population based.

Conclusion
Metabolic abnormalities were found in 22.8% of children 
presenting with urinar y lithiasis. Hy pocitraturia 
and hypercalciuria are the most frequently observed 
metabolic abnormalities observed in our series. Children 
having metabolic abnormalities depicted frequent 
bilateral recurrent stones, underscoring the importance 
of 24-hour urine metabolic screening.

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24 SIUJ  •  Volume 2, Number 1  •  January 2021 SIUJ.ORG

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