Kidney Stone Composition in Third-World Areas: What Kashgar Tells Us?

Abstract

Objective:

To analyze urinary stone compositions in patients from Kashgar, China.

Materials and Methods:

We analyzed the components of urinary stones in 732 consecutive patients with urolithiasis admitted to the First and Second People's Hospital of Kashgar Prefecture, Xinjiang, from July 2014 to November 2016. The patients were divided into two groups by ages: group A, 0 to 18 years and group B, >18 years old. The distributions of various stone compositions were analyzed and correlated with the gender and age.

Results:

The mean age of group A was 3.90 ± 4.09 years and that of group B was 39.88 ± 16.40 years. The overall gender ratio (male:female) was 2.27:1. Ammonium acid urate (AAU) stone was the most frequent stone, male 35.83% and female 33.48%. Female patients were significantly more common than male patients in calcium apatite stone (p = 0.004). Of all 732 cases, patients younger than 18 years were more than patients older than 18 years (58.47% vs 41.53%). The majority of the patients (77.87%) had the stone located in the upper urinary tract. Two peak ages for both genders were noted in 1 to 3 years and 19 to 40 years group of the patients. In group of 1 to 3 years patients, male were more than female (37.60% vs 24.55%, p = 0.001), whereas in the group of 10 to 18 years patients, female were more than male (10.71% vs 4.13%). AAU was the predominant stone component in group <1 year (70. 5%, p < 0.01, as compared with other groups.). Uric acid stone was more prevalent in group >60 years (66.8%, p < 0.01) than in other groups. Patients in 1 to 3 years were in the peak age group of AAU stones in both the upper and lower urinary tract.

Conclusion:

Most of the patients with urolithiasis diagnosed and treated in Kashgar are <18 years old, especially younger than 3 years old. The most frequent stone component in this area was AAU. More than 50% patients <18 years old had AAU stone. The mechanisms that could trigger the high prevalence of AAU stone in patients <18 years old are worth further investigation.

Introduction

Urolithiasis is a common disease occurring in both developed and developing countries, and its prevalence has been gradually increasing over several decades.^1,2 Several studies have shown that the risk of developing urolithiasis is apparently higher in Western countries (5%–9% in Europe and 13%–15% in the United States³) than in Asian countries (1%–5%).⁴ In a given population, the stone compositions were influenced by many variables, including age, gender, genetic, climatic, dietary, and social factors.⁵

Children with nephrolithiasis often have a high recurrence rate and risk of long-term detrimental effects on kidney function.⁶ Although urinary stone disease remains less frequent in children than in adults,⁷ the prevalence of urolithiasis in the pediatric population is increasing worldwide over the past few decades.^6,8

It was reported that a high incidence of nephrolithiasis in children, ranging from 33 to 93%, was associated with metabolic abnormalities because of the effects of environmental or dietary factors.⁸ Local conditions in Xinjiang, such as weather, geographic location, and nutrition, may play a major role in defining the profile of pediatric urolithiasis.⁹ Therefore, analysis of stone composition would be beneficial to reveal the underlying metabolic risk factors and to explore a proper strategy for stone treatment and prevention. So far, there is a paucity of study on epidemiological characteristics of urinary calculi in Kashgar, an Uygur nationality area in Northwestern China.

Hence, in this study, we retrospectively analyzed the stone compositions of 732 consecutive patients who underwent surgical treatment in Kashgar from 2014 to 2016, and correlated them to the gender and age.

Materials and Methods

This retrospective study included 732 consecutive patients with urolithiasis admitted to the First and Second People's Hospital of Kashgar Prefecture, Xinjiang, from July 2014 to November 2016 (Table 1). Stone specimens were collected by endoscopic or open surgery and were analyzed by infrared spectroscopy (ThermoNicolet 380). The predominant stone components were recorded, and all the compositions were then separated into eight major categories: calcium oxalate monohydrate (COM), calcium oxalate dehydrate (COD), calcium phosphate (CP), calcium apatite (CA), uric acid (UA), ammonium acid urate (AAU), magnesium ammonium phosphate (MAP), and others (xanthine, sodium urate, quartz, calcium acetate, silica, calcite, cystine, and anhydrous oxalic acid).

Table 1.

Distribution of Patients and Stone General Characteristics (n = 732)

Characteristics
Age
≤18 years, n (%); mean (SD)	428 (58.47); 3.90 ± 4.09
>18 years, n (%); mean (SD)	304 (41.53); 39.88 ± 16.40
Gender, n (%)
Male	508 (69.40)
Female	224 (30.60)
Stone homogeneity, n (%)
Pure stones	467 (63.80)
Mixed stones	265 (36.20)
Stone location, n (%)
Upper tract
Renal	513 (70.08)
Ureter	57 (7.79)
Lower tract
Bladder	144 (19.67)
Urethral	18 (2.46)
Nationality, n (%)
Hann	18 (2.46)
Uyghur	713 (97.40)
Khalkhas	1 (0.14)
Living condition, n (%)
City	124 (16.94)
Countryside	608 (83.06)

To analyze the correlation of stone composition with age, the patients were divided into two groups: group A, 0 to 18 years old and group B, >18 years old (Table 1). For further analysis of distributions of different stone components in different ages, the patients were subdivided into eight groups: <1, 1 to 3, 4 to 6, 7 to 9, 10 to 18, 19 to 40, 41 to 60, and >60 years.

Statistical analysis

Statistical analyses were performed using SPSS 22.0 software (SPSS, Chicago, IL). Categorical data, shown as the number or percentage, were analyzed by the chi-square test. Mutisample comparison was conducted by Kruskal–Wallis test. A two-sided p < 0.01 was considered to be statistically significant.

Results

Stone general characteristics

Stone analysis was performed in 732 cases: 508 (69.40%) males and 224 (30.60%) females. The mean age of patients in group A was 3.90 ± 4.09 years old and that of patients in group B was 39.88 ± 16.40 years old (Table 1). The number of patients in group A was more than those in group B (58.47% vs 41.53%). Of all the cases, stones with single component were 63.80%. Regarding the stone locations, upper urinary tract consisted of 513 (70.08%) renal stones and 57 (7.79%) ureter stones, whereas lower urinary tract consisted of 144 (19.67%) bladder stones and 18 (2.46%) urethral stones. In terms of nationalities of China, most of the patients were Uyghur (97.40%), followed by Han (2.46%) and Khalkhas (0.14%).

Distribution of stone compositions by gender

The occurrence frequency of each stone component is presented in Table 2. AAU was the most frequent stone composition with an overall prevalence of 35.63% in males and 33.48% in females. Compared with AAU stones, CaOx stones were less frequent (30.91% for male and 31.25% for female in COM, 1.78% for male and 2.68% for female in COD). UA stones were seen in 17.72% of males and 13.84% of females. The following stone compositions of male/female were CP (5.12%/4.91%), MAP (4.53%/6.25%), CA (1.38%/4.91%), and others (2.95%/2.68%, including six xanthine, six sodium urate, three quartz, two silica, one calcium acetate, one anhydrous oxalic acid, one calcite, and one cystine.). It showed that female patients were significantly more common than male patients only in CA stone (p = 0.004).

Table 2.

Stone Composition and Location According to Patient Gender

Position	Upper tract, n (%)		Lower tract, n (%)		Overall, n (%)
Gender	Male	Female	Male	Female	Male	Female	p
COM	127 (34.89)	68 (33.01)	30 (20.83)	2 (11.11)	157 (30.91)	70 (31.25)	0.884
COD	6 (1.65)	6 (2.91)	3 (2.08)	0 (0)	9 (1.78)	6 (2.68)	0.425
CP	21 (5.77)	11 (5.34)	5 (3.47)	0 (0)	26 (5.12)	11 (4.91)	0.906
CA	6 (1.65)	9 (4.37)	1 (0.69)	2 (11.11)	7 (1.38)	11 (4.91)	0.004^a
MAP	20 (5.50)	14 (6.80)	3 (2.08)	0 (0)	23 (4.53)	14 (6.25)	0.327
AAU	118 (32.42)	67 (32.52)	63 (43.75)	8 (44.44)	181 (35.63)	75 (33.48)	0.540
UA	53 (14.56)	26 (12.62)	37 (25.69)	5 (27.78)	90 (17.72)	31 (13.84)	0.193
Other	13 (3.57)	5 (2.43)	2 (1.39)	1 (5.56)	15 (2.95)	6 (2.68)	0.838
All	364	206	144	18	508	224

COM = calcium oxalate monohydrate; COD = calcium oxalate dehydrate; CP = calcium phosphate; CA = calcium apatite; UA = uric acid; AAU = ammonium acid urate; MAP = magnesium ammonium phosphate.

p < 0.01, male vs female by chi-square test.

There were 364 males and 206 females who had upper urinary tract stone (77.87%), whereas 144 male and 18 female patients who had lower urinary tract stone (22.13%, Tables 1 and 2). The ratio of male to female was 1.77 among patients with upper urinary tract stones and 8 among patients with lower urinary tract stones. CaOx was the most common composition of the upper urinary tract stones (36.54%/35.92%, male/female), whereas AAU was the predominant stone composition of the lower urinary tract stones (43.75%/44.44%, male/female).

Distribution of age groups for male and female patients

The number of patients stratified by age and gender is shown in Table 3. The two peaks of age group with urolithiasis were 1 to 3 years and 19 to 40 years. When stones from both genders were compared, the occurrence rate of male was higher than the occurrence rate of female in 1 to 3 years (37.60% vs 24.55%, p = 0.001), whereas the rate of female was higher than the rate of male in 10 to 18 years (10.71%, vs 4.13%, p = 0.001).

Table 3.

Percentage of Each Age Group of Male and Female Patients

Group (year)	Overall, n (%)	Male, n (%)	Female, n (%)	p
<1	44 (10.19)	30 (5.91)	14 (6.25)	0.857
1–3	246 (33.61)	191 (37.60)	55 (24.55)	0.001^a
4–6	62 (8.47)	36 (7.09)	26 (11.61)	0.043
7–9	31 (4.23)	18 (3.54)	13 (5.80)	0.162
10–18	45 (6.15)	21 (4.13)	24 (10.71)	0.001^a
19–40	185 (25.27)	117 (23.03)	68 (30.36)	0.036
41–60	68 (9.29)	56 (11.02)	12 (5.36)	0.015
>60	51 (6.97)	39 (7.68)	12 (5.36)	0.256
All	732	508	224

p < 0.01, male vs female by chi-square test.

Occurrence frequency of stone compositions by age

As shown in Table 4, the component of urinary stones was statistically different between each age groups (p < 0.01, multisample comparison by Kruskmal–Wallis test). AAU was the predominant stone component in <1 year (70.5%, p < 0.01, as compared with other groups by chi-square test). UA stone was more prevalent in group >60 years (66.8%) than in other groups (p < 0.01).

Table 4.

Occurrence Frequency of Stone Components in Different Age Groups

Component	<1 year, n (%)	1–3 years, n (%)	4–6 years, n (%)	7–9 years, n (%)	10–18 years, n (%)	19–40 years, n (%)	41–60 years, n (%)	>60 years, n (%)
COM	0 (0)	28 (11.38)	20 (32.26)	14 (45.16)	27 (60.00)	97 (52.43)	28 (41.18)	13 (25.49)
COD	0 (0)	4 (1.63)	1 (1.61)	0 (0)	1 (2.22)	7 (3.78)	2 (2.94)	0 (0)
CP	7 (15.91)	13 (5.28)	1 (1.61)	6 (19.35)	1 (2.22)	6 (3.24)	2 (2.94)	1 (1.96)
CA	0 (0)	4 (1.63)	0 (0)	0 (0)	2 (4.45)	12 (6.49)	0 (0)	0 (0)
MAP	2 (4.55)	8 (3.25)	4 (6.45)	2 (6.45)	4 (8.89)	16 (8.65)	1 (1.47)	0 (0)
AAU	31 (70.5)^a	164 (66.7)	29 (46.77)	6 (19.35)	4 (8.89)	14 (7.57)	6 (8.82)	2 (3.92)
UA	2 (4.55)	22 (8.94)	5 (8.06)	3 (9.68)	4 (8.89)	24 (12.97)	27 (39.71)	34 (66.8)^a
Other	2 (4.55)	3 (1.22)	2 (3.23)	0 (0)	2 (4.45)	9 (4.86)	2 (2.94)	1 (1.96)
All	44	246	62	31	45	185	68	51

p < 0.01, male vs female by chi-square test.

Table 5 showed the comparisons of the location and age distribution of AAU stones between groups of male and female patients. We found that there were 123 males (40.05%) and 61 females (23.83%) who had upper urinary tract stone, whereas 63 male (24.61%) and 9 female (3.52%) patients who had lower urinary tract stone. The ratio of male to female was 2.02 among patients with upper urinary tract stones and 7 among patients with lower urinary tract stones. Group 1 to 3 years was the peak age group of AAU stones in both the upper and lower urinary tract.

Table 5.

Percentage of Each Age Group and Location According to Patients' Gender in AAU Stones

Position	Upper tract, n (%)		Lower tract, n (%)
Gender (years)	Male	Female	Male	Female	Overall, n (%)
<1	14 (11.38)	9 (14.75)	6 (9.52)	2 (22.22)	31 (12.11)
1–3	80 (65.04)	33 (54.10)	48 (76.19)	3 (33.33)	164 (64.06)
4–6	12 (9.76)	12 (19.67)	4 (6.35)	1 (11.11)	29 (11.33)
7–9	3 (2.44)	1 (1.64)	1 (1.59)	1 (11.11)	6 (2.34)
10–18	2 (1.63)	2 (3.28)	0 (0)	0 (0)	4 (1.56)
19–40	6 (4.88)	3 (4.92)	4 (6.35)	1 (11.11)	14 (5.47)
41–60	5 (4.07)	1 (1.64)	0 (0)	0 (0)	6 (2.34)
>60	1 (0.81)	0 (0)	0 (0)	1 (11.11)	2 (0.78)
All	123 (40.05)	61 (23.83)	63 (24.61)	9 (3.52)	256

AAU = ammonium acid urate.

Discussion

Since the past several decades, the research on etiology, cost-effective, and preventive means of urolithiasis has been a hot topic. Yet there is still up to 30% to 50% of recurrence rate, patients with the formation of another stone occurring within 5 years of first stone incident.¹⁰ The percentage of each stone type in different countries and areas differs markedly because of variability in climate, lifestyles, and dietary habits.¹¹ Therefore, the stone analysis has been recommended to explore the risk factors associated with stone formation such as metabolic abnormalities, predict the stone fragility, and provide theoretical rationale for prevention of urolithiasis recurrence.

In this study, the gender ratio of male to female patients was 2.27:1, corresponding to the reports from Spain¹² and the United States.⁵ Regarding the urolithiasis compositions, multicomponent stones were less frequent, which was similar to the previous reports (26%–95%).^13,14

Contrary to earlier report,¹⁵ our study showed that the prevalence of urolithiasis in patients <18 years was significantly higher than that >18 years. Among those patients ≤18 years, the average age was 3.90 ± 4.09 years (range 3 months to18 years), similar to other reports that ranged from 36 months to 13.3 years.^16
–18 Nevertheless, we found that among 428 (296 males and 132 females) patients <18 years old, the peak incidence of urolithiasis was at the age of 1 to 3 years old. This difference may be associated with differences of stone composition.

The reported male-to-female ratio of pediatric urinary calculi is highly varied. One study showed that the prevalence of calculi was higher in males when they were younger than 10 years, and in females when they were older than 10 years.⁶ However, we found that the males were statistically dominant in the 1 to 3-year age group, whereas females were dominant in the 10 to 18-year age group. In terms of stone location, the incidence of urolithiasis in males was much higher than in females either in upper or lower urinary tract, especially the highest composition stones such as AAU. These results were different from other studies, which showed a low incidence of AAU in these age groups of patients.^15,19 We proposed that the discrepancy was possibly because of the different dietary habits in this special area.

AAU stones are not common in advanced regions, and the prevalence varies with different geographical areas: 0.38% in Japan,²⁰ 0.75% in Norway,²¹ and up to 3.1% in North America.²² However, similar results were detected in developing countries. In Egypt, AAU was found in 26% of the upper tract stones and in 27% of the lower tract stones.¹⁸ In Tunisia, 14% of the stones was AAU,²³ whereas another study from Tunisia reported AAU in 47% of the stones.²⁴ Studies from the North of Pakistan reported AAU in 45% and 65% of the stones, respectively.^25,26 These obvious geographic variations indicated that genetic, dietary, and environmental factors might play an important role in the formation of AAU stones. For instance, chronic diarrhea, which has a high incidence in developing countries, would be a major underlying factor for the formation of AAU stones because of a tremendous loss of body water and ions.

Furthermore, urinary tract infections (UTIs), nutritional deficiencies combined with low-protein and high-carbohydrate diet have been considered a risk factor in the lithogenic process.¹³ Bacterial urease, which is normally intracellular, is released into the urine after the lysis of bacterial cells.²⁷ As a result, a UTI with urease-producing bacteria could increase the levels of urinary ammonium and lead to highly alkaline urine, both being preconditions for the formation of struvite and AAU crystals. Kashgar is a poverty-stricken area in Northwestern China, where the people are living in a relatively poor sanitary condition and nutriture deficiencies, especially in children. Their diets are lower in calcium, phosphate, and water, while higher in cereal. Their UTI was common mainly because of the poor hygienic condition. The hot climate and long summer of Kashgar could be another risk factor for stone development, since the children in this area undergo more dehydration and urine concentration, thus promoting a urinary supersaturation, crystallization, and stone formation.²⁸ It is possible that hyperuricosuria, low phosphorus intake, low diuresis, and chronic diarrhea in children promoting the formation of AAU stone, respectively, or collectively. All these factors might be the further explanations for high incidence of urolithiasis in younger children and higher proportion of AAU stones in this area.

CaOx containing stones (including COM and COD) are mainly observed in developing countries, for example, the countries in North Africa and Asia Minor.²⁹ However, we found that the CaOx stones were 33.06% of all cases, which was less than other studies (44%–82.56%).^15,30,31 The lower rate of CaOx stone in Kashgar might be associated with ethnicity, geographic location, and diet, which contains less oxalate.

In our data, the percentage of UA stone was 16.53%, lower than that reported in Australia³⁰ but higher than that reported in France.³² The main reasons for the differences could be the different lifestyle and dietary habits. In agreement with other investigations,³³ our study revealed that the incidences of UA stone were increased with age, and were higher in males than in females. This could also be explained by low urinary pH and the dietary habits with more meat in Kashgar, Xinjiang.

It is widely accepted that MAP is the best marker to detect the persistent UTIs induced by urease-producing bacteria. We showed that the rate of MAP stone was 5.05%. Inadequate medical service might be the main reason for such a problem.

Cystine stone accounts for 1% to 5% in pediatric patients, which is the only phenotypic manifestation of cystinuria.³⁴ It is a sequela of hereditary disorder. In our study, cystine stone was observed in only one pediatric patient. This scarcity of cystine stone was in agreement with many other studies.³⁵ In Alaya's study,³¹ there was not a single case of cystine stone in 1301 Tunisian patients, despite that there were 21 cases of cystinuria.

Conclusions

Most of the patients with urolithiasis diagnosed and treated in Kashgar are <18 years old, especially <3 years old. The most frequent stone component in Kashgar was AAU)and >50% of this kind of stones occurred in patients <18 years old. Yet, the mechanisms that could trigger the high prevalence of AAU stone in patients especially younger than 18 years old are not clear, which needed to be further investigated and identified.

Footnotes

Acknowledgments

This work was financed by grants from the Science and Technology Department of Guangdong Province, China (No. 2016A020212023), and Science and Technology project in Guangzhou (No. 201507020026).

Author Disclosure Statement

No competing financial interests exist.

Abbreviations Used

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