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Saudi Journal of Kidney Diseases and Transplantation
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ORIGINAL ARTICLE Table of Contents   
Year : 2008  |  Volume : 19  |  Issue : 3  |  Page : 361-370
Normal Reference Levels of Serum Cystatin C in Saudi Adults

Department of Medicine, King Khalid University Hospital, Riyadh, Saudi Arabia

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This is the first report from Saudi Arabia studying the normal reference intervals in adult Saudi subjects and evaluating serum cystatin C as a prospective marker for the assessment of the glomerular filtration rate (GFR). Three hundred healthy adult Saudi subjects including 156 males (52%) and 144 females (48%), with a mean age of 31.21 ± 9.82 years were prospectively studied to establish normal reference ranges for cystatin C. A total of 68.34% of the study patients were in the age-group of 21-40 years. The mean serum cystatin C in the 300 healthy subjects was 0.751 ± 0.11 mg/L (0.50 - 1.09), increasing gradually with age: it was 0.738 ± 0.11 mg/L (0.51 - 1.09) in the age­group 21 - 30 years and 0.807 ± 0.12 (0.51 - 1.09) among subjects who were > 50 years of age. The mean serum cystatin C in females (0.778 ± 0.118 mg/L) was significantly hig-her than in males (0.726 ± 0.095 mg/L) (p < 0.0001). The serum cystatin C level was within the defined reference range of 0.53 - 0.95 mg/L in 95% of the subjects with a mean value of 0.74 ± 0.097 mg/L, and was falling within the 95% confidence interval of 0.73865 - 0.7637 mg/L, and with 98.84% area under the curve (AUC). All the other renal function markers (urea, serum crea-tinine, calculated GFR, BMI) among the studied subjects were within the normal reference ranges for adult Saudi population. The serum cystatin C level had a significant correlation with the body mass index (BMI) (r = 0.155; p = 0.007) and a correlation with serum creatinine as well (r = 0.009; p = 0.873). It showed a negative correlation with calculated GFR as per Cockroft-Gault equation (r = - 0.101; p = 0.083).

Keywords: Markers of GFR, Cystatin C, Normal reference range

How to cite this article:
Al Wakeel JS, Memon NA, Chaudhary AR, Mitwalli AH, Tarif N, Isnani A, Hammad D. Normal Reference Levels of Serum Cystatin C in Saudi Adults. Saudi J Kidney Dis Transpl 2008;19:361-70

How to cite this URL:
Al Wakeel JS, Memon NA, Chaudhary AR, Mitwalli AH, Tarif N, Isnani A, Hammad D. Normal Reference Levels of Serum Cystatin C in Saudi Adults. Saudi J Kidney Dis Transpl [serial online] 2008 [cited 2021 Jun 21];19:361-70. Available from: https://www.sjkdt.org/text.asp?2008/19/3/361/40494

   Introduction Top

Estimation of the glomerular filtration rate (GFR) using the endogenous marker, cys­tatin C, has been recently described. Cystatin C is a 13.3 KD protein, which is elimi­nated from the circulation almost exclu­sively by glomerular filtration. [1] Studies in adults have shown cystatin C to be a more sensitive marker of changes in the GFR [2] than serum creatinine. [3] Beyond the first year of life, serum cystatin C concentration is constant, while that of creatinine increases steadily until adulthood. [3] According to seve­ral reports, cystatin C reflects GFR inde­pendent of body weight and height, ma­king GFR estimates with this marker less variable than with creatinine. [4] In view of its growing importance as a prospective marker for the assessment of renal status, we evaluated the normal reference range of serum cystatin C in adult Saudi population.

   Subjects and Methods Top

A total of 547 healthy adult Saudi sub­jects, consisting of 378 male and 169 female blood donors of various age-groups, were recruited through the Blood Bank at the King Khalid University Hospital (KKUH) Riyadh, Saudi Arabia. Full informed consent was obtained from all the participants. All of them underwent routine medical examina­tion as required for the blood donors. Their selection was based on the following criteria: a. No history and signs/symptoms of any renal or non-renal disease as well as hyper­tension during the past six months. b. Not on any type of medications. c. Normal dipstick urine test, and normal serum creatinine (62.0 - 119.0 µmol/L).

Their demographic data was carefully re­corded and blood samples were collected and processed according to standard pro­tocols. Anthropometric measurements were taken using a standard portable scale. Height (meters) and body weight (kg) were recorded. Body mass index (BMI) was cal­culated. Estimated GFR (e-GFR) was cal­culated according to the Cockroft-Gault equation. [5] This equation is adequate to cal­culate the GFR (creatinine clearance) of most patients with normal muscle mass and serum creatinine < 4.5 mg/dl.

   Results Top

A total of 547 healthy subjects were screened of whom 247 were excluded be­cause of underlying diabetes mellitus, hyper­tension or raised serum levels of sodium and/or potassium. The remaining 300 sub­jects, with a mean age of 31.21 ± 9.82 years (15-61), who fulfilled the required criteria, were finally selected. Of these 300 subjects, 156 (52.0%) were male with a mean age of 31.26 ± 9.48 years (18-61), and 144 (48%) were female with a mean age of 31.15 ± 10.21 years (15-53).

[Table - 1] shows the distribution of serum cystatin C according to various age-groups. The overall mean cystatin C among the study subjects was 0.751 ± 0.11 mg/L (0.5­1.09), which was well within the reference range suggested by the manufacturer (0.53 - 0.95 mg/L). Although the overall cystatin C concentration was within the normal refe­rence range (0.53 - 0.95 mg/L) in all the age-groups, relative variations were observed between various age-groups. For example, the cystatin C concentration was lowest among the younger age-group (21-30 years) (0.738 ± 0.11; 0.25-1.09 mg/L), and increased gradually to 0.807 ± 0.12 mg/L (0.6-0.95) in the older age-group of above 50 years indicating a slight age-dependent rise. This rise in serum cystatin C with age was, however, significant only between the age­groups 21-30 years and > 50 years (p = 0.05).

The mean serum cystatin C among the 156 (52%) healthy male subjects was 0.726 ± 0.095 mg/L (0.50 - 0.97), being highest (0.834 ± 0.10; 0.66 - 0.95 mg/L) in the oldest age-group >50 years and the lowest (0.710 ± 0.10; 0.55 - 0.87 mg/L) in the youngest age group <- 20 years.

The overall mean serum cystatin C in the 144 (48%) healthy adult female subjects was 0.778 ± 0.118 mg/L (0.53 - 1.09), which was significantly higher than in male subjects (0.726 ± 0.098; p< 0.0001). The increase in serum cystatin C with age in female subjects was not that prominent as seen in male subjects: it increased from 0.778 ± 0.104 mg/L (0.6 - 0.93) in the age-group < 20 years to 0.780 ± 0.11 mg/L (0.53 - 0.9) in the age group 41 - 50 years without showing any significant inter-group differ­in the age-group > 50 years showed slightly lower cystatin C (0.760 ± 0.148 mg/L) than the other age-groups (0.778 ± 0.104 to 0.780 ± 0.11 mg/L; p= 0.763). However, the inter-group differences in the cystatin C concentration among healthy female subjects were not significant [Table - 2].

The presence of significantly higher cys­tatin C concentration among females was not restricted only to the total sample size but also reflected in each group except the age-group >50 years where healthy males had slightly raised cystatin C (0.834 ± 0.10 mg/L) as compared to healthy females (0.760 ± 0.148 mg/L), p = 0.3439. How­ever, this observation could not be gene­ralized due to the less number of studied subjects in the age-group of > 50 years (n=11).

Since no previous data on the normal reference ranges of serum cystatin C in Saudi population was available, the refe­rence ranges recommended by the manu­facturer (0.53 - 0.95 mg/L; Dade Behring Marburg GmbH, Germany) was employed to group healthy subjects into three categories:

a. below normal (<- 0.53 mg/L),

b. normal (0.53 - 0.95 mg/L) and

c. above the normal range (> 0.95 mg/L).

Three subjects (1%) had the serum cystatin C values below the normal range with a mean concentration of 0.51 ± 0.01 mg/L (0.50-0.52), and a mean age of 27.33 ± 3.22 years (25-31). Eleven (3.7%) had their serum cystatin C above the normal refe­rence range with a mean serum concen­tration of 1.01 ± 0.044 mg/L (0.96-1.09), and an age of 31.91 ± 10.12 years. The remaining 286 subjects (95.3%) had their serum cystatin C levels within the defined normal reference range of 0.53 - 0.95 mg/L with a mean concentration of 0.74 ± 0.097 mg/L (0.53-0.95), and a mean age of 31.22 ± 9.87 years [Table - 3].

[Table - 4] highlights the distribution of mean serum cystatin C among healthy Saudi sub­jects according to the gender and defined reference ranges. Majority of the males (96.8%) had serum cystatin C within the normal reference range as compared to fe­male subjects (93.8%; p = 0.1312). Of the 11 healthy subjects (3.7%) who had the serum cystatin C above the normal refe­rence range (> 0.95 mg/L), nine (82%) were males and only two (18%) were females. All three subjects who had the mean serum cystatin C below the reference range (< 0.53 mg/L) were males [Table - 4], [Figure - 1].

The mean BMI was 25.9 ± 3.82 kg/m 2 (14.0-40.2), which was at the upper limit of the normal (20 - 25 kg/m 2 ) and showing a slight trend towards being "overweight" [Table - 5]. The mean BMI in female subjects (26.018 ± 4.46 kg/m 2 ) was slightly higher than in male subjects (25.782 ± 3.12 kg/m 2 ) (p = 0.5935). The mean serum concentra­tions of urea and creatinine in male and fe­male subjects were within the normal refe­rence range for adult Saudi population. However, men had significantly higher urea and creatinine than women (p = <0.001). On the other hand, women had signifi­cantly higher serum cystatin C as com­pared to men (p < 0.0001). Cockroft-Gault based GFR of our study subjects was within the normal reference range and more or less of the same magnitude among males (125.04 ± 18.95 ml/min) and females (124.57 ± 18.84 ml/min).

Serum cystatin C exhibited a positive cor­relation with BMI in our study subjects. Thus, the cystatin C levels increased signi­ficantly from 0.74 ± 0.11 mg/L, at normal BMI, to 0.80 ± 0.11 mg/L in mild to mode­rately obese subjects (p <0.012). The lowest was seen in the underweight group (BMI less than 20) with cystatin C value of 0.74 ± 0.95 mg/L. None of the subjects were morbidly obese, i.e. BMI > 40 kg/m 2 . Serum creatinine and urea also showed a slight progressive increase with the rise in the BMI; however it was not significant. The GFR also showed a positive correlation with BMI and increased progressively and significantly from 119.97 ± 16.97 ml/min/ 1.73 m 2 , at normal BMI of 20-25 kg/m 2 , to 137.06 ± 8.87 ml/min/1.73 m 2 at a BMI of 30.1 - 40 kg/m 2 (p= < 0.0002).

In the present study, serum cystatin C levels had a significant positive correlation with BMI (r= 0.155; p= 0.007) whereas a slight positive correlation was seen with age (r= 0.094; p= 0.107), weight (r= 0.109; p= 0.061) and serum creatinine (r= 0.009; 0.873). A slight negative correlation was observed bet­ween cystatin C and GFR (r= 0.101; p= 0.083), height (r=-0.082; p=0.161) and urea levels (r=0.012; p=0.833) [Table - 6].

A significant positive correlation was seen between creatinine and height (r= 0.443; p= < 0.001), weight (r= 0.346; p= < 0.001), urea (r=0.427; p=<0.001), and BMI (r= 0.113; p= 0.022). A weak positive corre­lation was observed between creatinine and cystatin C (r= 0.009; p= 0.879), and crea­tinine and age (r= 0.002; p= 0.970). In our subjects, the serum creatinine showed a significant negative correlation with GFR (r=-0.352; p= < 0.001) as compared to cystatin C (r= _ - 0.101; p= 0.083).

The mean GFR data was stratified into normal (90-120 ml/min) and above normal (> 120 ml/min) levels and its correlation was evaluated with other renal markers. In the present study, the GFR had a significant negative correlation with age (r=-0.119; p= 0.044) and a positive correlation with height (r= 0.151; p= 0.009), weight (r= 0.488; p< 0.001) and BMI (r= 0.466; p< 0.001). A weak, negative correlation was also present between GFR and blood urea (r=-0.043; p= 0.465) and cystatin C (r=-0.101; p= 0.083).

   Discussion Top

This is the first report from Saudi Arabia studying the normal reference intervals in adult Saudi subjects and evaluating serum cystatin C as a prospective marker for the assessment of GFR in patients with renal disease. The measurement of serum cystatin C in healthy adults and children has been studied by several authors and wide varia­tions exist in its reference values, [4] both in adults and children. [6],[7],[8],[9],[10],[11],[12] A single combined­ gender reference interval of 0.50-1.09 mg/L was obtained (95% confidence interval of 0.738 - 0.763 mg/L) having 98.84% area under the curve (AUC). Our results are in agreement with earlier reports that also used PENIA to establish reference intervals for serum cystatin C. For example, Finney et al, [13] studied 309 adult healthy subjects and reported a reference interval of 0.51-0.98 mg/L, and Uhlmann et al, [11] studied 133 adult volunteers and reported a 95% central reference interval of 0.51-0.92 mg/L. Our reference range was also similar to Stowe et al, [14] who studied 103 adults aged 20-71 years and reported a central reference interval of 0.57-1.05 mg/L. However, the reference interval of Saudi adults was con­siderably lower than that reported by Norlund et al, [15] (0.70-1.21 mg/L; n= 242), Newman et al, [16] (< 1.25 mg/L; n= 206) and Erlandsen et al, [17] (.054-1.21 mg/L; n=270), all of whom employed particle-enhanced turbid metric immunoassay (PETIA). Simi­larly, our reference interval was slightly lower than that reported by and Norlund et al, [12] (0.56-1.22 mg/L; n= 249) who also em­ployed PETIA. It was interesting to note that studies which employed PETIA [12],[16],[18],[19],[20] for the measure-ment of serum cystatin C had higher reference intervals than those which used PENIA. [11],[13],[14] This observation has also been reported in a recent review by Laterza et al.

Earlier studies suggested that serum cystatin C concentrations were independent of gender. [18],[19] However, more recent studies have demonstrated the influence of gender on the mean serum levels of cystatin C. [11],[13],[14],[15],[17],[21] Pergnade and Jung [21] were the first to report that serum cystatin levels were lower in women (1.26-2.30mg/L) than men (1.52­2.76 mg/L). Recent studies have also documented the presence of higher serum cystatin C among males than females. [11],[13],[14],[15],[17] For example, Finney et al, [13] reported that their study female volunteers (n= 155) had lower cystatin C reference interval (0.49-0.94 mg/L) than males (0.56-0.98 mg/L; n= 154). Similarly, Norlund et al, [15] reported a slightly higher mean serum cys­tatin C in males (0.92 ± 0.13 mg/L; n= 57) than females (0.87 ± 0.12 mg/L; n= 67). In our study, the mean serum cystatin C (0.778 ± 0.118 mg/L) as well as the reference interval (0.53-1.09 mg/L) was significantly higher (p< 0.0001) in females than males (0.726 ± 0.095 (0.50-0.97) mg/L) [Table - 5]. This difference in the mean serum cys­tatin C levels could not be attributed to age because the mean age was similar (p= 0.9230) both in men (31.26 ± 9.48; 18-61 years) and women (31.15 ± 10.21; 15-53 years). Although our findings are not in agreement with other studies reporting a slightly higher serum cystatin C reference interval in males than females, [13],[15],[21] never­ theless, our results are in partial agreement with Uhlman et al, [11] who reported a slightly higher reference limit in women (0.51-0.94 mg/L) than men (0.48-0.98 mg/L). The pre­sence of significantly higher cystatin C in our healthy women may be due to slightly higher BMI in women (26.018 ± 4.46 kg/m 2 ) than men (25.782 ± 3.12 kg/m 2 ), p= 0.593. Galteau et al, [22] have also reported a moderate, biologically insignificant, corre­lation between serum cystatin C and BMI in their healthy adults. In our study, despite higher BMI in women, both serum crea­tinine and urea were significantly lower in females than males (p< 0.0001). Therefore, the presence of higher BMI may not be the only contributing factor for higher serum cystatin C levels in our studied women. Vinge et al, [23] have demonstrated the lack of significant relationship between serum cystatin C and the muscle mass. Slayden et al, [24] have recently shown in animal models (Rhesus macaques) that estradiol (E2) increased vaginal cystatin C expression in fibroblasts and smooth muscle bundles whereas progesterone suppressed this effect.

Pergande and Jung [21] have recommended establishing gender specific reference inter­vals. Similarly, Galteau et al, [22] have sugges­ted separate reference intervals for men (0.740.0 ± 0.100 mg/L) and women (0.65 ± 0.085 mg/L) aged 20-59 years. Based upon the significant difference in the mean serum cystatin C concentration observed in our study, we also recommend independent refe­rence intervals for men (0.50-0.97 mg/L) and women (0.53-1.09 mg/L).

Renal function has been shown to decline with increasing age, with both kidney size and volume decreasing after the 4 th decade of life. [25],[26] Back et al, [27] using iohexol clearance measurements in adult healthy males, reported that GFR declines after 50-years of age, decreasing by 12 ml/min per decade. Although serum cystatin C concentration was found to be within the normal defined reference range among all the age-groups in our healthy subjects, significant age de­pendent variations were seen in some of the age-groups. A gradual rise in the mean serum cystatin C was seen with age [Table - 1]: it was 1.3 to 1.8% with every decade of age until the age of 50 years, after which cystatin C showed a rise of 5.9% in pa­tients above 50 years of age. This was in agreement with others who have also re­ported a relationship between serum cys­tatin C and age. [6],[7],[8],[13],[15],[18],[22],[28],[29] Based upon the highest mean serum concentration ob­served in our healthy subjects above 50 years of age (0.807 ± 0.12 mg/L), we suggest an independent reference interval for healthy adults aged > 50 years (0.6-0.95 mg/L). Several other studies have also recommended a separate reference interval for healthy subjects above the age of 50 years. [7],[8],[13],[15],[22],[28],[29] Although GFR has been shown to decline steadily with increasing age, [26],[30] the mean serum creatinine levels in our study remained, more or less, cons­tant (68.0-71.39 µmol/L) in all the decades (21 to > 50 years) whereas serum cystatin C concentration increased gradually with age showing a significant rise after the 5th decade [Table - 1]. The failure of creatinine to rise with increasing age is probably due to a reduction in the muscle mass and the rate of creatinine production. [25] Our results indicated and confirmed the earlier reports [6],[7],[8] that the decline in the GFR with in­creasing age was reflected better by serum cystatin C levels than creatinine. Moreover, we found that the rise in serum cystatin C with age was more prominent in men than women [Table - 2]. Our findings contrast with the study of Finney et al, [13] who showed that the rise in serum cystatin C levels with age after the age of 50 years was more significant in women than men. Further studies with larger sample size are needed to evaluate the gender-associated changes in the serum cystatin C with increasing age.

Another important aspect of our results is the presence of slightly higher serum cys­tatin C (p= 0.423) in the younger age­group subjects ( < 20 years) as compared to older groups (21-40 years). This is in agreement with Galteau et al, [22] who also reported higher cystatin C in younger age­groups and, therefore, proposed a separate reference interval for children aged 4-19 years of age. Similarly, Harmoinen et al, [31] have suggested independent reference inter­val for children aged 3-16 years of age. Previous studies have shown that at birth, serum cystatin C values are usually high (1.17-3.06 mg/L) due to the immature renal function, and then decreases gradually and reaches a stable level by the age of 16-19 years. [22],[31],[32] When we examined the correlation of serum cystatin C and creatinine with the calculated GFR (Cockcroft-Gault), it was found that in healthy subjects, serum creatinine had better correlation with GFR (r=-0.352; p= 0.001) than cystatin C (-0.101; p= 0.083).

In conclusion, we were able to establish normal reference interval in our studied Saudi adults and showed that serum cys­tatin C concentration rises with age and is not independent of gender as previously reported.[33]

   References Top

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14.Stowe H, Lawrence D, Newman DJ, Lamb EJ. Analytical performance of a particle­enhanced nephlometric immunoassay for serum cystatin C using rate analysis. Clin Chem 2001;47(6):1482-5.  Back to cited text no. 14    
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23.Vinge E, Lindergard B, Nilsson-Ehle P,   Back to cited text no. 23    
24.Grubb A. Relationships among serum cystatin C, serum creatinine, lean tissue mass and glomerular filtration rate in healthy adults. Scand J Clin Lab Invest 1999;59 (8):587-92.  Back to cited text no. 24    
25.Slayden OD, Hettrich K, Carroll RS, Otto LN, Clark AL, Brenner AM. Estrogen enhances cystatin C expression in the macaque vagina. J Clin Endocrinol Metab 2004;89(2):883-91.  Back to cited text no. 25    
26.Lurban MM. Renal function in the elderly. Ann Clin Lab Sci 1995;25(2):122-33.  Back to cited text no. 26    
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29.Finney H, Bates CJ, Price CP. Plasma cystatin C determinations in a healthy elderly population. Arch Gerontol Geriatr 1999;29(1):75-9.  Back to cited text no. 29    
30.Keevil BG, Kilpatrick ES, Nichols SP, Maylor PW. Biological variation of cystatin C: Implications for the assessment of glomerular filtration rate. Clin Chem 1998;44(7):1535-9.  Back to cited text no. 30    
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32.Harmoinen A, Ylinen E, Ala-Houhala M, Janas M, Kaila M, Kouri T. Reference intervals for cystatin C in pre- and full-term infants and children. Pediatr Nephrol 2000;15(1-2):105-8.  Back to cited text no. 32    
33.Cataldi L, Mussap M, Bertelli L, Ruzzante N, Fanos V, Plebani M. Cystatin C in healthy women at term pregnancy and in their infant newborns: Relationship between maternal and neonatal serum levels and reverence values. Am J Perinatol 1999;16 (6):287-95.  Back to cited text no. 33    

Correspondence Address:
Jamal S Al Wakeel
Department of Medicine, King Khalid University Hospital, Riyadh
Saudi Arabia
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  [Figure - 1]

  [Table - 1], [Table - 2], [Table - 3], [Table - 4], [Table - 5], [Table - 6]

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