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Mineral bone disorder and osteoporosis in hemodialysis patients

Abstract

Background

Bone disease is common in patients undergoing hemodialysis. It is the result of bone turnover abnormalities and the decrease of bone mineral density (BMD). We aimed to determine the usefulness of serum bone turnover markers and BMD measurement by dual-energy x-ray absorptiometry (DXA) in hemodialysis patients.

Methods

We conducted a cross-sectional study including 90 hemodialysis for more than 12 months. Bone mineral density was assessed by DXA. Peripheral blood samples were obtained from each patient before dialysis in a fasting state within a week of the DXA. Biochemical variables of calcium and phosphate were measured. One bone formation marker (bone-specific alkaline phosphatase (bAP), one bone resorption marker (carboxy-terminal telopeptides of type 1 collagen (CTX)) were measured. Total alkaline phosphatase (TAP), intact parathyroid hormone (PTH) and fibroblast growth factor 23 (FGF23) which is a bone-derived hormone were also measured.

Results

CTX values were 6.25 times higher than the normal limit of the assay. Bone alkaline phosphatase levels were less than 10 ng/mL in 28.8% of cases. 23% of patients have osteoporosis and 45% have osteopenia. Femoral BMD had negative correlations with age and PTH levels. FGF23 levels were significantly increased in patients with osteoporosis affecting the lumbar. The levels of bAP and CTX showed a positive correlation. Both circulating bAP and CTX levels showed also positive correlations with PTH levels. Fractures, observed in 12.2% of cases, were associated with low PTH values and the existence of osteoporosis.

Conclusions

Our study showed that osteoporosis and fracture are common in dialysis patients. The reduced BMD was associated with advanced age and elevated levels of PTH. Markers of bone turnover and FGF23 may play a role in the diagnosis of bone disease in hemodialysis patients. DXA measurement is necessary for the monitoring for bone loss.

Background

Bone disease is highly prevalent in patients with chronic kidney disease on dialysis (CKD-5D) [1]. It can induce serious bone health problems, especially fragility fractures. Bone disease in patients with CKD-5D is the result of bone turnover abnormalities and the decrease of bone mineral density (BMD). Bone biopsy remains the gold standard for the diagnosis of bone turnover abnormalities. However, it is an invasive method and repetitive assessment of bone status cannot be possible. Measurements of serum bone turnover markers are not common practice in the management of CKD-5D patients [1]. Fibroblast growth factor-23 (FGF23) is a circulating factor produced by osteocytes. This hormone inhibits phosphate reabsorption and renal production of 1,25(OH) vitamin D. FGF23 regulates phosphate and vitamin D. This hormone plays an important role in bone metabolism of patients with chronic kidney disease [2]. Moreover, the assessment of bone mass in patients under dialysis is not yet codified. Both bone resorption and bone formation markers in patients with CKD-5D may be up- or down-regulated by systemic hormones such as parathormone. The measurement of BMD by dual-energy x-ray absorptiometry (DXA) is recommended only in patients with a history of fractures. Multiple factors are associated with reduced BMD and may affect bone health [3].

This study aimed to determine the usefulness of serum bone turnover markers by measuring one bone formation marker (bone-specific alkaline phosphatase) and one bone resorption marker (carboxy-terminal telopeptides of type 1 collagen) and the usefulness of the BMD by DXA in patients with CKD-5D. We aimed also to assess the frequency and risk factors of osteoporosis and osteoporotic fracture in hemodialysis patients.

Methods

Patients

We conducted a cross-sectional study including patients in maintenance hemodialysis three times weekly for more than 12 months.

Exclusion criteria included patients younger than 20 years, premature menopause (occurring before the age of 40), prolonged immobilization and patients receiving treatments related to mineral metabolism (long-term steroids, hormone replacement therapy, and bisphosphonate). Patients with a history of gastrectomy, parathyroidectomy, neoplasia or hysterectomy were excluded from this study. Patients with disease that may affect bone such as chronic inflammatory bowel disease, cirrhosis, and endocrinopathies except diabetes were also excluded.

Demographic and clinical data, including age, gender, anthropometric measurements, body mass index (weight/height2), comorbidities, menopausal status, etiology of kidney disease, and duration of dialysis were collected. We inquired also about low trauma fractures since starting dialysis.

Measurements of biochemical variables

Peripheral blood samples were obtained from each patient before dialysis in a fasting state within a week of the DXA. Biochemical variables of calcium and phosphate were measured using an in vitro photometric assay for automated clinical chemistry analyzers.

Plasma intact PTH (PTH) levels were measured using chemiluminescent microparticle immunoassay. Normal values range from 15-65 pg/mL.

Serum concentrations of 25(OH) vitamin D (25(OH)D) were measured using chemiluminescent immunoassay. Vitamin D deficiency was defined as 25(OH)D values lower than 10 ng/mL, vitamin D insufficiency was defined as 25(OH)D values between 10 and 30 ng/mL [4]. Recommended rates of vitamin D ranged between 30 and 70 ng/mL.

Bone alkaline phosphatase (bAP), a marker of osteoblastic activity, was measured using an immunosorbent enzyme-linked assay.

C-terminal telopeptide of type I collagen (CTX), a marker of osteoclastic activity, was measured by chemiluminescent immunoassay.

Fibroblast growth factor 23 (FGF23) was measured with the ELISA technique. Normal values range from 30 to 176 pg/mL.

Measurements of BMD

Dual-energy X-ray absorptiometry (DXA) was performed to assess bone mineral density (BMD). Instrument quality control was performed regularly. Bone mass density, expressed in gm/cm2, was measured at the lumbar spine, total hip, femoral neck, and total body.

In the lack of diagnostic criteria for defining osteoporosis in men and premenopausal women, we used WHO criteria as a cutoff point. Osteopenia corresponded to T-score more than − 2.5 SD but less than − 1 SD. Osteoporosis was defined as T-score less than or equal to − 2.5 SD in at least one of these sites: lumbar spine, femoral neck or total hip [5].

Fragility fractures

Fragility fractures were defined as fractures resulting from low-trauma (fall from standing-height or lower).

Lateral dorsal and lumbar spine X-rays were performed to assess vertebral fracture.

Statistical analysis

Statistical Package for Social Sciences (SPSS) version 19.0 was used to perform statistical analysis. Means and standard errors were calculated. Comparisons were performed using Student’s t-test and analysis of variance (ANOVA) for normally distributed variables. The chi-square test was used to analyze categorical data. The multiple linear regression was performed to identify predictors of low bone mass. The significance level was set at < 0.05. Correlations were reported as either the Pearson correlation coefficient.

Results

Patients’ characteristics

A total of 90 patients were included in the study. All of them were Caucasian. There were 58 men (64%) with a sex ratio of 1.8. The mean age was 53.01 years [20; 89]. Sixty-eight percent of patients were under the age of 50 years. There were 8 post-menopausal women. The duration of hemodialysis was less than 5 years in 61% of patients whereas it was more than 10 years in only two cases. The calcium intake was noted in 97% of cases with a mean dose of 1.89 g daily [0.5; 3]. Only 30% of patients were orally supplemented with 0.5 microg of alfacalcidol daily.

Hyperphosphatemia was noted in 62.22% and hypocalcemia was found also in 62.22%. Fifty-six percent of patients have PTH values between 2 and 9 times the upper normal limit of the assay. However, 19% of patients have PTH values less than 2 times the upper normal limit of the assay. Insufficiency and deficiency of vitamin D were found respectively in 41.11 and 44.44% of cases. CTX values were 6.25 times higher than the normal limit of the assay.

Only 6 patients had CTX levels within the normal range. Bone alkaline phosphatase levels were less than 10 ng/mL in 26 cases and higher than 25 ng/mL in 31 cases. Table 1 summarized the clinical and biological characteristics of patients.

Table 1 Clinical and biological characteristics of patients

Prevalence of osteoporotic fracture

Osteoporotic fractures were noted in 12.22% of cases (n = 11) and had occurred after the age of 50 years in 9 cases. Vertebral fractures are the most common type of osteoporotic fractures, found in 6 patients, followed by hip fractures noted in 3 cases. For the two other cases, there were wrist fracture and tibial fracture.

Prevalence of osteoporosis

As shown in Table 2, osteoporosis was common among patients undergoing hemodialysis. 23% of patients have osteoporosis and 45% have osteopenia. Osteoporosis affected the hip more than the spine.

Table 2 Results of bone mass in hemodialysis patients

Correlation between biological parameters

There was a positive correlation between bAP and CTX. Moreover, both bone markers showed positive correlations with serum PTH levels. Table 3 demonstrated correlations between biological parameters.

Table 3 Pearson’s correlation between biological parameters

Associated factors of BMD

As illustrated in Table 4, patients with osteoporosis were older than patients without osteoporosis. Men had higher DXA BMD than women at only the total body (1.160 ± 0.141 vs 1.053 ± 0.105 g/cm2, p< 10-3).

Table 4 Comparison of clinical and biological characteristics between patients with and without osteoporosis

The mean BMD was significantly lower among patients with a history of diabetes at the total hip femoral (0.894 ± 0.162 in patients with diabetes vs. 0.894 ± 0.162 in patients without diabetes, p: 0.003). Diabetic nephropathy was the most common etiology associated with decreased BMD at the femoral site whereas patients with polycystic kidney disease tended to have higher BMD than the other patients (0.789 ± 0.118 g/cm2 in patient with diabetic nephropathy vs. 0.980 ± 0.249 in patient with polycystic kidney disease, p: 0.031).

Parathyroid hormone levels were significantly increased in patients with osteoporosis affecting the total hip. Fibroblast growth factor 23 levels were significantly increased in patients with osteoporosis affecting the lumbar. However, vitamin D levels did not differ significantly between patients with and without osteoporosis.

The Pearson’s correlations between clinical, anthropometric, biological and BMD were presented in Table 5.

Table 5 Pearson’s correlation between clinical, anthropometric, biological and BMD

As shown in Table 6, age and PTH levels significantly predicted the total hip BMD.

Table 6 Predicting models of total hip BMD and total body BMD

Associated factors of fractures

As demonstrated in Table 7, PTH levels were significantly lower in patients with fractures. Besides, patients with osteoporosis had more osteoporotic fractures than patients without osteoporosis.

Table 7 Comparison between patients with and without osteoporotic fractures

Discussion

Patients with chronic kidney disease on dialysis (CKD-5D) are at increased risk of osteoporosis and fractures than the general population [6]. In this bone DXA densitometry-based study, we detected that osteoporosis was common in dialysis patients, observed in 23% of cases. Indeed, literature data showed that the prevalence of osteoporosis varied from 4 to 47% at the lumbar spine and from 10 to 64% at the femoral site [7,8,9,10,11,12,13,14,15]. Moreover, Avramovski et al. [16] demonstrated that the progression of bone mass loss was significantly greater in chronic hemodialysis patients than in general population patients. Using DXA assessment, Sit D et al. [13] showed that the lumbar spine was the region with the highest prevalence of osteoporosis. However, other studies are consistent with our study showing that osteoporosis affected the total hip (20%) more than the lumbar spine (9%). DXA technology can overestimate the BMD measured in the lumbar because of the existence of osteophytes and aortic calcification, frequently observed in hemodialysis patients [17].

Bone mass loss is considered as the consequence of several factors in hemodialysis patients. Several studies are consistent with our study showing that BMD decreased as age increased [14, 17, 18]. The effect of gender on bone mass in hemodialysis is controversial [19, 20]. We found that BMD was significantly lower in women at the total body. The impact of diabetes on BMD is not yet clear. According to the study of Elder et al., we found that BMD at total hip was lower among dialysis patients with diabetes [21].

Chronic kidney disease is associated with hyperphosphatemia and hypocalcemia, observed in 62.22% in our patients, and induce secondary hyperparathyroidism. Fifty-six percent of patients have PTH values between 2 and 9 times the upper normal limit of the assay as recommended by KDIGO [1]. Observational studies demonstrated that PTH values at the extremes (lower than 2 times and more than 9 times) are associated with an increased relative risk of death in dialysis patients. Nevertheless, until now, there is no reference range of PTH values corresponding with normal bone turnover [22]. As in our study, Taal et al. [7] showed that the total hip BMD had a negative correlation with PTH. Besides, TAP correlated negatively with BMD in the total body. We didn’t find an association between the serum albumin level and BMD. Even if Huang et al. [23] found a positive correlation between serum albumin levels and femoral neck BMD in dialysis patients. Lai et al. [24] showed that there was no relationship between these parameters.

Even if CTX is cleared by the kidney, our study showed that circulating bAP and CTX levels are correlated with serum PTH levels. Serum CTX levels have been found to predict bone loss in patients under dialysis [25, 26]. Several studies have also demonstrated that CTX concentrations are raised in patients with CKD-5D and correlate well with BMD measurements [27]. Moreover, Maeno et al. [26] reported that CTX levels significantly correlate with annual bone loss with sensitivity and specificity at respectively 41 and 83%.

Nevertheless, in another study, serum CTX levels were not different between patients with and without loss of BMD at the distal radius [28].

FGF23 plays an important role in regulating bone mineralization. In our study, FGF23 levels were significantly increased in patients with osteoporosis affecting the lumbar. High FGF23 levels were associated with reduced osteoid thickness in children undergoing dialysis [29]. However, in other studies, BMD was not correlated with serum FGF23 levels [30].

Insufficiency on vitamin D, observed in 41.11% in our study, is common among dialysis patients [31,32,33,34,35]. There has been much debate about the relationship between vitamin D and BMD. Several studies have demonstrated that low vitamin D level induced a decrease of cortical BMD in the presumed healthy adult [36]. Our study revealed a positive correlation between vitamin D levels and femoral BMD.

Fracture rates, observed in 12.1% in our study, are greatly increased in dialysis patients compared to the general population [37]. From our study, it is evident that lower PTH value was associated with an increased risk of osteoporotic fracture. It has been demonstrated that both high and low PTH levels can be associated with a high fracture rate [38, 39].

Another finding of interest in our study is that osteoporotic fractures were associated with the existence of osteoporosis. In a meta-analysis, Jamal et al. suggested that BMD is lower in patients with stage 5 CKD who have fractures [40]. The relationship between BMD measured by DXA and fracture in dialysis patients remains unclear.

There are numerous limitations to our study. First, it is a cross-sectional study. Besides, some other factors which might be associated with osteoporosis such as dosage of heparin and hypogonadism were not studied.

Conclusion

Our study showed that osteoporosis and fracture are common in patients under dialysis. We highlighted that bone mass loss is the consequence of several factors including age, diabetes and elevated levels of PTH. Osteoporotic fracture risk was associated with the existence of osteoporosis suggesting that DXA measurement is mandatory for the monitoring of bone loss. Our study showed also that both circulating bAP and CTX levels correlated positively with PTH levels. We suggest that bone metabolic markers including BAP and CTX may accurately reflect bone turnover. FGF23 levels were significantly increased in patients with lumbar osteoporosis. Certainly, FGF23 plays a role in the pathogenesis of bone disease in patients with CKD-5D. Other larger longitudinal studies are necessary to codify the assessment of bone disease.

Availability of data and materials

The datasets used and/or analysed during the current study are available from the corresponding author on reasonable request.

Abbreviations

25(OH)D:

25(OH) vitamin D

bAP:

bone-specific alkaline phosphatase

BMD:

Bone mineral density

CKD-5D:

Chronic kidney disease on dialysis

CTX:

Carboxy-terminal telopeptides of type 1 collagen

DXA:

Dual-energy x-ray absorptiometry

FGF23:

Fibroblast growth factor 23

PTH:

Intact parathyroid hormone

TAP:

Total alkaline phosphatase

References

  1. 1.

    Ketteler M, Block GA, Evenepoel P, Fukagawa M, Herzog CA, McCann L, Moe SM, Shroff R, Tonelli MA, Toussaint ND, Vervloet MG, Leonard MB. Diagnosis, evaluation, prevention, and treatment of chronic kidney disease-mineral and bone disorder: synopsis of the kidney disease: improving global outcomes 2017 clinical practice guideline update. Ann Intern Med. 2018;168(6):422–30.

    Article  Google Scholar 

  2. 2.

    Zheng S, Chen Y, Zheng Y, Zhou Z, Li Z. Correlation of serum levels of fibroblast growth factor 23 and Klotho protein levels with bone mineral density in maintenance hemodialysis patients. Eur J Med Res. 2018;23(1):18.

    Article  Google Scholar 

  3. 3.

    Gordon PL, Frassetto LA. Management of Osteoporosis in CKD stages 3 to 5. Am J Kidney Dis. 2010;55:941–56.

    Article  Google Scholar 

  4. 4.

    Dawson-Hugues B, Mithal A, Bonjour JP, Boonen S, Burckhardt P, Fuleihan GEH, Josse RG, Lips P, Morales-Torres J, Yoshimura N. IOF position statement: vitamin D recommendations for older adults. Osteoporos Int. 2010;21:1151–4.

    Article  Google Scholar 

  5. 5.

    Kanis JA, Glüer CC. An update on the diagnosis and assessment of osteoporosis with densitometry. Committee of Scientific Advisors, international Osteoporosis Foundation. Osteoporos Int. 2000;11:192–202.

    CAS  Article  Google Scholar 

  6. 6.

    Nickolas TL, Leonard MB, Shane E. Chronic kidney disease and bone fracture: a growing concern. Kidney Int. 2008;74(6):721–31.

    Article  Google Scholar 

  7. 7.

    Taal MW, Masud T, Green D, Cassidy MJ. Risk factors for reduced bone density in haemodialysis patients. Nephrol Dial Transplant. 1999;14:1922–8.

    CAS  Article  Google Scholar 

  8. 8.

    Fontaine MA, Albert A, Dubois B, Saint-Remy A, Rorive G. Fracture and bone mineral density in hemodialysis patients. Clin Nephrol. 2000;54:218–26.

    CAS  PubMed  Google Scholar 

  9. 9.

    Ureña P, Bernard-Poenaru O, Ostertag A, Baudoin C, Cohen-Solal M, Cantor T, de Vernejoul MC. Bone mineral density, biochemical markers and skeletal fractures in haemodialysis patients. Nephrol Dial Transplant. 2003;18:2325–31.

    Article  Google Scholar 

  10. 10.

    Yücel AE, Kart-Köseoglu H, Isiklar I, Kuruinci E, Ozdemir FN, Arslan H. Bone mineral density in patients on maintenance hemodialysis and effect of chronic hepatitis C virus infection. Ren Fail. 2004;26:159–64.

    Article  Google Scholar 

  11. 11.

    Mucsi I, Almasi C, Deak G, Marton A, Ambrus C, Berta K, et al. Serum 25(OH)-vitamin D levels and bone metabolism in patients on maintenance hemodialysis. Clin Nephrol. 2005;64:288–94.

    CAS  Article  Google Scholar 

  12. 12.

    Petrauskiene V, Petrauskienė V, Bumblytė IA, Šileikienė E, Gineikaitė R, Burbulytė R. Evaluation of bone mineral density and its importance for hemodialysis patients. Medicina. 2007;43:90–5.

    PubMed  Google Scholar 

  13. 13.

    Sit D, Kadiroglu AK, Kayabasi H, Atay AE, Yilmaz Z, Yilmaz ME. Relationship between bone mineral density and biochemical markers of bone turnover in hemodialysis patients. Adv Ther. 2007;24:987–95.

    CAS  Article  Google Scholar 

  14. 14.

    Avila M, Prado C, Ventura MJ, Mora C, Briones D, Valdez H, et al. Vitamin D receptor gene, biochemical bone markers and bone mineral density in Mexican women on dialysis. Nephrol Dial Transplant. 2010;25:2259–65.

    CAS  Article  Google Scholar 

  15. 15.

    Khan MI, Syed GM, Khan AI, Sirwal IA, Anwar SK, Al-Oufi AR, Balbaid KA. Mean bone mineral density and frequency of occurrence of osteopenia and osteoporosis in patients on hemodialysis: a single-center study. Saudi J Kidney Dis Transpl. 2013;25:38–43.

    Article  Google Scholar 

  16. 16.

    Avramovski P, Sikole A. The progression of bone mineral density loss in Dialysis patients compared with the general population. Korean J Intern Med. 2012;27:436–42.

    CAS  Article  Google Scholar 

  17. 17.

    Toussaint ND, Lau KK, Strauss BJ, Polkinghorne KR, Kerr PG. Associations between vascular calcification, arterial stiffness and bone mineral density in chronic kidney disease. Nephrol Dial Transplant. 2008;23:586–93.

    Article  Google Scholar 

  18. 18.

    Malluche HH, Davenport DL, Cantor T, Monier-Faugere MC. Bone mineral density and serum biochemical predictors of bone loss in patients with CKD on dialysis. Clin J Am Soc Nephrol. 2014;9(7):1254–62.

    CAS  Article  Google Scholar 

  19. 19.

    Nybo M, Jespersen B, Aarup M, Ejersted C, Hermann AP, Brixen K. Determinants of bone mineral density in patients on haemodialysis or peritoneal dialysis--across-sectional, longitudinal study. Biochem Med. 2013;23(3):342–50.

    CAS  Article  Google Scholar 

  20. 20.

    Valkovsky I, Olsanska R, Tvrdik J, Martinek A, Svagera Z, Pernicova M, Dedochova J, Cermakova Z. Evaluation of biochemical markers and bone mineral density in patients with chronic kidney disease stage 5D at the start of hemodialysis treatment. Biomed Pap Med Fac Univ Palacky Olomouc Czech Repub. 2015;159(1):93–9.

    Article  Google Scholar 

  21. 21.

    Elder GJ, Mackun K. 25-Hydroxyvitamin D Deficiency and Diabetes Predict Reduced BMD in Patients With Chronic Kidney Disease. J Bone Miner Res. 2006;21:1778–84.

    CAS  Article  Google Scholar 

  22. 22.

    Souberbielle JP, Roth H, Fouque DP. Parathyroid hormone measurement in CKD. Kidney Int. 2010;77:93–100.

    CAS  Article  Google Scholar 

  23. 23.

    Huang GS, Chu TS, Lou MF, Hwang SL, Yang RS. Factors associated with low bone mass in the hemodialysis patients—a cross-sectional correlation study. BMC Musculoskelet Disord. 2009;10:60.

    Article  Google Scholar 

  24. 24.

    Lai MN, Hsu IS, Chen YY, Gee MJ, Kao MT. Osteoporosis and associated risk factors for chronic hemodialysis patients. Acta Nephrol. 2002;16:25–30.

    Google Scholar 

  25. 25.

    Okuno S, Inaba M, Kitatani K, Ishimura E, Yamakawa T, Nishizawa Y. Serum levels of C-terminal telopeptide of type I collagen: a useful new marker of cortical bone loss in hemodialysis patients. Osteoporos Int. 2005;16:501–9.

    CAS  Article  Google Scholar 

  26. 26.

    Maeno Y, Inaba M, Okuno S, Yamakawa T, Ishimura E, Nishizawa Y. Serum concentrations of cross-linked N-telopeptides of type I collagen: new marker for bone resorption in hemodialysis patients. Clin Chem. 2005;51:2312–7.

    CAS  Article  Google Scholar 

  27. 27.

    Herrmann M, Seibel MJ. The amino- and carboxyterminal cross-linked telopeptides of collagen type I, NTX-I and CTX-I: a comparative review. Clin Chim Acta. 2008;393(2):57–75.

    CAS  Article  Google Scholar 

  28. 28.

    Ueda M, Inaba M, Okuno S, Maeno Y, Ishimura E, Yamakawa T, Nishizawa Y. Serum BAP as the clinically useful marker for predicting BMD reduction in diabetic hemodialysis patients with low PTH. Life Sci. 2005;77:1130–9.

    CAS  Article  Google Scholar 

  29. 29.

    Bacchetta J, Cochat P, Salusky IB, Wesseling-Perry K. Uric acid and IGF1 as possible determinants of FGF23 metabolism in children with normal renal function. Pediatr Nephrol. 2012;27:1131–8.

    Article  Google Scholar 

  30. 30.

    Urena Torres P, Friedlander G, de Vernejoul MC, Silve C, Prié D. Bone mass does not correlate with the serum fibroblast growth factor 23 in hemodialysis patients. Kidney Int. 2008;73:102–7.

    CAS  Article  Google Scholar 

  31. 31.

    Wolf M, Shah A, Gutierrez O, Ankers E, Monroy M, Tamez H, et al. Vitamin D levels and early mortality among incident hemodialysis patients. Kidney Int. 2007;72:1004–13.

    CAS  Article  Google Scholar 

  32. 32.

    Jean G, Charra B, Chazot C. Vitamin D deficiency and associated factors in hemodialysis patients. J Ren Nutr. 2008;18:395–9.

    Article  Google Scholar 

  33. 33.

    Seck SM, Cisse MM, Ka EF, Doupa D. Epidemiology of vitamin D deficiency in west African hemodialysis patients: a pilot study from Senegal. Indian J Nephrol. 2014;24:27–128.

    Article  Google Scholar 

  34. 34.

    Krassilnikova M, Ostrow K, Bader A, Heeger P, Mehrotra A. Low dietary intake of vitamin D and vitamin D deficiency in hemodialysis patients. J Nephrol Ther. 2014;4. https://doi.org/10.4172/2161-0959.1000166.

  35. 35.

    Drechsler C, Verduijn M, Pilz S, Dekker FW, Krediet RT, Ritz E, et al. Vitamin D status and clinical outcomes in incident dialysis patients: results from the NECOSAD study. Nephrol Dial Transplant. 2011;26:1024–32.

    CAS  Article  Google Scholar 

  36. 36.

    Guinota C, Ezzedinec K, Maugera E, Ambroisinea L, Latreillea J, Bertraisd S, et al. Phototype, vitamin D status and bone mineral density among women at risk of osteoporosis. Rev Med Intern. 2006;27:369–74.

    Article  Google Scholar 

  37. 37.

    Pimentel A, Ureña-Torres P, Zillikens MC, Bover J, Cohen-Solal M. Fractures in patients with CKD-diagnosis, treatment, and prevention: a review by members of the European calcified tissue society and the European renal Association of Nephrology Dialysis and Transplantation. Kidney Int. 2017;92(6):1343–55.

    Article  Google Scholar 

  38. 38.

    Guh JY, Chen HC, Chuang HY, Huang SC, Chien LC, Lai YH. Risk factors and risk for mortality of mild hypoparathyroidism in hemodialysis patients. Am J Kidney Dis. 2002;39:1245–54.

    Article  Google Scholar 

  39. 39.

    Lertdumrongluk P, Lau WL, Park J, Rhee CM, Kovesdy CP, Kalantar-Zadeh K. Impact of age on survival predictability of bone turnover markers in hemodialysis patients. Nephrol Dial Transplant. 2013;28:2535–45.

    CAS  Article  Google Scholar 

  40. 40.

    Jamal SA, Hayden JA, Beyene J. Low bone mineral density and fractures in long-term hemodialysis patients: a meta-analysis. Am J Kidney Dis. 2007;49(5):674–81.

    Article  Google Scholar 

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MS has drafted the work. HS has substantively revised the work. AB has made substantial contributions to the analysis of data. LL has made substantial contributions to the interpretation of data. WS, SR, IG and MS have made substantial contributions to the acquisition of data. FBM has made substantial contributions to the design of the work. ME has approved the submitted version. EC has made substantial contributions to the conception of the work. All authors read and approved the final manuscript.

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Correspondence to Maroua Slouma.

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Slouma, M., Sahli, H., Bahlous, A. et al. Mineral bone disorder and osteoporosis in hemodialysis patients. Adv Rheumatol 60, 15 (2020). https://doi.org/10.1186/s42358-020-0118-0

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Keywords

  • Osteoporosis
  • Hemodialysis
  • Fracture
  • Bone mineral density
  • Fibroblast growth factor 23
  • Bone specific alkaline phosphatase
  • Carboxy-terminal telopeptide of type 1 collagen