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Metabolic bone disease in children and adolescent patients with ulcerative colitis

Abstract

Objective:

Metabolic bone disease concerns a broad spectrum of conditions related to reduced bone density. Metabolic bone disease has been linked to chronic inflammatory diseases, such as ulcerative colitis. This study examines the prevalence of metabolic bone disease in ulcerative colitis patients and explores possible clinical predictors.

Method:

The authors performed a retrospective study involving children and adolescents with confirmed ulcerative colitis between January 2013 and December 2018. Bone density was evaluated through a dual-energy X-ray absorptiometry scan of the spine and total body. Osteoporosis was defined as a bone mineral density Z-score of <−2 and osteopenia as a Z-score of between −1.0 and −2.

Results:

A total of 37 patients were included in this analysis, with a mean age of 13.4 ± 3.9 years and a mean duration of illness of 2.1 ± 2.4 years. Using lumbar spine Z-scores and total body Z-scores, osteoporosis and osteopenia were identified by dual-energy X-ray absorptiometry scan measurements in 11 patients (29.7%) and 15 patients (40.5%), and in ten patients (27%) and 13 patients (35%), respectively. Lumbar spine Z-scores were significantly positively associated with male gender (B = 2.02; p = 0.0001), and negatively associated with the presence of extraintestinal manifestations (B = −1.51, p = 0.009) and the use of biologics (B = −1.33, p = 0.004). However, total body Z-scores were positively associated with body mass index Z-scores (B = 0.26, p = 0.004) and duration of illness in years (B = 0.35, p = 0.003).

Conclusions:

Metabolic bone disease is very common in this cohort of Saudi Arabian children and adolescents with ulcerative colitis and its occurrence appears to increase in female patients who suffer from extraintestinal manifestations.

KEYWORDS
Ulcerative colitis; Osteoporosis; Bone mineral density; Predictors; Children; Saudi Arabia

Introduction

Ulcerative colitis (UC) is a chronic inflammatory condition known for its relapsing and remitting course that exclusively affects the large intestine.11 Fumery M, Singh S, Dulai PS, Gower-Rousseau C, Peyrin-Biroulet L, Sandborn WJ. Natural history of adult ulcerative colitis in population-based cohorts: a systematic review. Clin Gastroenterol Hepatol. 2018;16, 343-56.e3.2. UC has clinical characteristics that differ from the other main subtype of inflammatory bowel disease (IBD), Crohn's disease (CD), which can involve any part of the gastrointestinal tract. Patients with UC tend to complain of bloody diarrhea and tenesmus, and are less likely to have abdominal pain and malnutrition. Moreover, UC typically demonstrates continuous inflammation of the colonic mucosa, and almost always involves the rectum on endoscopy, whereas CD is known to be a patchy disease that often does not concern the rectum.22 Torres J, Mehandru S, Colombel JF, Peyrin-Biroulet L. Crohn's disease. Lancet. 2017;389:1741-55. There are also a number of other diagnostic differences between the two diseases, with correspondingly diverse therapeutic strategies. In recent years, treatment of IBD has evolved to encompass more personalized approaches that not only focus on treating symptoms, but address objective markers of inflammation and determinants of quality of life.33 Floyd DN, Langham S, Severac HC, Levesque BG. The economic and quality-of-life burden of Crohn's disease in Europe and the United States, 2000 to 2013: a systematic review. Dig Dis Sci. 2015;60:299-312. Furthermore, one of the main objectives of treatment in children and adolescents is fulfilling the ability to thrive normally.44 Belli DC, Seidman E, Bouthillier L, Weber AM, Roy CC, Pletincx M, et al. Chronic intermittent elemental diet improves growth failure in children with Crohn's disease. Gastroenterology. 1988;94:603-10.

The management of UC currently utilizes more personalized approaches based on multidisciplinary team interactions.55 Sun YN, Feng XY, He L, Zeng LX, Hao ZM, Lv XH, et al. Prevalence and possible risk factors of low bone mineral density in untreated female patients with systemic lupus erythematosus. Biomed Res Int. 2015;2015:510514. Extraintestinal manifestations (EIMs) can occur in up to 70% of patients with IBD. EIMs include musculoskeletal complaints such as arthralgia and arthritis, sacroiliitis, and ankylosing spondylitis.66 Peyrin-Biroulet L, Loftus EV, Colombel JF, Sandborn WJ. Long-term complications, extraintestinal manifestations, and mortality in adult Crohn's disease in population-based cohorts. Inflamm Bowel Dis. 2011;17:471-8. EIMs can also involve the skin, eyes, and hepatobiliary tract, and involve micro- and macro-nutrient deficiencies, such as vitamin D deficiency.66 Peyrin-Biroulet L, Loftus EV, Colombel JF, Sandborn WJ. Long-term complications, extraintestinal manifestations, and mortality in adult Crohn's disease in population-based cohorts. Inflamm Bowel Dis. 2011;17:471-8. In adults, concerns regarding fertility, employment, and social productivity are often addressed.77 Reilly MC, Gerlier L, Brabant Y, Brown M. Validity, reliability, and responsiveness of the work productivity and activity impairment questionnaire in Crohn's disease. Clin Ther. 2008;30:393-404. However, for both children and adolescents, growth is a primary concern.44 Belli DC, Seidman E, Bouthillier L, Weber AM, Roy CC, Pletincx M, et al. Chronic intermittent elemental diet improves growth failure in children with Crohn's disease. Gastroenterology. 1988;94:603-10.,88 Schmidt S, Mellstrom D, Norjavaara E, Sundh SV, Saalman R. Low bone mineral density in children and adolescents with inflammatory bowel disease: a population-based study from Western Sweden. Inflamm Bowel Dis. 2009;15:1844-50. The ability to grow adequately requires an intact pituitary-hypothalamic axis and a healthy musculoskeletal system that reacts properly to hormonal stimulation. In the presence of chronic inflammation, both of these elements are affected, and hence younger patients with chronic inflammatory conditions are susceptible to growth failure.55 Sun YN, Feng XY, He L, Zeng LX, Hao ZM, Lv XH, et al. Prevalence and possible risk factors of low bone mineral density in untreated female patients with systemic lupus erythematosus. Biomed Res Int. 2015;2015:510514.,99 Pineau CA, Urowitz MB, Fortin PJ, Ibanez D, Gladman DD. Osteoporosis in systemic lupus erythematosus: factors associated with referral for bone mineral density studies, prevalence of osteoporosis and factors associated with reduced bone density. Lupus. 2004;13:436-41. Tight control of the disease through highly effective therapies in addition to frequent surveillance for malnutrition or metabolic bone disease (MBD) is necessary; otherwise, these derangements can go unnoticed and ultimately result in growth failure.88 Schmidt S, Mellstrom D, Norjavaara E, Sundh SV, Saalman R. Low bone mineral density in children and adolescents with inflammatory bowel disease: a population-based study from Western Sweden. Inflamm Bowel Dis. 2009;15:1844-50. Many inflammatory conditions, including IBD, have been associated with MBD, including osteopenia and osteoporosis.55 Sun YN, Feng XY, He L, Zeng LX, Hao ZM, Lv XH, et al. Prevalence and possible risk factors of low bone mineral density in untreated female patients with systemic lupus erythematosus. Biomed Res Int. 2015;2015:510514.,99 Pineau CA, Urowitz MB, Fortin PJ, Ibanez D, Gladman DD. Osteoporosis in systemic lupus erythematosus: factors associated with referral for bone mineral density studies, prevalence of osteoporosis and factors associated with reduced bone density. Lupus. 2004;13:436-41.,1010 Miranda-Bautista J, Verdejo C, Diaz-Redondo A, Breton I, Bellon JM, Perez-Valderas MD, et al. Metabolic bone disease in patients diagnosed with inflammatory bowel disease from Spain. Therap Adv Gastroenterol. 2019;12, 1756284819862152. The mechanisms behind this association include the effect of circulating pro-inflammatory cytokines, enhanced osteoclastic activity, the use of corticosteroids, and vitamin D deficiency.1010 Miranda-Bautista J, Verdejo C, Diaz-Redondo A, Breton I, Bellon JM, Perez-Valderas MD, et al. Metabolic bone disease in patients diagnosed with inflammatory bowel disease from Spain. Therap Adv Gastroenterol. 2019;12, 1756284819862152.1717 Tsai MS, Lin CL, Tu YK, Lee PH, Kao CH. Risks and predictors of osteoporosis in patients with inflammatory bowel diseases in an Asian population: a nationwide population-based cohort study. Int J Clin Pract. 2015;69:235-41. This association carries many implications owing to the potential for increased morbidity and a significant impact on quality of life, especially in younger patients who often fail to grow adequately.1818 Hidalgo DF, Boonpheng B, Phemister J, Hidalgo J, Young M. Inflammatory bowel disease and risk of osteoporotic fractures: a meta-analysis. Cureus. 2019;11:e5810. Thus, the ability to predict the presence of MBD in patients with IBD is an important part of the clinical assessment of these patients in order to facilitate optimal treatment. In children, some studies have suggested that patients with IBD are more prone to developing MBD than healthy controls.1919 Gupta A, Paski S, Issenman R, Webber C. Lumbar spine bone mineral density at diagnosis and during follow-up in children with IBD. J Clin Densitom. 2004;7:290-5. In the study by Gupta et al., lumbar spine bone mineral density (BMD) Z-score was reduced for CD patients as compared to controls, but there was a similar BMD Z-score between UC patients and controls. There is currently limited data evaluating MBD in pediatric IBD patients.2020 Carroll MW, Kuenzig ME, Mack DR, Otley AR, Griffiths AM, Kaplan GG, et al. The impact of inflammatory bowel disease in Canada 2018: children and adolescents with IBD. J Can Assoc Gastroenterol. 2019;2:S49-67.

Since the prevalence of MBD in UC is not as well studied as MBD in CD,88 Schmidt S, Mellstrom D, Norjavaara E, Sundh SV, Saalman R. Low bone mineral density in children and adolescents with inflammatory bowel disease: a population-based study from Western Sweden. Inflamm Bowel Dis. 2009;15:1844-50. this study was conducted to report on the prevalence of osteoporosis and osteopenia in a cohort of Saudi Arabian children and adolescents diagnosed with UC, and to identify possible predictors of low BMD based on dual-energy X-ray absorptiometry (DEXA) scanning.

Materials and methods

Study participants

The authors conducted a retrospective analysis of all patients diagnosed with UC at King Abdulaziz University Hospital and treated in the same hospital between January 2013 and December 2018. The diagnosis of UC was based on conventional clinical, endoscopic, and histological criteria.2121 Turner D, Travis SP, Griffiths AM, Ruemmele FM, Levine A, Benchimol EI, et al. Consensus for managing acute severe ulcerative colitis in children: a systematic review and joint statement from ECCO, ESPGHAN, and the Porto IBD Working Group of ESPGHAN. Am J Gastroenterol. 2011;106:574-88. All data concerning demographics, disease characteristics, history of surgical resections, laboratory results at the time of the DEXA scan, and prescribed medications were collected and entered into a standard data entry sheet. C-reactive protein (CRP) was determined by the nephelometry method, serum albumin by using bromocresol purple (BCP), serum calcium by the o-cresolphthalein complexone method, serum phosphate by the molybdate ultraviolet method, and 25-hyroxyvitamin D and parathyroid hormone (PTH) by using the immunoassay method.

BMD measurements

BMD was measured using DEXA (Hologic, QDR 4500; Hologic Inc. – Bedford, Massachusetts, United States) scans at the radiology department at King Abdulaziz University Hospital, Jeddah, Saudi Arabia. The results were expressed as BMD Z-scores from different regions of the musculoskeletal system, including femoral neck, lumbar spine (L1-4), and total body (excluding the head). Lumbar spine and total body scans have been more commonly utilized for BMD evaluation in children,2222 Nobile S, Grand RJ, Pappa HM. Risk factors for low bone mineral density in pediatric inflammatory bowel disease: the positive role of physical activity. Eur J Gastroenterol Hepatol. 2018;30:471-6. hence it was decided to use them in this study. Femoral head Z-score was not used in the analysis of BMD given that previous literature has suggested that this region is not reflective of actual BMD in children.2323 Crabtree NJ, Arabi A, Bachrach LK, Fewtrell M, El-Hajj Fuleihan G, Kecskemethy HH, et al. Dual-energy X-ray absorptiometry interpretation and reporting in children and adolescents: the revised 2013 ISCD Pediatric Official Positions. J Clin Densitom. 2014;17:225-42. Osteoporosis was defined as a BMD Z-score of <−2 and osteopenia as a Z-score of between −1.0 and −2, which is in accordance with the guidelines of the International Society for Clinical Densitometry (ISCD).2424 Bishop N, Arundel P, Clark E, Dimitri P, Farr J, Jones G, et al. Fracture prediction and the definition of osteoporosis in children and adolescents: the ISCD 2013 Pediatric Official Positions. J Clin Densitom. 2014;17:275-80.

Anthropometric measurements

At the time of the DEXA scan, the patients’ weight (in kg) and height (in cm) were measured with a digital weighing scale (which was calibrated daily) and a standard wall-fixed stadiometer. Following this, the body mass index (BMI) was calculated.

Using the anthropometric statistical software program Epi Info (Centers for Disease Control and Prevention – Atlanta, GA, United States), weight and height measurements were converted into standard deviations (SDs) and Z-scores.

Statistical analysis

Baseline characteristics of the cohort were summarized. Frequencies with percentages were used to present categorical data, and means with SDs or medians with interquartile ranges (IQRs), according to the distribution, were used for numerical variables. Univariate analysis was performed using the chi-squared test or Fisher's exact test to compare categorical variables, and Student's t-test or the Mann–Whitney U-test were used to compare summary statistics of numerical variables, according to the distribution. The authors used pairwise correlation to examine the linear relationship between the BMD Z-scores of the total body and the lumbar spine scans. Pearson's correlation coefficient (r) was used to express the degree of correlation. A backward and forward stepwise regression elimination model was used to identify predictors of total and lumbar spine Z-scores. Statistical significance was set at a p-value of <0.05. Statistical analysis was conducted using Stata 2011. (Stata Statistical Software: Release 12; StataCorp LP – College Station, TX, United States)..

Ethical consideration

Approval for this study was granted by the Ethical Research Committee of the Biomedical Ethics Unit at King Abdulaziz University Hospital, Jeddah (Reference No. 801-12) prior to its commencement. Standard ethical considerations were followed in accordance with the Declaration of Helsinki.

Results

Baseline characteristics

A total of 37 patients were included in this analysis with a mean age of 13.4 ± 3.9 years and a mean duration of illness of 2.1 ± 2.4 years. The majority of patients were females (n = 19, 51.4%) and eight patients (21.6%) reported positive parenteral consanguinity. The vast majority had extensive colitis (n = 31, 83.8%) and the mean BMI Z-score was 0.35 ± 6.2. Three patients reported EIMs (8%) and 29 patients (78.4%) reported using corticosteroids, with an average number of courses of 3.6 ± 2.7. Mesalamine derivatives were used by most patients (n = 36, 97.3%) and anti-tumor necrosis factor (TNF) therapy by only seven patients (18.9%). Anti-TNF therapies used included infliximab (n = 1) and adalimumab (n = 6). Twenty-seven patients (73%) reported using AZA as a therapy. Baseline characteristics are summarized in Table 1.

Table 1
Baseline characteristics of the study cohort at the time of osteoporosis screening (n = 37).

Study outcomes

Metabolic bone disease

Using lumbar spine Z-scores and total body Z-scores, osteoporosis and osteopenia were identified in 11 patients (29.7%) and 15 patients (40.5%), and in ten patients (27%) and 13 patients (35%), respectively. More patients without osteoporosis (n = 7/26, 26.9%) were treated with anti-TNF therapies compared to patients with osteoporosis (0/11, 0%) (p = 0.056). Aside from these, no significant differences were detected between the two groups (Table 2).

Table 2
Bivariate analysis of patients with and without osteoporosis according to lumbar spine Z-scores.

Predictors of body mass density

Using the stepwise regression elimination model, lumbar spine Z-scores were significantly positively associated with male gender (B coef. = 2.02; 95% CI = 1.27 to 2.76, p = 0.0001), and negatively associated with the presence of EIMs (B coef. = −1.51, 95% CI = −2.61 to −0.42, p = 0.009) and the use of biologics (B coef. = −1.33, 95% CI = −2.18 to −0.47, p = 0.004). However, total body Z-scores were positively associated with BMI Z-scores (B coef. = 0.26, 95% CI = −0.09 to 0.42, p = 0.004), and duration of illness in years (B coef. = 0.35, 95% CI = 0.14 to 0.58, p = 0.003; Table 3).

Table 3
Final predictive models according to stepwise elimination selection model for lumbar and total body Z-scores.

Correlation between lumbar spine and total body BMD Z-scores

Pairwise correlation between lumbar and total body Z-scores demonstrated a positive linear relationship between the two measurements (r = 0.54, p = 0.0005; Fig. 1).

Figure 1
Correlation between lumbar spine and total body Z-scores.

Discussion

Growth failure is a common complication among children with IBD that occurs more frequently in CD compared to UC.1212 Guz-Mark A, Rinawi F, Egotubov O, Shimon I, Shamir R, Assa A. Pediatric-onset inflammatory bowel disease poses risk for low bone mineral density at early adulthood. Dig Liver Dis. 2017;49:639-42. A meta-analysis of seven cross-sectional and cohort studies reported a significant association between adulthood IBD and osteoporosis, with a pooled OR of 1.32 (95% CI, 1.2 to 1.4).1818 Hidalgo DF, Boonpheng B, Phemister J, Hidalgo J, Young M. Inflammatory bowel disease and risk of osteoporotic fractures: a meta-analysis. Cureus. 2019;11:e5810. Previous studies have reported high prevalence rates of MBD in children and adolescents suffering from CD1717 Tsai MS, Lin CL, Tu YK, Lee PH, Kao CH. Risks and predictors of osteoporosis in patients with inflammatory bowel diseases in an Asian population: a nationwide population-based cohort study. Int J Clin Pract. 2015;69:235-41. but similar studies for UC are sparse.1616 Szafors P, Che H, Barnetche T, Morel J, Gaujoux-Viala C, Combe B, et al. Risk of fracture and low bone mineral density in adults with inflammatory bowel diseases. A systematic literature review with meta-analysis. Osteoporos Int. 2018;29:2389-97. A Spanish study that included a large cohort of IBD patients (n = 612 patients, 58.6% had CD) reported that male gender, menopausal women, and patients with UC to be at risk for osteoporosis, whereas older age, more than three IBD-related hospitalizations, and previous steroid treatment were associated with MBD in general.1010 Miranda-Bautista J, Verdejo C, Diaz-Redondo A, Breton I, Bellon JM, Perez-Valderas MD, et al. Metabolic bone disease in patients diagnosed with inflammatory bowel disease from Spain. Therap Adv Gastroenterol. 2019;12, 1756284819862152. For this reason, the present study specifically examined the prevalence of MBD in a Saudi Arabian cohort of patients with UC. However, prevalence of MBD is site-dependent, and therefore varies according to the type of score used (t-score or Z-score).1111 Abrahamsen B, Hansen TB, Jensen LB, Hermann AP, Eiken P. Site of osteodensitometry in perimenopausal women: correlation and limits of agreement between anatomic regions. J Bone Miner Res. 1997;12:1471-9. A previous study by Ismail et al. examined the prevalence of MBD in 95 adult patients with IBD and reported a prevalence rate of osteopenia of 44.2%, and osteoporosis of 30.5%, based on measurements made by both lumbar spine and proximal femur Z-scores. Higher Z-scores were associated with BMI, age, and calcium supplementation.1414 Ismail MH, Al-Elq AH, Al-Jarodi ME, Azzam NA, Aljebreen AM, Al-Momen SA, et al. Frequency of low bone mineral density in Saudi patients with inflammatory bowel disease. Saudi J Gastroenterol. 2012;18:201-7. Another study that examined a number of EIMs in 120 Indian patients with IBD reported a prevalence rate of osteoporosis or osteopenia of 50%, and higher rates of EIMs for females, Hindu religion, severe disease, and steroid usage.2525 Bandyopadhyay D, Bandyopadhyay S, Ghosh P, De A, Bhattacharya A, Dhali GK, et al. Extraintestinal manifestations in inflammatory bowel disease: prevalence and predictors in Indian patients. Indian J Gastroenterol. 2015;34:387-94. Furthermore, data from a previous retrospective analysis of patients with intestinal failure reported an MBD rate of 50% and good agreement between total body and lumbar Z-scores.1515 Neelis E, Rijnen N, Sluimer J, Olieman J, Rizopoulos D, Wijnen R, et al. Bone health of children with intestinal failure measured by dual energy X-ray absorptiometry and digital X-ray radiogrammetry. Clin Nutr. 2018;37:687-94. It is noted that BMD measurements of different parts of the skeleton can give varying results, since bone loss is not a homogenous process.2626 Franck H, Munz M. Total body and regional bone mineral densitometry (BMD) and soft tissue measurements: correlations of BMD parameter to lumbar spine and hip. Calcif Tissue Int. 2000;67:111-5. This may be related to the fact that lumbar spine mainly consists of trabecular bone, whereas the bone of the total body consists of 80% cortical bone.2626 Franck H, Munz M. Total body and regional bone mineral densitometry (BMD) and soft tissue measurements: correlations of BMD parameter to lumbar spine and hip. Calcif Tissue Int. 2000;67:111-5. It was found that the rate of MBD in the present cohort, of osteoporosis (29.7%) and osteopenia (40.5%) according to lumbar spine Z-scores in adults with IBD, is broadly in line with previous reports.1414 Ismail MH, Al-Elq AH, Al-Jarodi ME, Azzam NA, Aljebreen AM, Al-Momen SA, et al. Frequency of low bone mineral density in Saudi patients with inflammatory bowel disease. Saudi J Gastroenterol. 2012;18:201-7.

Osteoporosis and osteopenia are commonly associated with female gender, corticosteroid use, surgical resections, and vitamin D deficiency in adults with IBD.1313 Herzog D, Bishop N, Glorieux F, Seidman EG. Interpretation of bone mineral density values in pediatric Crohn's disease. Inflamm Bowel Dis. 1998;4:261-7.,2727 Bischoff-Ferrari HA, Kiel DP, Dawson-Hughes B, Orav JE, Li R, Spiegelman D, et al. Dietary calcium and serum 25-hydroxyvitamin D status in relation to BMD among U.S. adults. J Bone Miner Res. 2009;24:935-42.2929 Sohn J, Chang EJ, Yang HR. Vitamin D status and bone mineral density in children with inflammatory bowel disease compared to those with functional abdominal pain. J Korean Med Sci. 2017;32:961-7. The present study sought to identify predictors of MBD in children and adolescents with UC. A stepwise regression elimination model using both lumbar spine and total body Z-scores as dependent variables identified male gender (B coef. = 2.02; 95% CI = 1.27 to 2.76, p = 0.0001), the presence of EIMs (B coef. = −1.51, 95% CI = −2.61 to −0.42, p = 0.009), and the use of biologics (B coef. = −1.33, 95% CI = −2.18 to −0.47, p = 0.004) to be positively and negatively associated with lumbar spine Z-scores, respectively. Total body Z-scores were positively associated with BMI Z-scores (B coef. = 0.26, 95% CI = −0.09–0.42, p = 0.004), and duration of illness in years (B coef. = 0.35, 95% CI = 0.14 to 0.58, p = 0.003). The propensity for females to develop MBD is in line with previously published literature.1616 Szafors P, Che H, Barnetche T, Morel J, Gaujoux-Viala C, Combe B, et al. Risk of fracture and low bone mineral density in adults with inflammatory bowel diseases. A systematic literature review with meta-analysis. Osteoporos Int. 2018;29:2389-97.,2222 Nobile S, Grand RJ, Pappa HM. Risk factors for low bone mineral density in pediatric inflammatory bowel disease: the positive role of physical activity. Eur J Gastroenterol Hepatol. 2018;30:471-6. The negative association between higher Z-scores and other EIMs and the use of biologics could be a surrogate marker of severity, since patients with EIMs and those with UC who require biologics are more likely to have severe disease, which predisposes to MBD. A possible explanation of why patients with longer duration of disease tend to have higher Z-scores is that as patients grow older, they automatically have higher Z-scores.

Previous data from Rajaei et al. has suggested that total body Z-scores underestimate site-specific DEXA scan measurements.3030 Rajaei A, Dehghan P, Ariannia S, Ahmadzadeh A, Shakiba M, Sheibani K. Correlating whole-body bone mineral densitometry measurements to those from local anatomical sites. Iran J Radiol. 2016;13:e25609. The present results support this notion, since osteopenia defined by total body Z-scores was calculated to be 27%, but was 29.7% according to the lumbar spine Z-scores. A study by Moreira et al. revealed good inter-rater reliability between DEXA scan measurements from various anatomical sites.3131 Moreira OC, Oliveira CE, De Paz JA. Dual energy X-ray absorptiometry (DXA) reliability and intraobserver reproducibility for segmental body composition measuring. Nutr Hosp. 2018;35:340-5. However, to the authors’ knowledge, no studies have directly correlated total body and lumbar spinal Z-scores. Based on the present analysis, a moderate linear correlation exists between these two types of measurements (r = 0.54, p = 0.0005).

It is noteworthy that the current study is limited by its retrospective design, short duration of follow-up, and small sample size. The authors therefore recommend interpreting these results with caution.

In conclusion, MBD is very common in children with UC and its occurrence was found to be greater in female patients who suffer from EIMs. Future studies could focus on establishing more reliable predictive models for MBD in child and adolescent patients with UC.

Acknowledgments

The authors acknowledge Dr. Trevor Rawbone, Cardiff, UK for the English proofreading of the manuscript.

References

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    Fumery M, Singh S, Dulai PS, Gower-Rousseau C, Peyrin-Biroulet L, Sandborn WJ. Natural history of adult ulcerative colitis in population-based cohorts: a systematic review. Clin Gastroenterol Hepatol. 2018;16, 343-56.e3.2.
  • 2
    Torres J, Mehandru S, Colombel JF, Peyrin-Biroulet L. Crohn's disease. Lancet. 2017;389:1741-55.
  • 3
    Floyd DN, Langham S, Severac HC, Levesque BG. The economic and quality-of-life burden of Crohn's disease in Europe and the United States, 2000 to 2013: a systematic review. Dig Dis Sci. 2015;60:299-312.
  • 4
    Belli DC, Seidman E, Bouthillier L, Weber AM, Roy CC, Pletincx M, et al. Chronic intermittent elemental diet improves growth failure in children with Crohn's disease. Gastroenterology. 1988;94:603-10.
  • 5
    Sun YN, Feng XY, He L, Zeng LX, Hao ZM, Lv XH, et al. Prevalence and possible risk factors of low bone mineral density in untreated female patients with systemic lupus erythematosus. Biomed Res Int. 2015;2015:510514.
  • 6
    Peyrin-Biroulet L, Loftus EV, Colombel JF, Sandborn WJ. Long-term complications, extraintestinal manifestations, and mortality in adult Crohn's disease in population-based cohorts. Inflamm Bowel Dis. 2011;17:471-8.
  • 7
    Reilly MC, Gerlier L, Brabant Y, Brown M. Validity, reliability, and responsiveness of the work productivity and activity impairment questionnaire in Crohn's disease. Clin Ther. 2008;30:393-404.
  • 8
    Schmidt S, Mellstrom D, Norjavaara E, Sundh SV, Saalman R. Low bone mineral density in children and adolescents with inflammatory bowel disease: a population-based study from Western Sweden. Inflamm Bowel Dis. 2009;15:1844-50.
  • 9
    Pineau CA, Urowitz MB, Fortin PJ, Ibanez D, Gladman DD. Osteoporosis in systemic lupus erythematosus: factors associated with referral for bone mineral density studies, prevalence of osteoporosis and factors associated with reduced bone density. Lupus. 2004;13:436-41.
  • 10
    Miranda-Bautista J, Verdejo C, Diaz-Redondo A, Breton I, Bellon JM, Perez-Valderas MD, et al. Metabolic bone disease in patients diagnosed with inflammatory bowel disease from Spain. Therap Adv Gastroenterol. 2019;12, 1756284819862152.
  • 11
    Abrahamsen B, Hansen TB, Jensen LB, Hermann AP, Eiken P. Site of osteodensitometry in perimenopausal women: correlation and limits of agreement between anatomic regions. J Bone Miner Res. 1997;12:1471-9.
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    Guz-Mark A, Rinawi F, Egotubov O, Shimon I, Shamir R, Assa A. Pediatric-onset inflammatory bowel disease poses risk for low bone mineral density at early adulthood. Dig Liver Dis. 2017;49:639-42.
  • 13
    Herzog D, Bishop N, Glorieux F, Seidman EG. Interpretation of bone mineral density values in pediatric Crohn's disease. Inflamm Bowel Dis. 1998;4:261-7.
  • 14
    Ismail MH, Al-Elq AH, Al-Jarodi ME, Azzam NA, Aljebreen AM, Al-Momen SA, et al. Frequency of low bone mineral density in Saudi patients with inflammatory bowel disease. Saudi J Gastroenterol. 2012;18:201-7.
  • 15
    Neelis E, Rijnen N, Sluimer J, Olieman J, Rizopoulos D, Wijnen R, et al. Bone health of children with intestinal failure measured by dual energy X-ray absorptiometry and digital X-ray radiogrammetry. Clin Nutr. 2018;37:687-94.
  • 16
    Szafors P, Che H, Barnetche T, Morel J, Gaujoux-Viala C, Combe B, et al. Risk of fracture and low bone mineral density in adults with inflammatory bowel diseases. A systematic literature review with meta-analysis. Osteoporos Int. 2018;29:2389-97.
  • 17
    Tsai MS, Lin CL, Tu YK, Lee PH, Kao CH. Risks and predictors of osteoporosis in patients with inflammatory bowel diseases in an Asian population: a nationwide population-based cohort study. Int J Clin Pract. 2015;69:235-41.
  • 18
    Hidalgo DF, Boonpheng B, Phemister J, Hidalgo J, Young M. Inflammatory bowel disease and risk of osteoporotic fractures: a meta-analysis. Cureus. 2019;11:e5810.
  • 19
    Gupta A, Paski S, Issenman R, Webber C. Lumbar spine bone mineral density at diagnosis and during follow-up in children with IBD. J Clin Densitom. 2004;7:290-5.
  • 20
    Carroll MW, Kuenzig ME, Mack DR, Otley AR, Griffiths AM, Kaplan GG, et al. The impact of inflammatory bowel disease in Canada 2018: children and adolescents with IBD. J Can Assoc Gastroenterol. 2019;2:S49-67.
  • 21
    Turner D, Travis SP, Griffiths AM, Ruemmele FM, Levine A, Benchimol EI, et al. Consensus for managing acute severe ulcerative colitis in children: a systematic review and joint statement from ECCO, ESPGHAN, and the Porto IBD Working Group of ESPGHAN. Am J Gastroenterol. 2011;106:574-88.
  • 22
    Nobile S, Grand RJ, Pappa HM. Risk factors for low bone mineral density in pediatric inflammatory bowel disease: the positive role of physical activity. Eur J Gastroenterol Hepatol. 2018;30:471-6.
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Publication Dates

  • Publication in this collection
    19 Apr 2021
  • Date of issue
    Mar-Apr 2021

History

  • Received
    22 Feb 2020
  • Accepted
    24 Mar 2020
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