X-linked hypophosphatemic rickets across the lifespan
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1 X-linked hypophosphatemic rickets across the lifespan AACE Midwest Regional Meeting Erik A. Imel, M.D. Associate Professor of Medicine and Pediatrics Indiana Center for Musculoskeletal Health July 28, 2018
2 Disclosures Research funding, consultation Kyowa Hakko Kirin Pharma, Inc. Ultragenyx Pharmaceuticals, Inc. Travel and meeting support Alexion Pharmaceuticals, Inc. Off-label use of medications Calcitriol Phosphate Cinacalcet
3 Goals Describe the clinical features and pathophysiology of hypophosphatemic rickets Discuss the clinical diagnosis of hypophosphatemic rickets Discuss medical management of X-linked hypophosphatemic rickets
4 PTH FGF23 Intracellular space Phosphate Reabsorption Serum Phosphate Urinary Phosphate 1,25OHD Dietary intake
5 Fibroblast growth factor 23 (FGF23) is a peptide hormone PTH FGF23 N FGF23 RXXR^ C Phosphate Reabsorption Pi FGF receptors/ Klotho Urinary Phosphate 1,25(OH)2D Intestinal phosphate absorption
6 Fibroblast growth factor 23 (FGF23) is a peptide hormone PTH FGF23 Phosphate Reabsorption Pi Urinary Phosphate 1,25(OH)2D Intestinal phosphate absorption
7 Urine phosphate excretion mg/min Tubular maximum reabsorption of phosphate TmP/GFR r Serum phosphorus mg/dl Walton and Bijvoet. Lancet 1975; ii: , TP/GFR = Serum Pi (Urine Pi x Serum Cr/Urine Cr) Brodehl et al. Pediatr Nephrol 1988;2:
8 Know age-related normal ranges Phosphorus Alkaline phosphatase 600 Males, MAYO Alkaline phosphatas, U/L Age, years The TmP/GFR age normal range is numerically similar to the age normal range for phosphorus
9 Chronic Hypophosphatemia Intake deficiency: normal or high TmP/GFR Dietary phosphate depletion Phosphate binders, malabsorption Premature neonates (need more phosphate than term neonates) Renal phosphate wasting: low TmP/GFR
10 Renal hypophosphatemia Non-FGF23 mediated Hyperparathyroidism Fanconi syndrome: Genetic causes Drugs Toxins Hereditary hypophosphatemic rickets with hypercalciuria NPT2c Diuretics FGF23 mediated XLH-PHEX-most common ADHR-FGF23 ARHR DMP1 ENPP1 FAM20C Fibrous dysplasia/ McCune- Albright Tumor induced osteomalacia
11 4 year old girl
12 Laboratory tests Values Normal SI Normal Phosphorus 2.1 mg/dl ( ) 0.68 mmol/l ( ) Calcium 9.4 mg/dl ( ) 2.35 mmol/l ( ) Creatinine 0.2 mg/dl (<0.7 ) Alkaline phosphatase 653 U/L ( ) 25-OHD 30 ng/ml (25-50) 74.9 nmol/l ( ) 1,25(OH) 2 D 41 pg/ml (15-75) pmol/l (39-195)
13 Laboratory tests Values Normal SI Normal Phosphorus 2.1 mg/dl ( ) 0.68 mmol/l ( ) Calcium 9.4 mg/dl ( ) 2.35 mmol/l ( ) Creatinine 0.2 mg/dl (<0.7 ) 17.7 mmol/l (<61.9) Urine glucose: 0 Alkaline phosphatase 653 U/L ( ) 10.9 μkat/l ( ) Urine amino acids not elevated 25-OHD 30 ng/ml (25-50) 74.9 nmol/l ( ) 1,25(OH) 2 D 41 pg/ml (15-75) pmol/l (39-195) TmP/GFR 1.8 mg/dl ( ) 0.7 mmol/l ( ) Urine Calcium/Creatinine 0.05 mg/mg (<0.42) 0.14 mmol/mmol (<1.18) PTH 37 pg/ml (10-65) 3.9 pmol/l ( ) FGF23 (intact) 173 pg/ml (<70) No generalized tubulopathy
14 XLH Most common genetic hypophosphatemia 1:20,000 Inactivating mutations in PHEX X-linked dominant Frequently sporadic Disease state Hyp Consortium Nat Genet 1995;11:130-6 Econs et al. Skeletal Radiology 1991;20:109-14
15 PHEX deficiency increases FGF23 Increases bone (osteocyte) FGF23 expression Elevates plasma intact FGF23 Intact FGF23 pg/ml Liu et al JBC 2003 & Imel et al JCEM N RXXR XLH Normal * P<0.05 C
16 At the renal tubular epithelium Excessive intact FGF23 mediates Renal tubular phosphate reabsorption Serum Pi Activation of 1,25(OH) 2 D Renal Tubular Cell Imel et al. ICE/ENDO 2014, Chicago, Illinois, Oral session OR
17 FGF23 induced hypophosphatemia impairs mineralization of bone Osteomalacia/excess unmineralized osteoid Rickets Bowing deformities Bone pain Insufficiency fractures or pseudofractures Aono et al. JBMR 2009:24;1879
18 X-linked Hypophosphatemia Features Osteomalacia Rickets Leg deformities Short stature ±Bone pain Insufficiency fractures Poor fracture healing Dental abscesses Enthesopathy/osteophytes Osteoarthritis Several features are related to the hypophosphatemia. Others are not direct effects of low phosphate. Carpenter, Imel et al JBMR 2011; ;26(7): , Peterson et al JBMR 1992;7(6):583, Reid et al Medicine 1989;68(6);336
19 XLH is not merely a pediatric disease! Adults with XLH Imel files
20 The pediatric consequences of short stature and leg deformities persist in adulthood Children Adults Sitting height Arm length Stature Leg length Zivicnjak et al Ped Nephr 2011 Beck-Nielsen et al Calcified Tissue Int 2010;87(2):108
21 Joint pains (knees, ankles) 82% Joint complications Enthesopathy was present in 30-84% or more Up to 100% with increasing with age More males affected with enthesopathy Osteoarthritis, especially in lower extremities: 61% of pts 40 yrs Linglart et al. Endocrine Connections 2014.doi: /EC ; Beck-Nielsen et al Calcified Tissue Int 2010;87(2):108; Liang et al Calcif Tissue Int 2009;85(3):235, Polisson et al NEJM 1985, Hardy et al Radiology 1989, Reid et al Medicine 1989;68(6)336; Connor et al. JCEM 2015:100(10);3625
22 Insufficiency fractures Up to half of adults have pseudofractures Sometimes asymptomatic or minimally symptomatic May fracture through Reid et al Medicine 1989;68(6);336 Imel files
23 Dental issues are common Tooth Abscess occur in up to 86%. Reid et al Medicine 1989;68(6)336 Impaired dentin mineralization Periodontal disease common In 34 adults with XLH, >75% with periodontitis on exam >25 % with severe periodontitis Less common and less severe in those on treatment as adults Biosse Duplan et al. J. Dent Res 2017;96(4):388; Boukpessi et al. Bone 2017; 95:151 XLH Control Linglart et al. Endocrine Connections 2014.doi: /EC
24 Muscle weakness Assessments influenced by leg deformities and decreased activity But, patients with XLH have Lower muscle density Lower peak muscle force and power Impaired walking and mobility JCEM 2012;97(8)E1492; JCEM 2013;98(5):E990; Ruppe et al. ASBMR 2016; and others
25 Craniosynostosis and Chiari 1 malformations Cranial bone abnormalities common Frontal bossing Dolicocephaly Flattened cranial base Decreased depth of posterior fossa Chiari Type 1 malformation- up to 44% Craniosynostosis, especially of sagittal suture May require surgery Vega et al. J Nurosurg Pediatr 2016;17(6);694 Caldemeyer et al Radiology 1995;195(3):733 Gjorup et al Am J Med Genet 2011;155a(11):2654
26 Treatment
27 Goals of conventional therapy for XLH Children ü Improve osteomalacia/rickets ü Straighten legs ü Improve growth ü Improve alkaline phosphatase ü Avoid complications The goal is not specifically to normalize the serum phosphorus. Adults ü Improve osteomalacia ü Improve bone pain ü Improve alkaline phosphatase ü Decrease or heal pseudofractures ü Improve healing after orthopedic surgery ü Decrease tooth abcesses? ü Avoid complications Carpenter, Imel et al JBMR 2011, Glorieux et al NEJM 1980, Harrell et al JCI 1985, many other citations
28 Conventional medical treatment for XLH Phosphate salts: mg/kg/day Never treat XLH with phosphate alone! Calcitriol [1,25(OH) 2 D]: ng/kg/day Requires multiple daily doses Start about 1/3 or 1/2 dose and titrate to target dose over several weeks based in part on tolerability Relatively frequent laboratory monitoring for safety Pi, Ca, PTH, ALP, Urine Calcium/creatinine Carpenter, Imel, Holm et al JBMR 2011, Glorieux et al NEJM 1980, Harrell et al JCI 1985, many other citations
29 Efficacy monitoring- Calcitriol/Pi Children Alkaline phosphatase Radiographic improvement Rickets Bowing deformities Height Bone pain Dental abscesses Adults Alkaline phosphatase Bone pain Fracture or pseudofracture healing Mobility Quality of Life measures Dental abscesses
30 Safety monitoring during Calcitriol/Pi Serum Phosphorus in normal or high range: Decrease phosphate and/or calcitriol Serum Calcium or Urine Calcium elevated: Decrease calcitriol PTH rising: Decrease the phosphate and/or increase calcitriol Creatinine elevated: Decrease or stop phosphate and calcitriol Renal ultrasound screen for nephrocalcinosis Decrease doses Carpenter, Imel, Holm et al JBMR 2011
31 What is the effect of calcitriol and phosphate treatment on FGF23? A. Increase? B. No change? C. Decrease? Percent of baseline Intact FGF23 500% 400% 300% 200% 100% 0% Treated Untreated Imel et al JCEM 2010
32 Limitations of current treatment of XLH Started treatment age 4 years Started treatment age 24 months At 8 yr old Height 10 th %ile At 8 yr old Height -3SD
33 Limitations of current treatment of XLH Sitting height Sitting Height Arm length Stature Leg length Zivicnjak et al Ped Nephr 2011
34 Benefit of early treatment: Starting before vs after 1 year old Gray: Group 1, n=8 (3F) Start treatment at median age of 0.35 yr (range yr). White: Group 2, n=11(9f) Start treatment at median age of 2.1 yr (range yr) Makitie et al JCEM 2003; 88(8):3591
35 There is no clear consensus on when to treat adults with calcitriol and phosphate Most patients stop treatment at adulthood Some untreated adults have few or no symptoms Many others have mild to severe symptoms and restart treatment for: Bone pain Osteomalacia Insufficiency fractures Planned orthopedic surgeries
36 What are the risks of Calcitriol/Pi?
37 Risks of calcitriol and phosphate Gastrointestinal side effects Dyspepsia, laxative effect of phosphate Hyperparathyroidism* Hypercalciuria, hypercalcemia Nephrocalcinosis-in up to 50 to 80% Chronic kidney disease* Grade 3 Other ectopic calcification reported *Exact incidence uncertain Peterson et al. JBMR 1992, Reid et al. Medicine 1989, Rivkees et al. JCEM 1992, Goodyer et al. J Pediatr 1987, Reusz et al. Arch Dis Child 1990, Verge et al. NEJM 1991, Taylor et al. Pediatr Nephrol 1995
38 Hyperparathyroidism Nearly half of XLH children have elevated PTH BEFORE starting treatment. Carpenter et al JCEM 1994;78(6):1378 Hyperparathyroidism also complicates treatment with phosphate. Many cases in the literature, but exact incidence not certain Longer treatment and higher phosphate dose may increase risk of tertiary (hypercalcemic) hyperparathyroidism. Makitie et al Clin Endocrinol 2003;58(2):163, Rivkees et al JCEM 1992;75(6):1514, several other series.
39 Tertiary hyperparathyroidism Multi-gland hyperplasia + autonomy Hypercalcemia Nephrolithiasis Hypertension Parathyroidectomy Removing only one gland often does not cure Three and a half gland resection Risk of recurrence Risk of post-surgical HYPOparathyroidism Which further complicates management Calcimimetic case reports Yavropoulou et al Hormones 2010
40 Common mistakes: Trying to normalize phosphorus Too much phosphate Too little calcitriol PTH I don t understand.i keep increasing the phosphate dose, but the PTH won t come down. What PTH concentration should we target? Ideally normal
41 Chronic kidney disease Nephrocalcinosis can lead to chronic kidney disease BUT, the exact incidence of CKD in XLH is not certain. End stage renal disease - rare Kidney transplantation rare Hypertension
42 Calcitriol and phosphate do not help some features Joint dysfunction/stiffness Osteoarthritis Osteophytes Enthesopathy Connor et al. JCEM 2015:100(10);3625; Karaplis et al 2012 Endocrinology 153(12): 5906
43 Conventional therapy may decrease tooth abscesses Those who were under treatment longer as adults had less severe dental disease Connor et al. JCEM 2015:100(10);3625; Biosse Duplan et al. J. Dent Res 2017;96(4):388; Boukpessi et al. Bone 2017; 95:151
44 Surgeries in XLH patients Childhood Leg straightening procedures Craniosynostosis Dental procedures Adulthood Rodding for insufficiency fractures Joint replacements (osteoarthritis) Laminectomies (spinal stenosis) Root canal Dental extractions Parathyroidectomy
45 New treatment option
46 Y Y Burosumab (KRN23) A recombinant human IgG1 monoclonal antibody that binds to FGF23 and inhibits FGF23 biologic activity Renal Tubular Cell Y KRN23 FGF23 Imel et al. ICE/ENDO 2014, Chicago, Illinois, Oral session OR
47 FGF23 neutralizing antibody treatment of Hyp (XLH) mouse Increases serum phosphorus Increases 1,25(OH) 2 D Improves osteomalacia, and bone growth control control FGF23Ab(4mg/kg) FGF23Ab(16/mg/kg) Aono et al. JBMR 2009:24;1879
48 Burosumab (KRN23) Phase I/II trial in Adults with XLH, dosed every 4 weeks. N =28 N =22 Burosumab increases: Serum Pi TmP/GFR 1,25(OH) 2 D Imel et al. JCEM, 2015;100:
49 Burosumab Phase 2 study children age 5-12 with XLH 52 children randomized to Q2W or Q4W burosumab for 64 weeks Doses started low and titrated based on serum phosphorus Primary outcome: change from baseline in Rickets Severity Score Carpenter TO et al. N Engl J Med 2018;378:
50 Burosumab in children age 5-12 with XLH Burosumab improved Serum phosphorus TmP/GFR 1,25(OH)2D Rickets (measured by two different scales) Height Z-score modestly Walking distance in those with impairment at baseline PRO functional outcomes Carpenter TO et al. N Engl J Med 2018;378:
51 Phase 3 RCT: Burosumab vs placebo in adults with XLH RCT 24 weeks of burosumab 1 mg/kg vs placebo, dose could be decreased for Pi above target 134 adults with XLH Centers in North America, Europe, Japan, South Korea Primary outcome: % achieving mean serum Pi above the lower limit of normal at midpoint of dose cycle Secondary outcomes: Pharmacodynamic parameters, safety, healing of fractures/pseudofractures Insogna et al JBMR 2018
52 Burosumab vs placebo in adults with XLH Baseline Characteristics n Total 134 Mean age, years 40 ± 12.2 Female 64.9% Race, White 80.6% Confirmed PHEX mutation or VUS 95% Enthesopathy on radiographs 99.3% Active Fractures/Pseudofractures Nephrocalcinosis 54.5% Pain medications 67.9% (opioids 22.4%) Insogna et al JBMR % in burosumab, 57.6% in placebo
53 Burosumab vs placebo in adults with XLH Mid-cycle Pi TMP/GFR Trough Pi 1,25(OH)2D 5 had dose reductions due to Pi >4.5 mg/dl Maintained on lower dose. Insogna et al JBMR 2018
54 Burosumab vs placebo in adults with XLH Baseline fracture/pseudofracture Burosumab 32 (47.1%) had 65 fractures Placebo 38 (57.6%) had 91 fractures At week 24, greater healing in burosumab group The odds ratio of full healing at week for burosumab, p<0.001 Insogna et al JBMR 2018
55 Children Burosumab 64W AEs Adults Burosumab 24W Adults Placebo 24W Total subjects Injection site 57% 11.8% 12.1% reactions Restless leg syndrome % 7.6%
56 Nephrocalcinosis and Echo Children Burosumab 64W Adults Burosumab 24W Adults Placebo 24W Total subjects in study Increase nephrocalcinosis score 1 point 6 (11%) 11 (16.2%) 12 (18.2%) Decrease nephrocalcinosis score 1 point 2 (3.8%) 4 (5.9%) 4 (6.1%) Increase Echo Calcium score 1 point 1 (1.5%) 7 (10.6%) Decrease Echo calcium score 1 point 3 (4.4%) 1 (1.5%) No changes >1 point
57 FDA approved burosumab April 2018! The only FDA approved drug for XLH Starting dose Children 0.8 mg/kg SC every 2 weeks Adults 1 mg/kg SC every 4 weeks Can decrease dose if Pi above target range Ongoing studies: Phase 3 RCT in children active comparator Burosumab every 2 weeks vs conventional therapy Long-term 10 year disease monitoring study
58 Important clinical issues When to use burosumab vs conventional therapy? Transition pediatric dosing to adult dosing? What is the long term effect on: Attained adult height Leg deformity in growing children Surgical needs or outcomes Nephrocalcinosis risk Enthesopathy
59 Summary XLH is not just a childhood disease XLH has lifelong consequences in adults Impairing mobility and quality of life Conventional medical therapy for XLH (calcitriol and phosphate) Addresses (replaces) the consequences of FGF23 excess Has risks of significant side effects requiring careful monitoring Burosumab blocks effects of excess FGF23 Improves Pi and rickets Improves healing of pseudofractures/fractures Improves functional outcomes
60 Post-Test Questions Which is an effect of FGF23 in mineral metabolism? A. Increase renal phosphorus reabsorption B. Increase intestinal phosphorus reabsorption C. Decrease activation of 1,25(OH) 2 D D. Increase serum calcium E. Decrease catabolism of 1,25(OH) 2 D
61 Post-Test Questions Which characteristics of XLH are only seen in children? A. Short stature B. Rachitic changes at the growth plate C. Enthesopaty D. Dental abscesses E. Bone pain F. Pseudofractures G. Leg deformities
62 Post-Test Questions You are seeing this child with rickets, hypophosphatemia, high Tmp/GFR. Parents and siblings are unaffected. What is the likely etiology of low Pi? A. XLH B. ADHR C. ARHR D. Dietary phosphate depletion E. Tumor induced osteomalacia Hypophosphatemia
63 Post-Test Questions You are seeing this child with rickets, hypophosphatemia, low Tmp/GFR. The father also has hypophosphatemia. What is the most likely etiology of low Pi? A. XLH B. ADHR C. ARHR D. Dietary phosphate depletion E. Tumor induced osteomalacia Hypophosphatemia
64 Post-Test Questions Which is an appropriate treatment for XLH? A. Phosphate salts alone B. Cholecalciferol alone C. Calcium with cholecalciferol D. Calcitriol with phosphate salts E. Calcitriol with calcium F. Burosumab with calcitriol
65 Post-Test Questions In clinical trials, burosumab had which of the following effects in patients with XLH? A. Improve enthesopathy B. Improve healing of pseudofractures C. No effect on serum phosphorus D. Decrease 1,25(OH) 2 D E. Improve nephrocalcinosis F. Worsen rickets
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