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 X-linked hypophosphatemic rickets Discuss the clinical diagnosis of X-linked 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) 2 D Intestinal phosphate absorption
6 Fibroblast growth factor 23 (FGF23) is a peptide hormone PTH FGF23 Phosphate Reabsorption Pi Urinary Phosphate 1,25(OH) 2 D Intestinal phosphate absorption
7 Urine phosphate excretion mg/min Tubular maximum reabsorption of phosphate TmP/GFR Serum phosphorus mg/dl Phosphate Walton and Bijvoet. Lancet 1975; ii: , Tm GF Low indi renal
8 Chronic Hypophosphatemia TmP/GFR high or normal: Intake deficiency Dietary phosphate depletion Premature neonates need more phosphate than term neonates Phosphate binders, malabsorption TmP/GFR low: Renal phosphate wasting
9 Renal hypophosphatemia Not 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 syndrome Tumor induced osteomalacia
10 Alkaline phosphatas, U/L Know age-related normal ranges Phosphorus Alkaline phosphatase 600 Males, MAYO Age, years The TmP/GFR age normal range is numerically similar to the age normal range for phosphorus
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 ) 17.7 mmol/l (<61.9) No generalized tubulopathy Alkaline phosphatase 653 U/L ( ) 10.9 μkat/l ( ) 25-OHD 30 ng/ml (25-50) 74.9 nmol/l Urine glucose: ( ) 0 1,25(OH) 2 D 41 pg/ml (15-75) Urine pmol/l amino acids (39-195) TmP/GFR 1.8 mg/dl ( ) 0.7 mmol/l not elevated ( ) 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)
13 XLH Most common genetic hypophosphatemia 1: 20,000-25,000 Inactivating mutations in PHEX X-linked dominant Frequently sporadic Disease state However consider other inheritance patterns Hyp Consortium Nat Genet 1995;11:130-6 Econs et al. Skeletal Radiology 1991;20:109-14
14 Intact FGF23 pg/ml PHEX deficiency increases FGF23 Increases bone (osteocyte) FGF23 expression Elevates plasma intact FGF XLH Normal * P<0.05 Liu et al JBC 2003 & Imel et al JCEM N RXXR C
15 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
16 Hypophosphatemia impairs mineralization of bone Osteomalacia - Excess unmineralized osteoid Rickets Bowing Pseudofractures Aono et al. JBMR 2009:24;1879
17 X-linked Hypophosphatemia Features Osteomalacia Rickets Leg deformities, skull shape abnormalities Short stature ± Bone pain Insufficiency fractures Poor fracture healing Dental abscesses Muscle weakness 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
18 XLH is not merely a pediatric disease! Adults with XLH have debilitating features
19 Joint complications Joint pains (knees, ankles) 82% 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
20 Fractures, pseudofractures In cross-sectional studies fractures are not higher than controls However, up to half of adults have pseudofractures Contribute to bone pain May fracture through Reid et al Medicine 1989;68(6);336 Imel files
21 XLH- Muscle weakness Assessments influenced by leg deformities and decreased activity 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
22 Dental issues are common Page 41 of 41 Tooth Abscess occur in up to 86%. Reid et al Medicine 1989;68(6)336 Periodontal disease common In 34 adults with XLH, >75% with periodontitis on exam Impaired dentin mineralization >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
23 Treatment
24 Goals of therapy for XLH Children Carpenter, Imel et al JBMR 2011, Glorieux et al NEJM 1980, Harrell et al JCI 1985, many other citations Adults Improve osteomalacia / rickets Improve alkaline phosphatase Straighten legs Improve growth Decrease or heal pseudofractures Improve bone pain Improve healing after orthopedic surgery Improve mobility Decrease tooth abscesses Avoid complications
25 Conventional medical treatment for XLH Phosphate salts: mg/kg/day Never treat XLH with phosphate alone! Calcitriol [1,25(OH) 2 D]: Requires multiple daily doses ng/kg/day Intake 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 Loss Target Phosphate level Carpenter, Imel, Holm et al JBMR 2011, Glorieux et al NEJM 1980, Harrell et al JCI 1985, many other citations
26 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
27 Started treatment age 4 years At 8 yr old Height 10 th %ile Limitations of calcitriol and phosphate Started treatment age 24 months At 8 yr old Height -3SD
28 Limitations of calcitriol and phosphate Sitting height Sitting Height Arm length Stature Leg length Zivicnjak et al Ped Nephr 2011
29 There has not been clear consensus on when to treat adults with calcitriol and phosphate Most patients have stopped treatment at end of adolescence 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
30 Other features Calcitriol and phosphate do not help Joint dysfunction/stiffness Osteoarthritis Osteophytes Enthesopathy Calcitriol and phosphate may decrease tooth abscesses 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; ; Karaplis et al 2012 Endocrinology 153(12): 5906
31 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* 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
32 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
33
34 Burosumab (KRN23) A recombinant human IgG1 monoclonal antibody that binds to FGF23 and inhibits FGF23 biologic activity Renal Tubular Cell KRN23 FGF23 Imel et al. ICE/ENDO 2014, Chicago, Illinois, Oral session OR
35 FGF23 neutralizing antibody treatment of Hyp (XLH) mouse Increased serum phosphorus, 1,25(OH) 2 D Improved osteomalacia, bone growth, muscle weakness control control FGF23Ab(4mg/kg) FGF23Ab(16/mg/kg) Aono et al. JBMR 2009:24;1879
36 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:
37 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 in Rickets Severity Score Carpenter TO et al. N Engl J Med 2018;378:
38 Burosumab in children age 5-12 with XLH Serum Pi TMP/GFR Carpenter TO et al. N Engl J Med 2018;378:
39 Burosumab in children age 5-12 with XLH 1,25(OH) 2 D Total ALP Carpenter TO et al. N Engl J Med 2018;378:
40 Burosumab improved rickets RSS Total 0-10: Wrist (0-4) plus Knee (0-6) Thacher et al J Trop Pediatr 2000; 46(3): RGI-C (-3, -2, -1, 0, +1, +2, +3) Changes in wrist, knee, leg Whyte et al. JBMR 2018; 33(5): Carpenter TO et al. N Engl J Med 2018;378:
41 Burosumab in XLH ages 5-12 Improved height Z-score Improved walking distance Physical functioning scores Carpenter TO et al. N Engl J Med 2018;378:
42 Phase 3 RCT: Burosumab vs placebo in adults with XLH 134 adults with XLH Centers in North America, Europe, Japan, South Korea 24 weeks of burosumab 1 mg/kg vs placebo Primary outcome: % achieving normal mean serum Pi at midpoint of dose cycle Secondary outcomes: Pharmacodynamic parameters, safety, healing of fractures/pseudofractures Insogna et al JBMR 2018
43 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 47.1% in burosumab, 57.6% in placebo Nephrocalcinosis 54.5% Pain medications 67.9% (opioids 22.4%) Insogna et al JBMR 2018
44 Burosumab vs placebo in adults with XLH Mid-cycle Pi Trough Pi 5 had dose reductions due to Pi >4.5 mg/dl Maintained on lower dose. TMP/GFR 1,25(OH) 2 D Insogna et al JBMR 2018
45 Burosumab vs placebo in adults with XLH Serum Calcium 24 hour Urine Calcium PTH Insogna et al JBMR 2018
46 Burosumab improved stiffness in adults with XLH PRO Stiffness Insogna et al JBMR 2018
47 Burosumab improved pseudofracture healing 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
48 Adverse Events Children Burosumab 64W Adults Burosumab 24W Adults Placebo 24W Total subjects Injection site reactions Restless leg syndrome 57% 11.8% 12.1% % 7.6% Insogna et al JBMR 2018
49 Nephrocalcinosis 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%) No changes >1 point Insogna et al JBMR 2018
50 FDA approved burosumab April 2018! Monotherapy: Do NOT combine with calcitriol or phosphate Starting dose Children (age 1 year and older) 0.8 mg/kg SC every 2 weeks Adults 1 mg/kg SC every 4 weeks Ongoing studies: Phase 3 RCT in children active comparator Burosumab every 2 weeks vs conventional therapy Long-term disease monitoring study
51 Monitoring during burosumab Serum phosphorus 2 wks or 4 wks after injections Especially after dose changes, and until stabilizes. Target low normal range at trough Make sure peak or trough not too high Alkaline phosphatase Radiographs for healing of rickets, pseudofractures Growth Serum calcium Urine calcium excretion Creatinine PTH Renal ultrasound
52 Remaining clinical questions?? What are the long term effects of burosumab on: Attained adult height Leg deformity in growing children Surgical needs or outcomes Nephrocalcinosis risk Enthesopathy Tooth abscesses
53 Summary XLH is not just a childhood disease XLH has lifelong consequences in adults Impairing mobility and quality of life Complications of XLH and of its therapy Therapeutic options now include Conventional therapy (calcitriol and phosphate) FDA approved burosumab Always discuss and balance risks and benefits in therapy and monitor carefully.
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56 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
57 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
58 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
59 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
60 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
61 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
62
63 Cinacalcet in XLH Cinacalcet decreases FGF23 in CKD. (Koizumi et al Nephr Dial Transplant 2011) In a hyperparathyroid XLH case reports cinacalcet decreased FGF23. (Yavropoulou et al Hormones 2010) In children with XLH, cinacalcet decreased FGF23, but not to normal. (Alon et al 2013, ASBMR abstract SA0128) One child treated with cinacalcet and calcitriol improved phosphorus and rickets. (Alon et al Clinical Endocrinology 87(1): )
64 Pediatric Phase 2 Study Design (UX023- CL201) Study Design Key Endpoints Study Population Children with XLH Ages 5-12 yrs N = 52 Tanner 2 Weeks Titration Period 16 Weeks Titration Period 16 Weeks Primary analysis: Week 40 (N=52) Biweekly (Q2W) Dose Group Extended analysis: Week 64 (N=36) Treatment Period 48 Weeks Monthly (Q4W) Dose Group Treatment Period 48 Weeks Pre-specified subgroups based on baseline total rickets severity score (RSS) Extension Study Week 40: 34 patients with RSS 1.5; 18 patients with RSS < 1.5 Week 64: 18 patients with RSS 1.5; 18 patients with RSS < 1.5 Pharmacodynamics: serum P, TRP, TmP/GFR, 1,25(OH) 2 D Rickets: graded by two scoring systems (RGI-C and RSS) Growth velocity Walking ability: 6 minute walk test Patient-reported Outcome: POSNA- PODCI Safety
65 Burosumab improved rickets RSS Total 0-10: Wrist (0-4) plus Knee (0-6) Thacher et al J Trop Pediatr 2000; 46(3): RGI-C (-3, -2, -1, 0, +1, +2, +3) Changes in wrist, knee, leg Whyte et al. JBMR 2018; 33(5): Carpenter TO et al. N Engl J Med 2018;378:
66 6m old male, pretreatment 15m old male, After 9 months calcitriol and phosphate
67 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.
68 PTH Common mistakes: Trying to normalize phosphorus Too much phosphate Too little calcitriol 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
69 Calcitriol and phosphate 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
70 Burosumab vs placebo in adults with XLH PRO Pain PRO Physical Function PRO Stiffness Insogna et al JBMR 2018
71 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
72 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
73 Children Improve osteomalacia/rickets Straighten legs Improve growth Improve alkaline phosphatase Decrease tooth abcesses? Avoid complications Goals of therapy for XLH Adults Improve osteomalacia Improve bone pain Improve alkaline phosphatase Decrease or heal pseudofractures Improve healing after orthopedic surgery Decrease tooth abcesses? Avoid complications Carpenter, Imel et al JBMR 2011, Glorieux et al NEJM 1980, Harrell et al JCI 1985, many other citations
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