McCune-Albright Syndrome (MAS)

The MAS is a non-inherited, genetic disorder that was first described over fifty years ago (1). The triad which has classically defined the syndrome consists of precocious puberty, café au lait skin pigmentation and
polyostotic fibrous dysplasia (PFD) of bone (2). Subsequently, it was found that besides bone, skin and gonads, and a number of other tissues could be involved, predominantly endocrine tissues such as thyroid (3), adrenal (4), and various pituitary cell populations, including growth hormone-secreting somatotrophs (5-7). Besides these endocrine tissues, liver (8), heart (9), and spleen (10) have been found to be affected. Hyperfunctioning gonads resulting in precocious puberty (11), as well as other hyperfunctioning endocrine tissues together with PFD account for the majority of the associated morbidity and are the hallmarks of the presentation and disease course.

The disease presents along a spectrum both in terms of tissues involved, the severity of involvement and the age at presentation. Sometimes, children are diagnosed in early infancy with obvious bone disease and markedly increased endocrine secretions from several glands. At the opposite end of the spectrum, many children are entirely healthy, and have little or no outward evidence of bone or endocrine involvement. They may enter puberty close to the normal age, and have no unusual skin pigmentation at all.

Because of the sporadic occurrence of the disease and the pattern of skin hyperpigmentation, it was postulated that a genetic defect involving a dominant somatic mutation, occurring early in embryonic development, may be responsible for the phenotypic presentation. In 1991, activating mutations of the a subunit of the G protein (Gsa) which stimulates cAMP formation were described in affected tissues from patients with MAS (12-14). It is now generally accepted that a somatic mutation occurring early in development in the Gsa protein is responsible for MAS.

The endocrine tissues most frequently affected in MAS are the gonads (ovaries or testes), the thyroid and the growth hormone-secreting somatotrophs of the pituitary. Therapies for hyperfunctioning endocrine tissues include surgical removal of affected glands or medications directed at hormonal inhibition or blockade. The response is variable depending on the involved tissue (15-17).

While the skin hyperpigmentation can occasionally be extensive and psychologically trying for the patient, there are seldom any medical problems associated with it. Treatment of the PFD is, to date, largely ineffective and this remains the major therapeutic challenge of the disease.

Current procedures

To date, there is no satisfactory treatment for the crippling, disfiguring lesions of PFD/MAS. Treatment has included both medical and surgical approaches. Medical treatment has primarily focused on the use of pamidronate, a second generation bisphosphonate. Surgical treatment has focused on the use of bone grafts and orthopedic hardware.

Bisphosphonates are a class of drugs with a chemical structure based on pyrophosphates, the one naturally occurring inhibitor of bone resorption (22). A recent uncontrolled trial suggested that intravenous pamidronate could reduce bone pain in patients with severe, symptomatic PFD (23), but objective radiographic improvement was observed in only a minority of treated patients and it is unclear what the long term effects of inhibition of bone resorption by pamidronate will be in patients with PFD. An open label phase III study also reported beneficial effects of intravenous pamidronate (24). A recently published case report in which a single patient received pamidronate followed by alendronate, a third generation bisphosphonate, reported a "spectacular" increase in bone density and a resolution of debilitating bone pain (25).

Fracture of long bones frequently occur in children and adults with FD either in the monostotic form or the polyostotic form. The fracture may lead to a progressive deformity such as progressive coxa vara and a Shepherd’s Crook deformity of the proximal femur. Surgical treatment consist of orthopedic procedures aimed at stabilizing fragile affected bone that cause pain and/or impaired mobility, and/or resecting regions of disfigurement or those which impair neural function. They consist of curettage and/or resection of lesion with and without corrective osteotomy, bone grafting and hardware fixation devices. The existing methods of surgical treatments are found to be unsatisfactory. In most cases, there was a recurrence of the lesion, disappearance of the bone grafting material and separation of the metal fixation devices from the bone. It was clear that even following these procedures, the deformity progressed during the post-operative period. The surgical procedure did not affect the long term frequency of fractures although fracture healing was not impaired. There are no good fixation devices that would suit young patients with Shepherd’s crook deformity and there is no surgical procedure that will prevent local recurrence (26-29).



Background: alendronate

Alendronate is a member of the class of drugs known as aminobisphosphonates which are compounds that are structurally similar to inorganic pyrophosphate. While the exact mechanism of action is not entirely clear, it is generally believed that as an analogue of pyrophosphate, it is incorporated into bone. During the remodeling cycle it is released from bone and through unknown mechanisms inhibits osteoclasts and thereby blocks active bone resorption. However, there is also some evidence that bisphosphonates have some activity on the osteoblast. Clinically, the effect is to reduce parameters of both bone resorption and formation, such as the excretion of collagen breakdown products and serum osteocalcin. These effects are most clearly demonstrated in situations of increased bone turnover/remodeling such as in Paget’s disease or hypercalcemia of malignancy.

Bisphosphonates have been used in the treatment of Paget’s disease of bone and in the emergency treatment of hypercalcemia in a variety of diseases. Pamidronate is licensed for use in both indications. Alendronate is approved for the treatment and prevention of postmenopausal osteoporosis as well as for Paget’s disease. There is extensive published data on alendronate and other bisphosphonates summarized in recent reviews (30, 31).

A recent publication looking at the effect of long term treatment (24 - 36 months) with alendronate at the histomorphometric level was reassuring in that it demonstrated normal mineralization (32-34).

There are limited data about the use of bisphosphonates in children. Pamidronate has been used to treat children with cerebral palsy , osteogenesis imperfecta (35) as well as other diseases (36) (37-39). In addition, other bisphosphonates have been used to treat a number of other diseases in children (40-42). In general, these drugs have been safe and effective.

Treatment

Alendronate Dosing

The dosing of alendronate used will be 0.5 mg/kg/d for 6 months, followed by 6 months off drug. The dose will be given orally, once in the morning. This will be followed by another cycle of 6 months on and 6 months off drug. The on and off cycle is being used to minimize the possibility of growth plate abnormalities. This dose and scheduled was arrived at through extrapolation and extension of the recommended doses and schedules of pamidronate and alendronate used in Paget’s disease and pamidronate used in PFD. The following ratio was used:


pamidronate in Paget’s = alendronate in Paget’s
pamidronate in PFD alendronate in PFD

This is comparable to the adult dose of alendronate for Paget’s disease of 40 mg per day. The dose for postmenopausal osteoporosis is 10 mg per day.

Given the limitation of available pill sizes (40, 20, and 10 mg,), the dose stratification will be as follows:

weight (kg) >50 30-50 20-30
dose (mg) 40 20 10




Dose Modification

The dose of alendronate may be modified if there are significant gastrointestinal adverse experiences. If these are experienced, the drug will be discontinued for 2 weeks and restarted at _ the original dose. This dose will be maintained for the rest of the study provided that it is well tolerated. If this is not tolerated, the drug will be discontinued and the patient withdrawn from this study but offered enrollment in the screening/natural history protocol.


Risks, Benefits, Hazards and Discomforts

Alendronate


Alendronate is rapidly cleared from the circulation after administration. That fraction which is not renally excreted in an unmetabolized form is incorporated into bone. Blood levels following therapeutic doses are below the limits of detection. With time, that drug which has been incorporated in bone is later released during the normal remodeling cycle. The terminal half life, including that drug incorporated in bone is greater than 10 years.

Animal testing showed that rats receiving high doses developed parafollicular thyroid adenomas. In vivo and in vitro mutagenesis studies were negative with the exception of the following: a weakly positive response at concentrations > 5 mM in cytotoxicity in in vitro chromosomal aberrations in Chinese Hamster ovary cells. There was no effect on male or female fertility in rats given 4 times the equivalent human dose. Fetal abnormalities were observed in fetal rats but not rabbits when high doses were given to the pregnant mothers.

The risks of the use of alendronate in children are unknown. There is only one published report of the use of alendronate in children. It involved the treatment of 4 children with glucocorticoid-induced osteoporosis (43). The drug was safe and effective. Specific concerns about the safety of alendronate will have to be extrapolated from the studies of other bisphosphonates in children. This subject has recently been reviewed and while inconclusive, the findings are reassuring (40-42). There are approximately 25 published reports of the use of bisphosphonates in children. The greatest theoretical concern was that by inhibiting bone turnover and disrupting the remodeling process there would be bone deformity and disruption of the mineralization process. The evidence so far is that this does not occur.

A specific observation that has been made in the use of pamidronate was of a widening of the growth plate that resolved when treatment was discontinued (23). In children with fibrodysplasia ossificans progressiva treated with etidronate there was and increase in translucent area in bone (44). Transient symptomatic hypocalcemia occurred with intravenous pamidronate (45). Undertubulation at the growth plate has been reported with the use of pamidronate without any evidence of bone deformity after treatment is discontinued (46). A number of eye problems (anterior uveitis, episcleritis, and transitory conjunctivitis) have been reported with pamidronate, but only when used intravenously (47-50).

The major side effects reported with alendronate in studies involving adults were gastrointestinal, and most of those were mild and dose-related. Those adverse effects reported that were greater than placebo were: abdominal pain (6.6%), dyspepsia (3.6%), constipation (3.1%), and diarrhea (3.1%). While there has been much concern about alendronate causing severe esophagitis, when patients in studies (n=597) were compared to controls (n=397), there was no greater incidence of esophageal problems. Mild and transient decreases in calcium (18% of patients) and phosphate (10%) were observed. However, clinically significant decreases in calcium (<8 mg/dl) and phosphate (<2 mg/dl) were the same in treatment and placebo groups.

Alendronate can cause secondary hyperparathyroidism. The probable mechanism is through decreasing serum calcium and thereby stimulating PTH release. The risk of this occurring can be decreased through the addition of supplemental calcium and vitamin D in the diet. Patients will be monitored as well as prescribed a weight-appropriate dose of calcium supplementation and vitamin D in the form of a multivitamin.

Reports of the impact of alendronate on reproduction in humans are lacking. Studies in rats show drug use during gestation may have maternotoxic effects and cause neonatal death when administered during gestation. Pharmacokinetic studies demonstrate that approximately 2/3 of the drug is eliminated unmetabolized in the urine within 6 months of stopping treatment. A bone biopsy study showed that there is no effect on mineralization (33). It is classified by the FDA as Pregnancy Category C and its use during pregnancy is not recommended.

Bone Biopsy

The bone biopsy will be performed under local anesthesia in adults and adolescent patients, and light general anesthesia in young children by one of the investigators who is has been deemed qualified to do so. The biopsy is performed through a small skin incision which is closed with 2-3 stitches that will dissolve within 2-3 weeks. The site of the biopsy may cause discomfort and pain for several days and can be treated safely with acetaminophen. Bleeding and infection at the site of biopsy are possible but rare. A skin biopsy will be performed at the time of the bone biopsy. The skin biopsy adds no additional risk or discomfort to the procedure.

Other risks associated with the study

1. Needle stick may cause pain. This can be alleviated by preapplication of a local anesthetic creme or gel (EMLA).

2. The total absorbed radiation per site is detailed in appendix 7, NIH Form 88-23. The usual dose permitted for research purposes in adults is 3 rem to any tissue in a 13 week period and 5 rem in one year. The dose for children is 1/10 that dose. The total dose to be received in this study exceeds this amount. This is largely due to the amount of exposure form the Tc-99m MDP bone scan. However, the bone scan is a clinically indicated study that should be performed in the appropriate diagnosis and management of all patients with PFD.

3. Procedures done under general anesthesia carry the risk of cardiac arrest, brain damage or death. Pneumonia may occur following general anesthesia. Patients with conditions other than MAS/PFD will not be enrolled into the study in order to minimize this risk.

4. Tetracycline labeling (domeclocycline) may cause staining of teeth in young children. Children over the age of six years are unlikely to have staining since their secondary teeth are already formed within the gums. In the summertime, tetracycline can cause rashes due to sensitizing the skin to sunlight. This can be prevented by use of sunscreens or appropriate protective clothing.

5. Blood withdrawal poses a very small risk due to depletion of blood volume. By staying within the NIH weight-based guidelines the possibility of this occurring is very remote


Potential Benefits

Patients will undergo extensive evaluations while enrolled in this study. It is possible that as a result of these evaluations previously undetected conditions or problems may be detected. This knowledge may be of benefit to the patient.

When appropriate, NIH physicians will offer treatment for these newly detected conditions to the patient. When treatment by NIH physicians is not appropriate or possible, the information and results of testing will be conveyed to referring physicians.



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