Abstract
Transient osteoporosis of the hip (TOH) is a temporary clinical condition of unknown etiology which usually resolves with conservative therapy though may be complicated by fracture or progression to avascular necrosis (AVN). TOH may be slightly more prevalent in men but when it occurs in women, it is most often seen in the latter part of pregnancy. Though fracture is a rare complication of TOH when it occurs, it is most often associated with TOH occurring in pregnancy. Magnetic resonance imaging (MRI) is the best method to diagnosis TOH. Low signal intensity on T1-weighted images, high signal intensity on T2-weighted images, and homogenous pattern of edema (the femoral head and/or neck) with normal subchondral area are in favor of TOH. A shortened course to recovery is reported by use of bisphosphonates, calcitonin, or teriparatide. Based on reported cases, core decompression is not superior to medical therapy. Transient osteoporosis of the hip, which often has no known etiology, usually resolves with conservative therapy but may predispose the patient to fracture or avascular necrosis. Diagnostic method of choice is magnetic resonance imaging. Bisphosphonates, calcitonin, or teriparatide are reported as a useful approach to reduce duration of recovery.
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Introduction
Transient osteoporosis of the hip (TOH) is usually a benign and self-limiting disorder with no obvious etiology [1–3]. It may also be referred to as the primary bone marrow edema syndrome (BMES), a term used to define bone marrow edema (BME) without an obvious cause. TOH is most common in middle-aged men. In women, it is most often seen in the last trimester of pregnancy. TOH may predispose these populations to fragility fractures [2–5]. An insult (such as trauma, infection, inflammation, degenerative process, ischemic injury, neoplasia, surgery, drugs, metabolic, and neurologic disorders) presumably initiates the process, leading to an increase in bone turnover, venous hypertension, and/or microfracture causing edema [5–7]. The differences between primary and secondary TOH in terms of natural course and radiological findings are often unclear; however, it is important to exclude secondary causes of TOH radiologically and clinically.
In 1959, Curtiss and Kincaid reported three cases of TOH who presented with unilateral or bilateral hip pain or thigh pain in the third trimester of pregnancy. Radiology showed spotty demineralization of the femoral head, a small part of the femoral neck, and the acetabulum which recovered spontaneously several months after delivery [8]. In 1988, Wilson et al. used the term “Transient Marrow Edema Syndrome” regarding patients with knee and hip pain who had normal bone or osteopenia on DXA, regional decrease in intensity of signal of the bone marrow on T1-weighted images, and increased signal intensity on T2-weighted images on MRI [9]. In 1993, Solomon introduced the importance of differentiation between BME with and without osteonecrosis: BME with osteonecrosis may cause bone collapse requiring reconstructive surgery, whereas BME without osteonecrosis is a transient and self-limited condition [10].
Information concerning TOH is scattered and in mostly small case series. We performed a literature review using “Bone Marrow Edema” and “Transient Osteoporosis of the Hip” to find articles cited on Pub Med between 1959 and May 2014 (Table 1). Two hundred seventy-four articles were identified, and 97 were selected for review after excluding articles lacking data about age, duration of recovery, tool of diagnosis, modality of treatment or complications, or lacking ability to obtain full text manuscript. Examining the abstract, we selected the articles reporting either cases of transient osteoporosis or bone marrow edema syndrome of the hip with or without other joint involvement. Epidemiology of TOH (age, sex, and reported risk factors), duration of recovery, modality of treatment and complications were assessed and compared. Most cases were diagnosed by MRI, especially articles published after 1990. However, some studies reported cases diagnosed by X-ray, DXA, or bone scans were considered to be TOH on the basis of clinical time course and recovery with pain resolution with or without motion. We found 437 reported cases of TOH (Table 1). Additional weight bearing joints that may be involved include the knee (47 cases), ankle (25 cases), foot (22 cases), spine (2 cases), and shoulder (1 case).
Epidemiology and pathophysiology
TOH is postulated to have three stages. The first stage with acute onset hip pain is due to edema potentially induced by trauma, neurovascular dysfunction, transient hyperemia, or microfracture. The second stage involves increased resorption and demineralization of the bone. The final stage consists of resolution of the process clinically and by radiograph [15, 16].
TOH should be considered in the differential diagnosis of sudden onset hip pain which typically gradually resolves within 6 months (2–12 months) with conservative strategies including minimizing weight-bearing activities, rest, using crutches, wheelchairs, hot packs, ultrasound therapy, and interferential current therapies or analgesics [7, 17, 18]. Pain can be possibly produced by increased intraosseous pressure, venous hypertension, increased focal bone turnover, microfracture, or periosteal irritation (5). Though unlikely, bone marrow edema may progress, causing vascular compression, resulting in ischemic injury to the femoral head and avascular necrosis (AVN) [19].
The distinction between TOH and early-phase AVN is difficult to judge both radiologically and clinically, and may result in needless surgical intervention in patients with only TOH. Furthermore, these two conditions are different in prognosis and treatment. Pain of TOH usually starts spontaneously. Presentation may be varied from insidious vague pain with limping to more severe progressive pain leading to immobility and hospitalization.
Pregnancy is the most common reported risk factor for TOH, though the overall incidence of TOH is higher in men than that of women (Table 1). Occasionally a precipitating event or etiology, such as trauma, alcohol consumption, smoking, corticosteroid, vascular insults, inflammation, drug use, or osteogenesis imperfecta, may be associated (Table 1) [5, 11–14]. The mean age of onset is 40 years of age with cases reported between ages 20 and 80 (Table 1).
Although dual energy X-ray absorptiometry (DXA) shows osteoporosis in some cases, it is not clear if osteoporosis is a risk factor for the development of microfracture and bone marrow edema. On the other hand, microfracture might itself cause the edema and separation of the bone trabeculae, reported as osteoporosis on DXA. Focal bone turnover markers are elevated in aspirates from bone, without any significant detectable change in mean serum concentration of bone turnover markers [5, 20].
Etiology
The etiology of TOH remains uncertain. It is also unclear whether TOH is an isolated entity from or represents the early stage of AVN. The aforementioned insults (trauma, infection, inflammation, degenerative process, ischemic injury, neoplasia, surgery, drugs, metabolic, and neurologic disorders) could be considered as a cause of TOH. Pregnancy is a well-known risk factor of TOH. A similar disorder, migratory osteoporosis, also associated with pregnancy, has been postulated to have increased osteoclast activation called regional acceleratory phenomena [21]. Other risk factors such as alcohol consumption, steroid usage, smoking, hypothyroidism, hypophosphatasia, osteogenesis imperfecta, low testosterone, low vitamin D (25-cholecalciferol), and certain occupations are reported in the literature [1, 5, 14, 22–25].
Diagnosis
Magnetic resonance imaging (MRI) is the best method to demonstrate edema within bone and is sensitive enough to detect TOH as early as 48 h after the onset of symptoms [5, 16]. MRI findings that support TOH include intermediate signal sequences on T1-weighted images (Fig. 1a) and high signal intensity on T2-weighted images (Fig. 1b). Another MRI finding is hyper intensity on contrast enhanced images. Short-tau inversion recovery (or STIR) imaging allows homogeneous and global fat suppression on MRI, which also may be helpful in defining TOH (Table 2 with references [5, 11–16, 26–28]). The delayed peak enhancement of edematous marrow is particularly characteristic of TOH. Findings that favor TOH include a homogenous pattern of enhancement with no clear border, a diffuse pattern of edema with no focal defect, along with the presence of an irregular band of low signal intensity due to stress fracture, and lack of subchondral changes on T2-weighted or contrast-enhanced T1-weighted images [5, 7, 15, 16, 26]. The edema of TOH is usually located at the femoral head and may extend to the femoral neck and intertrochanteric region and is often accompanied by joint effusion [7, 26]. However, there is much dispute about predictive factors and disease progression. While patients differ in the amount, extent of edema and subchondral changes; Malizos (2004) et al. report that there is no correlation between the extent of edema and the duration of symptoms, but TOH with a spared subchondral zone resolves faster clinically. However, the time interval between onset of symptoms and MRI was different for each patient in their study [26]. On the other hand, Ergun (2008) et al. state that duration of clinical recovery correlated with the extent of edema, and the presence and size of subchondral fracture. These investigators find that subchondral fracture itself is also linked to the extent of edema [29]. On the contrary, Klontzas (2015) et al. describe that the duration of symptoms correlates statistically with the extent of edema, but not subchondral fracture [30]. In contrast, MRI findings of AVN may reveal femoral head deformity, subchondral radiolucency (crescent sign) (Figs. 2 and 3), single line sign with edema on T1-weighted image and double line sign with edema on T2-weighted image (Table 2).
While no radiographic changes are noted initially, 3–6 weeks from the onset of symptoms, diffuse osteopenia of the femoral head or periarticular demineralization can be appreciated on X-ray, yet the femoral head usually remains intact [7, 26, 31]. The absence of subchondral changes is an indicator of TOH [22]. The increase in blood flow and capillary permeability causes an augmentation in radionuclide uptake, thus a positive bone scan may be seen in all three phases of TOH and persist for weeks after clinical improvement [15, 26, 31]. While regional migratory osteoporosis (RMO) is similar in that it is also usually transient; it is defined by its asymmetric involvement and in its movement from proximal to distal, progressing unilaterally from the hip to knee and ankle [32]. Since RMO is sometimes associated with changes in bone mineral density, serial bone density measurements may demonstrate the progression of both bone loss and subsequent recovery of affected areas [21].
Course and treatment
Transient osteoporosis, especially TOH, probably happens in the setting of microfractures and bone marrow edema causing separation of the bone trabeculae. During the recovery process, if the primary insult is removed and adequate reparative mechanisms proceed, then as edema and hypervascularity resolve, clinical and radiological improvement will follow. Conservative therapy, suppression of bone resorption, or induction of bone formation may reduce further damage, promote recovery, or shorten duration of recovery. However, if the patient with TOH does not follow these recommendations or, if for other reasons, TOH does not reverse, a fracture may ensue, confusing the diagnosis with AVN. Hayes et al. in a review in 1993, report that TOH improved after several weeks to months with conservative therapy. With the lack of histologic or radiographic evidence of bone necrosis in TOH patients, they surmise that risk factors for AVN determine the distinction between resolving TOH and further progression to osteonecrosis [33]. Otherwise, continued injury to the bone and further increase in edema may lead to necrosis, bone collapse, articular distortion, and fracture of the bone [5]. However, TOH and AVN have some common risk factors such as alcohol consumption, nicotine or corticosteroids usage, and coagulation disorders [5, 11, 14]. Debatably, TOH might be considered as an early-stage precursor of AVN. However, while TOH generally resolves without sequelae, AVN is usually an irreversible and progressive disease, resulting from interruption of blood supply to the femoral head, sometimes also leading to permanent joint failure [7].
The mechanism explaining bone fragility in TOH is not completely understood. Histopathology findings from patients with TOH show increased intramedullary pressure and enhanced bone formation [5]. Studies report evidence of osteoclastic bone resorption, increased resorption lacunae filled with osteoclasts, signs of microfractures, and thin bone trabeculae [15, 34–37].
Medical treatment with bisphosphonate therapy, calcitonin, or teriparatide is reported to shorten recovery time for TOH in small, non-randomized, and non-controlled case studies. We have summarized the outcomes of TOH patients with these various treatments (Tables 3, 4, 5). Conservative therapy, including minimizing weight-bearing activities, rest, using crutches, wheelchairs, hot packs, analgesics, ultrasound therapy, or interferential current therapies is commonly recommended [7, 17, 18]. Intravenous pamidronate in 15 cases shows an average clinical recovery of 2 months, comparing favorably to a historical control recovery of 6 months [45]. However, alendronate oral therapy in 8 cases shows an average clinical recovery of 6 months, similar to that of the controls (Table 3) [4]. Calcitonin use in 6 cases shows a shortened mean clinical recovery of 4.7 months (Table 3). Combination of calcitonin and bisphosphonate therapy, zoledronate, or teriparatide in different reports shows almost a 1 month recovery time (Tables 3, 4) [40–42]. Nasal calcitonin, strontium ranelate, teriparatide, and bisphosphonates are reported to treat pregnancy-associated osteoporosis during pregnancy or lactation. Bisphosphonate therapy may improve bone density in pregnancy-associated osteoporosis [65, 66]. However, exposure to bisphosphonate before conception or during pregnancy might affect fetal skeletal mineralization, shorten gestational age, cause low birth weight, transient hypocalcaemia of the neonate, and spontaneous abortion and/or anomalies [66, 67]. Calcitonin does not cross the placenta, appears safe during pregnancy, and has no known deleterious effects on the fetus [68, 69]. Using calcitonin during pregnancy, as reported in some cases, may reduce duration or recovery [50, 59–64].
Core decompression therapy, which is recommended for AVN, does not appear to improve outcomes any more than medical therapy (duration of recovery was between 1 week and 8 months, medium 1.5–2 months) (Table 5). However, the data are limited to very few case reports, and further study of TOH therapy is needed before these agents can be recommended routinely.
Complications and prognosis
Subchondral, femoral neck, and subcapital fracture are rare but potential complications of TOH. While men and women have the same incidence of subchondral fracture, femoral neck, and subcapital, fracture are seen more frequently in female patients (Table 6). Of the two male cases, one occurred in a man with osteogenesis imperfecta and the other in a 79-year-old man (Table 6).
Of the 24 reported cases of TOH who developed femoral neck or subcapital fracture, 22 are women who fractured during pregnancy or after delivery. In one study, only one patient had a true femoral head fracture, as opposed to a femoral head stress fracture, and also suffered a subchondral fracture [70]. In pregnancy, mechanical overload and metabolic changes, such as an increase in 24-h urinary excretion of calcium, low PTH levels during the first trimester, increase in parathyroid hormone-related peptide (PTH-rP) levels around the mid-second to third trimester, and upregulation of calcitriol (1,25 (OH)2 vitamin D) may increase susceptibility to microfracture and fracture [17, 96–98]. Increase in bone resorption markers and decrease in bone mineral density are found during pregnancy and lactation. During lactation, suckling and prolactin reduce estradiol and progesterone by suppressing the hypothalamic-pituitary-ovarian axis. Suckling, prolactin, low estradiol, and calcium-sensing receptor increase production of PTH-rP from the mammary tissue and placenta [66, 99]. Most fractures (femoral neck, subcapital, femoral head, and subchondral fracture) occur before treatment, but some happen during conservative therapy (Table 6). As a clinical point, therapy to shorten recovery time might be helpful with regards to reducing risk of fracture.
Progression of TOH to AVN or osteonecrosis is another rare but potential complication of TOH. Five articles report the development of AVN in 9 cases of TOH [100–104]. Differentiation of AVN and TOH is important. Szwedowski et al. (2014) outlines that in AVN, T1-weighted imaging shows fibrotic connective tissue around necrotic bone with a weak signal. Bone marrow edema of AVN occurs in more advanced stages of necrosis and has correlation with pain progression and fracture of the femoral head [16]. Signs on MRI that indicate osteonecrosis include femoral head deformity, crescent sign (seen as subchondral radiolucency on MRI), single-line sign with edema on T1-weighted images, double-line sign with edema on T2-weighted images, low signal intensity of subchondral area, or the presence of subchondral area of low signal intensity at least 4 mm thick on T2 or contrast-enhanced T1-weighted images (Table 2) [31, 105].
Summary
Transient osteoporosis, especially TOH, usually presents with the acute onset of pain. A primary insult causing microfractures and vascular disturbance may result in bone marrow edema with separation of the bone trabeculae. Transient marrow edema causes temporary bone loss. While TOH usually affects the hip, it may migrate to other joints, especially those with weight bearing. MRI is the best method of diagnosis of TOH and to rule out traumatic injury, fracture, degenerative processes, inflammatory diseases, ischemic injury, infectious, and neoplasia. Differentiating AVN from TOH on MR imaging is important to prevent needless surgical intervention. Based on reported cases in the literature, medical therapies (including teriparatide, zoledronic acid, or combination of alendronate and calcitonin) may reduce duration of symptoms. Core decompression is not better than medical therapy in TOH alone. Pregnant women are at risk of femoral neck fracture, yet most treatments are contraindicated. In pregnancy, calcitonin, might shorten the duration of recovery which may prevent this complication. However, further investigation and randomized clinical trials are needed to determine the best method to reduce pain and improve bone health simultaneously, in order to decrease risk of complications such as AVN, fracture and joint degeneration [106].
Abbreviations
- AVN:
-
avascular necrosis
- BMD:
-
bone mineral density
- BME:
-
bone marrow edema
- BMES:
-
Bone marrow edema syndrome
- DXA:
-
dual-energy X-ray absorptiometry
- PTH:
-
parathyroid hormone
- PTH-rP:
-
parathyroid hormone-related peptide
- RMO:
-
regional migratory osteoporosis
- STIR:
-
short-tau inversion recovery
- TOH:
-
transient osteoporosis of the hip
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The authors express their appreciation to Namrata Gumaste, divisional assistant, NYU Langone Medical Center, for a helpful revision of this manuscript.
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The abstract of part of this study has been presented as an oral presentation at the American Society of Bone and Mineral Research (ASBMR), September 12–14, 2014, Houston, TX [1].
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Asadipooya, K., Graves, L. & Greene, L.W. Transient osteoporosis of the hip: review of the literature. Osteoporos Int 28, 1805–1816 (2017). https://doi.org/10.1007/s00198-017-3952-0
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DOI: https://doi.org/10.1007/s00198-017-3952-0