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NSAIDs may interfere with skeletal healing


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Taken from Medscape... who knew that NSAIDs could increase fracture risk and interfere with fracture healing (especially COX-2 inhibitors like Celebrex)... think about all the fractures we see and how people self-medicate, and the potential for complications in the hip fracture geriatric population...

To see Figure 1, you'll have to click this link: http://www.medscape.com/viewarticle/587888 and click through the article. For those who prefer the forum format, here it is below...

Treating Skeletal Pain: Limitations of Conventional Anti-inflammatory Drugs, and Anti-neurotrophic Factor as a Possible Alternative

Cory J. Xian; Xin-Fu Zhou

Authors and Disclosures

Posted: 02/10/2009; Nat Clin Pract Rheumatol. 2009;5(2):92-98. © 2009 Nature Publishing Group

Summary

Inflammatory and injury-induced skeletal pain are common conditions, and both conventional nonselective NSAIDs and the newer cyclo-oxygenase-2-specific inhibitors are widely used as post-traumatic and post-surgical analgesics. However, new research suggests that these drugs, particularly the cyclo-oxygenase-2 inhibitors, have a negative effect on the healing process in fractured bone and within orthopedic surgical sites, thus highlighting a need to develop new approaches for managing skeletal pain. Various experimental studies have revealed that locally upregulated neurotrophic factors, especially nerve growth factor, have a major role in mediating injury-induced or inflammatory pain. Nerve growth factor inhibitors, therefore, might be an effective alternative modality for post-traumatic and post-surgical analgesia, without impairing bone healing.

Introduction

Chronic pain is a leading cause of morbidity worldwide, with a prevalence of 50% in Europe—a figure that is likely to rise in elderly patients with chronic disorders, such as rheumatoid arthritis or osteoarthritis.[1] Nonselective NSAIDs, which inhibit cyclo-oxygenase (COX)-1 and COX-2, and the newer COX-2-specific inhibitors are commonly used in the management of post-traumatic or post-operative skeletal pain. However, studies have demonstrated a strong association between these agents and impaired bone healing, highlighting the need for new approaches to skeletal pain management. Data from the past few years indicate that neurotrophins—growth factors that are required for the survival, development and maintenance of neuronal cells—might be involved in the pathophysiology of injury-induced or inflammatory skeletal pain. This Review discusses the inhibitory effects of NSAIDs (particularly COX-2-specific agents) on bone healing, and the potential role of neurotrophic factors as mediators of skeletal pain and as targets for the treatment of skeletal pain.

NSAIDS as Post-traumatic or POST-operative Analgesia

Conventional, nonselective NSAIDs, which inhibit COX-mediated production of prostaglandins, are widely used to treat pain and reduce inflammation in patients with chronic inflammatory or autoimmune disorders.[2] The management of acute post-operative pain, however, remains suboptimal, despite the increasing use of clinical acute pain services; furthermore, there are disparities in opinion, both between clinicians and in the clinical practice guidelines, regarding the use of the newer modalities in this setting.[3,4,5] Conventional NSAIDS have become an important component of both post-traumatic and post-operative analgesia, and are used frequently in the treatment of acute athletic injury.[6,7,8,9] The proven efficacy of these agents in the management of post-operative pain, together with their opioid-sparing role in multimodal analgesia, have led to significantly reduced levels of opioid-related side effects.[10]

The therapeutic effects of nonselective NSAIDs are mediated by inhibition of injury-induced or inflammation-induced COX-2 expression.[11] Clinical studies have shown that, as a result of inhibition of the physiological enzyme, COX-1, NSAIDs can be associated with an increased risk of fracture in patients with rheumatic disease.[12] In addition, their use has been called into question following concerns about the associated increased risks of gastrointestinal and cardiovascular adverse events, increased bleeding, impaired wound healing, and increased bone nonunion rates.[3,13,14] Furthermore, evidence from experimental research conducted over the past two decades suggests that NSAIDs have an inhibitory effect on fracture repair.[11]

The newer NSAIDS, which specifically inhibit COX-2, are as effective as classical NSAIDs and are associated with a lower risk of gastrointestinal adverse events, as well as a lack of inhibitory effects on platelet function and, therefore, a reduced risk of blood loss.[1,3,9] Large-scale studies, however, have shown that these newer agents can increase the risk of adverse cardiovascular events.[1,15,16,17]

Effects of COX-2-specific Inhibitors on Bone Fracture Healing

Bone healing is a complex process that involves the coordinated actions of various cell types. The initial hematoma formation and inflammatory response result in the release of cytokines and growth factors that are important in regulating subsequent healing events, such as infiltration of progenitor cells. In the reparative and remodeling phases, bone formation and remodeling involve angiogenesis and the formation and functions of bone-forming cells (i.e. osteoblasts) and bone-resorptive cells (i.e. osteoclasts). It is now clear that all these events are regulated by prostaglandins, the products of COX enzymes.[11] When COX-2 is induced during the inflammatory response, increased prostaglandin expression upregulates various inflammation mediators and regulates the formation and activities of osteoblasts and osteoclasts.[18]

Given the central role of prostaglandins in the bone healing process and the widespread use of NSAIDs in the management of post-injury and post-surgery orthopedic pain, the possible adverse effects of these agents in bone healing, particularly the COX-2-specific inhibitors, are concerning. Blockade of COX-2 function has been associated with variable outcomes in experimental models of bone, ligament and tendon repair.[19] One clinical study showed that short-term use of the COX-2 inhibitor celecoxib had no effect on rates of nonunion following spinal fusion surgery;[20] however, another clinical study indicated that longer-term COX-2 inhibition could increase the risk of fracture and delay healing.[11]

Experimental studies suggest that COX-2 inhibitors can impair tissue repair and recovery of mechanical strength following acute skeletal injury, which could have important clinical implications for the rates of ongoing morbidity and future susceptibility to injury.[21] Accumulating evidence suggests that COX-2 activity in the early stages of bone healing is critical for efficient bone repair. Indeed, fracture healing was shown to be impaired in mice with mutated COX-2.[22] Furthermore, administration of celecoxib during the early stages of fracture repair in rats (but not before or 14 days after fracture) significantly reduced the mechanical strength of the fracture callus and often caused bone nonunion.[23] Similarly, early post-operative administration of COX-2 inhibitors in rodent bone fracture models resulted in increased fibrous tissue at fracture sites, limited blood flow across the fracture, delayed remodeling of calcified cartilage, and reduced bone formation in the fracture callus, or delayed allograft healing and incorporation.[24,25,26,27]

Interestingly, it has been shown that COX-2-specific drugs inhibit fracture healing to a greater degree than classical NSAIDS.[27] Moreover, the magnitude of this effect seems to be related to treatment duration, as the inhibitory effect was reversible after discontinuation of short-term treatment.[27] Up to 10% of bone fractures can result in delayed union or nonunion;[28] however, the extent of the contribution of COX-2 inhibitors to this rate of delayed union or nonunion remains to be investigated.

Guidelines on the use of NSAIDS in Fractures and Orthopedic Surgery

As NSAIDS are known to inhibit bone healing,[29] and opiates cause cognitive dysfunction and respiratory depression, the available treatment options for pain related to bone fractures or surgery remain limited. Based on animal and clinical studies, practical management guidelines have been generated to assist orthopedic surgeons and sports physicians with regard to the use of NSAIDS for analgesia. Clinicians are advised to carefully evaluate individual patient risk factors and the pharmacokinetics of individual NSAIDS when assessing the risks and benefits of discontinuing NSAID therapy in the perioperative setting.[14] NSAIDS can be used appropriately in the management of acute ligament sprains, muscle strains, tendinitis, and eccentric muscle injury, with the length of treatment being kept as short as possible. However, these agents are not recommended, or should be used with caution or only for a short duration,[6,27] in the treatment of fractures and stress fractures, which are associated with higher risks of nonunion or delayed union due to osseous, vascular, or patient-related factors,[25] or in the treatment of chronic muscle injury.[8]

Neurotrophic Factors in Injury-induced or Inflammatory Pain

Neurotrophins are a family of proteins that are essential for the proliferation, differentiation and survival of primary sensory neurons[30] and, as shown in recent studies, participate in the development of pain states. Each neurotrophin binds with high affinity to a specific receptor tyrosine kinase (Trk), and all bind to the common receptor p75. In adult animals, approximately 40–50% of primary sensory neurons express the nerve growth factor (NGF) receptor TrkA, 20–30% express the brain-derived neurotrophic factor (BDNF) receptor TrkB, and 20–30% of neurons express the neurotrophin 3 (NT3) receptor TrkC. Neurotrophins are expressed in sensory target organs and tissues, such as skin, blood vessels and visceral tissues;[31] BDNF is also highly expressed by a subpopulation of sensory neurons.[32] Neurotrophins released from their targets act on and maintain normal functioning of sensory neurons. In pathological conditions, such as trauma and inflammation, neurotrophins are upregulated by injured tissues,[33] and sensory nerve terminals are activated by target-derived neurotrophins, which participate in tissue healing and the development of pain.

Neurotrophins in Wound and Tissue Repair and Fracture Healing

Apart from its known biological effects on neuronal cells, NGF might also be an important component of the wound healing and tissue repair process. Early studies reported a therapeutic role for NGF in tissue repair, particularly in otherwise untreatable ulcers in patients with diabetes and in patients with severe pressure ulcers.[34] In addition, NGF accelerated the rate of wound healing both in normal mice and in healing-impaired diabetic mice.[35] Interestingly, NGF administered after injury was associated with the promotion of wound healing and increased numbers of fibroblasts and blood capillaries in granulation tissues in mice.[36]

While NGF can be detected in periosteal osteoprogenitor cells in intact bone, NGF protein has also been detected in osteoprogenitor cells, marrow stromal cells, osteoblasts, some chondrocytes, endothelial cells, the periosteal matrix of the fracture callus, and skeletal muscle, suggesting that NGF and all these entities participate in fracture repair and re-innervation.[37] In a mouse model of fractured ribs, immunoreactivity of NGF, BDNF and NT3, and the receptors TrkA and TrkC, was observed in osteoblasts and/or hypertrophic chondrocytes in the bone forming area at the fracture callus.[38] In addition, mRNA levels of these neurotrophins were elevated during the healing process. Localized, intense ingrowth of new sensory nerve fibers containing the neuropeptide CGRP (calcitonin gene-related peptide) was also observed at the fracture callus in rats.[39] As CGRP immunoreactivity coincides with the amount of new bone formation, this finding suggests an association between CGRP-positive innervation and fracture healing.

These findings indicate that neurotrophins might be involved in bone or nerve healing as autocrine and/or paracrine factors during fracture repair. Although treatment with anti-NGF antibodies did not seem to interfere with the bone healing process, as assessed by mechanical testing and histomorphometric analysis,[40] the potential role of neurotrophins and their mechanisms of action in bone fracture healing require further investigation.

Neurotrophins in Injury-induced or Inflammatory Pain

Various studies have shown that neurotrophins, mainly NGF, are involved in the pathophysiology of injury-induced pain in nerve tissues, peripheral tissues and intervertebral discs. Neurotrophins have an established role in neural survival, collateral sprouting of sensory axons,[41,42] and regulation of nociceptive sensory neurons.[43] Increased expression and secretion of NGF, NT3 and BDNF have been implicated in injury-induced neuropathic pain after axotomy of the sensory system or the motor nerve.[44] Interestingly, tibial fracture in rats induced upregulation of NGF in hindpaw skin and tibia bone, as well as sciatic nerve neuropeptide content.[45]

NGF is secreted by target tissues (such as macrophages and Schwann cells following nerve injury, and by basal keratinocytes in the skin), and regulates the excitability of nociceptor fibers by altering the expression of key sodium channels, receptors and neuropeptides involved in the transmission of pain stimuli.[46] Local or systemic administration of NGF in rodents has been shown to induce acute thermal hyperalgesia and delay mechanical hyperalgesia, suggesting that NGF itself is sufficient to elicit hyperalgesia.[47,48] In addition, injection of NGF into the neck muscles of mice evoked neuronal activation in areas of the brainstem and cervical spinal cord that are involved in the processing of deep noxious input,[49] indicating that NGF has a role in the pathophysiology of neck muscle nociception. In humans, intravenous or intramuscular injection of low-dose NGF (1 μg/kg) resulted in widespread pain in deep tissues and hyperalgesia at the injection site.[50,51] Systemic or local blockade of NGF bioactivity, however, inhibited the effects of inflammation on the sensitivity of sensory neurons.[48]

Nociceptive nerve ingrowth into the usually aneural inner parts of painful lumbar intervertebral discs is a known cause of discogenic back pain; accumulating evidence suggests that NGF-induced nerve growth could have a key role in the pathophysiology of inflammatory back pain. A localization study showed a causal link between substance-P-positive, CGRP-positive nociceptive nerve ingrowth into the painful disc and NGF produced by blood vessels growing into the disc from adjacent vertebral bodies.[52]

In addition, inflammatory back pain in the lumbar facet joints has been associated with increased numbers of BDNF-positive neurons and the phenotypic switch to large neurons innervating these joints in rats.[53] BDNF-positive small dorsal root ganglion (DRG) neurons have an important neuromodulatory role in inflammatory conditions; therefore, the presence of BDNF immunoreactivity in DRG neurons innervating the intervertebral disc suggests that, under physiological conditions, these DRG sensory neurons can transmit inflammatory pain from the intervertebral disc.[54] Furthermore, constitutive NGF expression in cultured human intervertebral disc cells was increased in the presence of the proinflammatory cytokines interleukin-1β and tumor necrosis factor.[55] Similarly, cultured lumbar NGF-sensitive DRG neurons exhibited increased axonal growth potential in response to neuronal injury in the presence of tumor necrosis factor.[56]

These studies suggest that, apart from being involved in the pathophysiology of neuropathic pain following nerve and peripheral tissue injury, neurotrophins have an important role in the development of injury-induced or inflammation-induced back pain.

Possible Mechanisms of Action of NGF in Bone-Injury-Induced Pain

Although the potential pathophysiological mechanisms of NGF in bone-injury-induced pain remain unclear, the studies discussed above suggest that the ensuing inflammation triggers a cascade of proinflammatory cytokine upregulation, which in turn increases NGF synthesis in macrophages, chondrocytes, fibroblasts and osteoblasts at the site of injury (Figure 1). NGF released from these cells might then directly or indirectly act on sensory neurons, resulting in pain. NGF activates TrkA on sensory nerves, upregulating the expression of pronociceptive molecules, such as capsaicin receptor (TRPV1), BDNF, and neuropeptides (substance P and CGRP), in sensory neurons, which mediate nociception via peripheral and central mechanisms. NGF also causes pain indirectly by activating TrkA on mast cells, which release a variety of nociceptive activators such as neuropeptides.[47] Furthermore, NGF can activate TrkA on sympathetic neurons, which triggers sprouting of sympathetic nerves and the release of catecholamines, which interact with sensory neurons and cause ectopic nerve firing. Nociceptive activators produced from central or peripheral routes might act upon nociceptive sensory neurons, causing the release of neurotransmitters in the dorsal horn, which in turn sensitize spinal cord neurons and transmit pain after a bone injury. Bone-injury-induced pain might, therefore, be mediated by increased nociception due to the actions of NGF on both the peripheral and central nervous pathways.

Figure 1.

Potential functions and mechanisms of action of NGF in the development of post-injury pain. Inflammatory cells or bone healing cells at the fracture site upregulate NGF, which can act on sensory neurons directly or indirectly, resulting in pain. NGF activates its receptor (TrkA) on sensory nerves, which upregulates the expression of pronociceptive molecules, such as BDNF and neuropeptides (e.g. SP and CGRP) in sensory neurons, which mediate nociception via peripheral and central mechanisms. In addition, NGF can cause pain indirectly by activating TrkA on mast cells (which release a variety of nociceptive activators) and on sympathetic neurons. Abbreviations: BDNF, brain-derived neurotrophic factor; CGRP, calcitonin gene-related peptide; DRG, dorsal root ganglion; NGF, nerve growth factor; SP, substance P; TrkA, receptor tyrosine kinase A.

Anti-NGF Therapy for Injury-INDUCED or Surgery-induced Pain

Despite the development of new technologies to aid post-operative pain control,[4] safer and more effective modalities for pain management after skeletal trauma or surgery are still needed. As most of the CGRP-positive sensory nerve fibers innervating the bone express the NGF receptors TrkA and p75,[57,58] blocking the sensitization and activation of these fibers and nociceptors would represent an attractive approach to relieving musculoskeletal pain induced by trauma, injury or surgery. Increasing attention, therefore, has focused on evaluating the potential efficacy of anti-NGF therapy in pain management.

In a mouse model of femur fracture, treatment with anti-NGF antibody on the first day after fracture resulted in a 50% reduction in pain-related behavior and did not seem to interfere with bone healing, as assessed by mechanical testing and histomorphometric analysis.[40] A similar study showed that administration of anti-NGF antibody reduced fracture-induced pain-related behaviors by over 50%, a level of reduction also achieved with a dose of 10 mg/kg of morphine.[29] Moreover, bone healing was not impaired, as measured by callus formation, fracture site bridging or mechanical bone strength. This study also indicated that NGF is likely to be involved in the maintenance, but not the acute generation, of fracture pain. As CGRP-positive and TrkA-positive fibers constitute the majority of sensory fibers innervating the bone, the antihyperalgesic action of an anti-NGF antibody could be effective in attenuating pain resulting from bone fracture or bone surgery. However, although anti-NGF treatment reduced nociceptive sensitization and preserved some bone mass in a rat model of tibial fracture, it did not decrease hindpaw edema, warmth or cytokine production, suggesting that anti-NGF treatment reduced some, but not all, signs characteristic of the complex regional pain syndrome.[45] This finding might have been due to the complexities involved in the pathogenesis of injury-induced skeletal pain and NGF signaling.[45]

Furthermore, anti-NGF therapy seems to be efficacious in reducing pain associated with spinal cord injury or bone cancer. Administration of anti-NGF antibodies attenuated mechanical hyperalgesia following spinal cord injury in rats, suggesting that anti-NGF therapy is a potential analgesic treatment for central pain.[59] In a mouse prostate model of bone metastasis, where significant bone formation and bone destruction occur simultaneously, NGF-blocking antibody produced a significant reduction in both the early and late stages of bone cancer pain-related behaviors.[57] Interestingly, this therapy did not influence tumor-induced bone remodeling, formation of osteoblasts and osteoclasts, tumor growth, or markers of sensory or sympathetic innervation in the skin or bone. In a similar mouse model of bone cancer, administration of an anti-NGF antibody was found to produce a profound reduction in both ongoing and movement-evoked pain-related behaviors.[58]

Conclusions

Both conventional and COX-2-specific NSAIDS are important components in the management of pain after skeletal trauma or surgery. The limitations associated with these agents, including a possible role in the impairment of fracture healing, highlight the need to develop new modalities of pain management. Neurotrophic factors, particularly NGF, have been shown to mediate injury-induced or inflammatory pain of the skeleton, and studies have demonstrated that anti-NGF therapy could represent an attractive and effective alternative to NSAIDs, without compromising bone healing and remodeling. Further studies are required to understand how NGF and other neurotrophic factors, and their receptors, mediate pain evoked by injury, surgery, chronic inflammation, or cancer of the skeletal system. Questions remain regarding the cellular sources of the neurotrophic factors at or near the pain epicenter, and the molecular mechanisms of pain development. In addition, future studies are needed to evaluate or develop more-effective analgesic agents, based on the neuropathic roles of neurotrophic factors with minimal interference of their normal physiological neurotrophic functions and their functions in tissue and bone healing. More preclinical and clinical studies are needed to determine the role of these potential new modalities in clinical practice.

Posted

Wendy,

It's interesting that you posted that study!

Recently, I was seen by my ortho doc; (follow up for the fractures I recieved in my motorcycle wreck), and he stated this very information. He said that one reason that the fractures were slow in healing was because NSAIDS were inhibiting bone production/healing. Unfortunately, I haven't had the time to research further into the subject.

In light of how often NSAIDS; (Motrin, Naproxin, Ibuprofen) are prescribed for their analgesic and anti-inflamatory properties, this information is unsettling to say the least.

I wasn't aware that NSAIDS were 'at risk' of decreasing bone strength and increase in the risk of fractures.

This definately makes one stop and consider the limited options for pain management after injury induced or post operative incidents, especially in those patients that are already dealing with osteoporosis.

Posted

Interesting. I knew that NSAIDs interfere with platelet function, and now this. Just another example of how dangerous OTC meds can be.

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