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Shark Cartilage
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[General information | History | Laboratory/Animal/Preclinical studies]
[Human/Clinical studies | Adverse effects | Glossary | References]
[For more information]

This shark cartilage summary provides an overview of the use of shark cartilage as a treatment for cancer. The summary includes a brief history of shark cartilage research, the results of clinical studies on shark cartilage, and possible side effects of shark cartilage use. A glossary of scientific terms used in the summary appears just before the references. This shark cartilage summary contains the following key information:

  • Shark cartilage and Bovine (cow) cartilage have been studied as treatments for cancer and other medical conditions for more than 30 years.
  • Numerous shark cartilage products are sold commercially in the United States as dietary supplements.
  • Three principal mechanisms of action have been proposed to explain the antitumor potential of shark cartilage: 1) it kills cancer cells directly; 2) it stimulates the immune system; 3) it blocks the formation of new blood vessels (angiogenesis), which tumors need for unrestricted growth.
  • At least three different inhibitors of angiogenesis have been identified in bovine cartilage, and two angiogenesis inhibitors have been purified from shark cartilage.
  • Only three human studies have been published to date, and the results are inconclusive about the effectiveness of shark cartilage as a treatment for cancer.
  • Additional clinical trials of shark cartilage as a treatment for cancer are now being conducted

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General Information
Shark cartilage and bovine cartilage have been investigated as treatments for cancer, psoriasis, arthritis, and a number of other medical conditions for more than 30 years.[1-13, reviewed in 14-21] At least some of the interest in shark cartilage as a treatment for cancer arose from the mistaken belief that sharks, whose skeletons are made primarily of cartilage, are not affected by this disease.[reviewed in 17,22] Although reports of malignant tumors in sharks are rare, a variety of cancers have been detected in these animals.[reviewed in 22-24] Nonetheless, several substances that have antitumor activity have been identified in shark cartilage.[25-48, reviewed in 2-4,6-10,16-21,49,50] More than a dozen clinical studies of shark cartilage as a treatment for cancer have already been conducted,[2-4,10-13, reviewed in 6-9,15-20] and additional clinical studies are now under way.[51,52, reviewed in 9,16]

The absence of blood vessels in shark cartilage led to the hypothesis that shark cartilage cells (also known as chondrocytes) produce one or more substances that inhibit blood vessel formation.[reviewed in 28-31,36,37,50] The formation of new blood vessels, or angiogenesis, is necessary for tumors to grow larger than a few millimeters in diameter (i.e., larger than approximately 100,000 to 1,000,000 cells) because tumors, like normal tissues, must obtain most of their oxygen and nutrients from blood.[reviewed in 34,35,42,53-56] A developing tumor, therefore, cannot continue to grow unless it establishes connections to the circulatory system of its host. It has been reported that tumors can initiate the process of angiogenesis when they contain as few as 100 cells.[55] Inhibition of angiogenesis at this early stage may, in some instances, lead to complete tumor regression.[55] The possibility that shark cartilage could be a source of one or more types of angiogenesis inhibitors for the treatment of cancer has prompted much research.

The major structural components of shark cartilage include several types of the protein collagen and several types of glycosaminoglycans, which are polysaccharides.[reviewed in 21,30,31,40,50,56,57] Chondroitin sulfate is the major glycosaminoglycan in shark cartilage.[reviewed in 40,56] Although there is no evidence that the collagens in shark cartilage, or their breakdown products, can inhibit angiogenesis, there is evidence that shark cartilage contains at least one angiogenesis inhibitor that has a glycosaminoglycan component (see Laboratory/Animal/Preclinical Studies section).[48] Other data indicate that most of the antiangiogenic activity in shark cartilage is not associated with the major structural components.[reviewed in 27,31,50]

Some glycosaminoglycans in shark cartilage reportedly have anti-inflammatory and immune system-stimulating properties,[58,59, reviewed in 1,2,14,17] and it has been suggested that either they or some of their breakdown products are toxic to tumor cells.[25, reviewed in 2,3] Thus, the antitumor potential of shark cartilage may involve more than one mechanism of action.

Shark cartilage products are sold commercially in the United States as dietary supplements. More than 40 different brand names of shark cartilage alone are available to consumers.[reviewed in 19] In the United States, dietary supplements are regulated as foods, not drugs. Therefore, premarket evaluation and approval by the Food and Drug Administration (FDA) are not required unless specific disease prevention or treatment claims are made. Because manufacturers of shark cartilage products are not required to show evidence of anticancer or other biologic effects,[reviewed in 19] it is unclear whether any of these products has therapeutic potential. In addition, individual products may vary considerably from lot to lot because standard manufacturing processes do not exist and binding agents and fillers may be added during production.[reviewed in 19]

To conduct clinical drug research in the United States, researchers must file an Investigational New Drug (IND) application with the FDA. To date, IND status has been granted to at least four groups of investigators to study shark cartilage as a treatment for cancer.[10,51,52,60, reviewed in 20] Because the IND application process is confidential and because the existence of an IND can be disclosed only by the applicants, it is not known whether other applications have been made.

In animal studies, shark cartilage products have been administered in a variety of ways. In some studies, oral administration of either liquid or powdered forms of shark cartilage has been used.[21,40,41,44- 46,61, reviewed in 7-9,16,49] In other studies, shark cartilage products have been given by injection (intravenous or intraperitoneal), applied topically, or placed in slow-release, plastic pellets that were surgically implanted.[27,28,33,34,36,39,41,43, reviewed in 29,48,50] Most of the latter studies investigated the effects of shark cartilage products on the development of blood vessels in the chorioallantoic membrane of chicken embryos, the cornea of rabbits, or the conjunctiva of mice.[27,28,33,36,39,41,43, reviewed in 29,48,50]

In human studies, shark cartilage products have been administered topically or orally, or they have been given by enema or subcutaneous injection.[2-4,6,10-13,51,52, reviewed in 7-9,15-18,20] For oral administration, liquid, powdered, and pill forms have been used.[2-4,6,10-13,51,52, reviewed in 7- 9,15-18,20] The dose and duration of shark cartilage treatment have varied in human studies, in part because different types of products have been tested.

In this summary, the brand name (i.e., registered or trademarked name) of the shark cartilage product(s) used in individual studies will be identified wherever possible.

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History
The therapeutic potential of shark cartilage has been investigated for more than 30 years. As noted previously (General Information section), shark cartilage products have been tested as treatments for cancer, psoriasis, and arthritis. Shark cartilage products have also been studied as enhancers of wound repair and as treatments for osteoporosis, ulcerative colitis, regional enteritis, acne, scleroderma, hemorrhoids, severe anal itching, and the dermatitis caused by poison oak and poison ivy.[59, reviewed in 1,14,17,21]

Early studies of shark cartilage's therapeutic potential used extracts of bovine cartilage. The ability of these cartilage extracts to suppress inflammation was first described in the early 1960s.[59] The first report that bovine cartilage contains at least one angiogenesis inhibitor was published in the mid-1970s.[33] The use of bovine cartilage extracts to treat patients with cancer and the ability of these extracts to kill cancer cells directly and to stimulate animal immune systems were first described in the mid- to late-1980s.[2,3,25,58]

In contrast, the first report that shark cartilage contains at least one angiogenesis inhibitor was published in the early 1980s,[39] and the only published report to date of a clinical trial of shark cartilage as a treatment for cancer appeared in the late 1990s.[10] The more recent interest in shark cartilage is due, in part, to the greater abundance of cartilage in sharks and its apparently higher level of antiangiogenic activity. It has been estimated that 6% of the body weight of a shark is composed of cartilage, compared with less than 1% of the body weight of a cow.[reviewed in 20] In addition, it has been estimated that, on a weight-for-weight basis, shark cartilage contains 1,000 times more antiangiogenic activity than bovine cartilage.[39, reviewed in 18]

As indicated previously, at least three different mechanisms of action have been proposed to explain the anticancer potential of shark cartilage: 1) it is toxic to cancer cells; 2) it stimulates the immune system; and 3) it inhibits angiogenesis. There is only limited evidence to support the first two mechanisms of action; however, the evidence in favor of the third mechanism is more substantial (see Laboratory/Animal/Preclinical Studies section).

The process of angiogenesis requires at least four coordinated steps, each of which may be a target for inhibition. First, tumors must communicate with the endothelial cells that line the inside of nearby blood vessels. This communication takes place, in part, through the secretion of angiogenesis factors, such as vascular endothelial growth factor (VEGF).[reviewed in 53-56,62] Second, the "activated" endothelial cells must divide to produce new endothelial cells, which will be used to make the new blood vessels.[reviewed in 54,56,62-64] Third, the dividing endothelial cells must migrate toward the tumor.[reviewed in 54-56,62-64] To accomplish this, they must produce enzymes called matrix metalloproteinases, which will help them carve a pathway through the tissue elements that separate them from the tumor.[reviewed in 62-65] Fourth, the new endothelial cells must form the hollow tubes that will become the new blood vessels.[reviewed in 56,62] It is conceivable that some angiogenesis inhibitors may be able to block more than one step in this process.

It is important to note that shark cartilage is relatively resistant to invasion by tumor cells [reviewed in 30-32,35,36,38,48,50] and that tumor cells use matrix metalloproteinases when they migrate during the process of metastasis.[reviewed in 18,26,32,49,65] Therefore, if the angiogenesis inhibitors in shark cartilage are also inhibitors of matrix metalloproteinases, then the same molecules may be able to block both angiogenesis and metastasis. It should also be noted that shark tissues other than shark cartilage have been reported to produce antitumor substances.[66-68, reviewed in 69]

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Laboratory/Animal/Preclinical Studies
The antitumor potential of cartilage has been investigated extensively in laboratory and animal studies. Some of these studies have focused on the toxicity of cartilage products toward cancer cells in vitro.[25,42, reviewed in 2,3,16,18,45]

In one study, cells from 22 freshly isolated human tumors (nine ovary, three lung, two brain, two breast, and one each of sarcoma, melanoma, colon, pancreas, cervix, and testis) and three human cultured cell lines (breast cancer, colon cancer, and myeloma) were treated with Catrix®, which is a commercially available powdered preparation of bovine cartilage.[25, reviewed in 2,3,18] In the study, the growth of all three cultured cell lines and of cells from approximately 70% of the tumor specimens was inhibited by 50% or more when Catrix® was used at high concentrations (1 to 5 milligrams per milliliter of culture fluid). It is unclear, however, whether the inhibitory effect of Catrix® in this study was specific to the growth of cancer cells because its effect on the growth of normal cells was not tested. In addition, the "toxic" component of Catrix® has not been identified, and it has not been shown that equivalent inhibitory concentrations of this component can be achieved in the bloodstream of patients who may be treated with either injected or oral formulations of this product. (See Human/Clinical Studies section for a discussion of human studies of Catrix®.)

A liquid (i.e., aqueous) extract of shark cartilage, called AE-941/Neovastat®, has also been reported to inhibit the growth of a variety of cancer cell types in vitro.[reviewed in 16,45] However, these results have not been published in a peer-reviewed, scientific journal.

In contrast, a commercially available preparation of powdered shark cartilage (no brand name given) was reported to have no effect on the growth of human astrocytoma cells in vitro.[42] In this published study, the shark cartilage product was tested at only one concentration (0.75 milligrams per milliliter).[42]

The immune system-stimulating potential of cartilage has also been investigated in laboratory and animal studies, but just one study has been published in the peer-reviewed, scientific literature.[58] In that study, Catrix® was shown to stimulate the production of antibodies by mouse B cells (B lymphocytes) both in vitro and in vivo. However, increased antibody production in vivo was observed only when Catrix® was given by intraperitoneal or intravenous injection. It was not observed when oral formulations of Catrix® were used.[58] It is important to note that, in most experiments, the proliferation of mouse B cells (i.e., normal, nonmalignant cells) in vitro was increasingly inhibited as the concentration of Catrix® was increased (tested concentration range: 1 to 20 milligrams per milliliter). Catrix® has also been reported to stimulate the activity of mouse macrophages in vivo,[reviewed in 2,18] but results demonstrating this effect have not been published in a peer-reviewed, scientific journal. To date, no studies of the immune system-stimulating potential of shark cartilage have been reported.

A large number of laboratory and animal studies have been published concerning the antiangiogenic potential of cartilage.[5,26-31,33-37,39-43] Overall, these studies have revealed the presence of at least three angiogenesis inhibitors in bovine cartilage[26,27,30,31,35,37, reviewed in 29,50] and, in shark cartilage, of at least two.[41-43,48]

Three angiogenesis inhibitors in bovine cartilage have been very well characterized.[26,27,30,31,35,37, reviewed in 29,50] They are relatively small proteins with molecular masses that range from 23,000 to 28,000.[26,27,37, reviewed in 29] These proteins, called cartilage-derived inhibitor (CDI), cartilage-derived antitumor factor (CATF), and cartilage-derived collagenase inhibitor (CDCI) by the researchers who purified them,[26,27,35] have been shown to block endothelial cell proliferation in vitro and new blood vessel formation in the chorioallantoic membrane of chicken embryos.[27,30,31,35,37, reviewed in 29,50] Two of the proteins (CDI and CDCI) have been shown to inhibit matrix metalloproteinase activity in vitro,[26,27,31, reviewed in 29] and one (CDI) has been shown to inhibit endothelial cell migration in vitro.[27, reviewed in 29] These proteins do not block the proliferation of normal cells or of tumor cells in vitro.[27,30,35, reviewed in 29,50] When the amino acid sequences of CDI, CATF, and CDCI were determined, it was discovered that they were the same as those of proteins known otherwise as TIMP-1 (tissue inhibitor of matrix metalloproteinases 1), ChMI (chondromodulin I), and TIMP-2 (tissue inhibitor of matrix metalloproteinases 2), respectively.[26,27,31,37, reviewed in 50]

As indicated previously, shark cartilage, like bovine cartilage, contains more than one type of angiogenesis inhibitor. One shark cartilage inhibitor, named U-995, reportedly contains two small proteins, one with a molecular mass of approximately 14,000 and the other with a molecular mass of approximately 10,000.[41] Both proteins have shown antiangiogenic activity when tested individually.[41] The exact relationship between these two proteins, as well as their relationship to the larger bovine angiogenesis inhibitors, is not known because amino acid sequence information for U-995 is not available. U-995 has been reported to inhibit endothelial cell proliferation, endothelial cell migration, and matrix metalloproteinase activity in vitro and the formation of new blood vessels in the chorioallantoic membrane of chicken embryos.[41] It does not appear to inhibit the proliferation of other types of normal cells or of cancer cells in vitro[41] Intraperitoneal, but not oral, administration of U-995 has been shown to inhibit the growth of mouse sarcoma-180 tumors implanted subcutaneously on the backs of mice and the formation of lung metastases of mouse B16-F10 melanoma cells injected into the tail veins of mice.[41]

The second angiogenesis inhibitor identified in shark cartilage appears to have been studied independently by three groups of investigators.[42,43,48] This inhibitor, which was named SCF2 by one of the groups,[48] is a proteoglycan that has a molecular mass of less than 10,000. Proteoglycans are combinations of glycosaminoglycans and protein.[reviewed in 56] The principal glycosaminoglycan in SCF2 is keratan sulfate.[48] SCF2 has been shown to block endothelial cell proliferation in vitro,[42,43,48] the formation of new blood vessels in the chorioallantoic membrane of chicken embryos,[42,43] and tumor-induced angiogenesis in the cornea of rabbits.[42,43]

Other studies have indicated that AE-941/Neovastat®, the previously mentioned aqueous extract of shark cartilage, has antiangiogenic activity,[5, reviewed in 45] but the molecular basis for this activity has not been defined. Therefore, whether AE-941/Neovastat® contains U-995 and/or SCF2 or some other angiogenesis inhibitor is not known. It has been reported that AE-941/Neovastat® inhibits endothelial cell proliferation and matrix metalloproteinase activity in vitro and the formation of new blood vessels in the chorioallantoic membrane of chicken embryos.[5, reviewed in 45] It may also inhibit the action of vascular endothelial growth factor (VEGF), thus interfering with the communication between tumor cells and nearby blood vessels.[47] AE-941/Neovastat® has also been reported to inhibit the growth of DA3 mammary adenocarcinoma cells and the metastasis of Lewis lung carcinoma cells in vivo in mice.[45,46, reviewed in 8,9,16,49] In the Lewis lung carcinoma experiments, AE-941/Neovastat® reportedly enhanced the antimetastatic effect of the chemotherapy drug cisplatin.[46, reviewed in 8,9,16,49] It is important to note, however, that most of the results obtained with AE-941/Neovastat® have not been published in peer-reviewed, scientific journals.

Additional in vivo studies of the antitumor potential of shark cartilage have been published in the peer-reviewed, scientific literature.[40,44,61] In one study, oral administration of powdered shark cartilage (no brand name given) was shown to inhibit chemically induced angiogenesis in the mesenteric membrane of rats.[40] In another study, oral administration of powdered shark cartilage (no brand name given) was shown to reduce the growth of GS-9L gliosarcomas in rats.[44] In contrast, it was reported in a third study that oral administration of two powdered shark cartilage products, Sharkilage® and MIA Shark Powder, did not inhibit the growth or the metastasis of SCCVII squamous cell carcinomas in mice.[61]

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Human/Clinical Studies
More than a dozen clinical studies of shark cartilage as a treatment for cancer have been conducted since the early 1970s.[2-4,10-13, reviewed in 6-9,15-20] However, results from only three studies have been published in peer-reviewed, scientific journals.[2,3,10] Although additional clinical studies are now under way,[51,52, reviewed in 9,16] the cumulative evidence to date is inconclusive regarding the effectiveness of shark cartilage as a cancer treatment in humans.

It has been reported that AE-941/Neovastat® the previously mentioned aqueous extract of shark cartilage has little toxicity,[6-9,15,16,45,46] and there are indications from a retrospective analysis of data from the phase I/II trial that it may have anticancer activity in humans.[7] In addition, there is evidence from a randomized clinical trial that examined the effect of AE-941/Neovastat® on the angiogenesis associated with surgical wound repair that this extract contains at least one antiangiogenic component that is orally bioavailable.[70]

Two of the three published clinical studies evaluated the use of Catrix®, the previously mentioned powdered preparation of bovine cartilage, as a treatment for various solid tumors.[2,3] One of these studies was a case series that included 31 patients;[2] the other was a phase II clinical trial that included nine patients.[3]

In the case series,[2] all patients were treated with subcutaneously injected and/or oral Catrix®; however, three patients (one with squamous cell carcinoma of the skin and two with basal cell carcinoma of the skin) were treated with topical preparations as well. The individual dose, the total dose, and the duration of Catrix® treatment in this series varied from patient to patient; however, the minimum treatment duration was 7 months, and the maximum duration was more than 10 years. Eighteen patients had been treated with conventional therapy (surgery, chemotherapy, radiation therapy, hormone therapy) within 1 year of the start of Catrix® treatment; nine patients received conventional therapy concurrently (at the same time) with Catrix® treatment; and seven patients received conventional therapy both prior to and during Catrix® treatment. It was reported that 19 patients had a complete response, 10 patients had a partial response, and one patient had stable disease following Catrix® treatment. The remaining patient did not respond to cartilage therapy. Eight of the patients with a complete response received no prior or concurrent conventional therapy. Approximately half of the patients with a complete response eventually experienced recurrent cancer.

This clinical study had several weaknesses that could have affected its outcome, including the absence of a control group and the receipt of prior and/or concurrent conventional therapy by the majority of patients.

In the phase II trial[3] Catrix® was administered by subcutaneous injection only. All patients in this trial had progressive disease following radiation therapy and/or chemotherapy. Identical individual doses of Catrix® were given to each patient, but the duration of treatment and the total delivered dose varied because of disease progression or death. The minimum duration of Catrix® treatment in this study was 4 weeks. It was reported that one patient (with metastatic renal cell carcinoma) had a complete response that lasted more than 39 weeks. The remaining eight patients did not respond to Catrix® treatment. The researchers in this trial also investigated whether Catrix® had an effect on immune system function in these patients. No consistent trend or change in the numbers, percentages, or ratios of white blood cells (i.e., total lymphocyte counts, total T cell counts, total B cell counts, percentage of T cells, percentage of B cells, ratio of helper T cells to cytotoxic T cells) was observed, although increased numbers of T cells were found in three patients.

Partial results of a third clinical study of Catrix® are described in an abstract submitted for presentation at a scientific conference,[4] but complete results of this study have not been published in a peer-reviewed, scientific journal. In the study, 35 patients with metastatic renal cell carcinoma were divided into four groups, and the individuals in each group were treated with identical doses of subcutaneously injected and/or oral Catrix®. Three partial responses and no complete responses were observed among 22 evaluable patients who were treated with Catrix® for more than 3 months. Two of the 22 evaluable patients were reported to have stable disease and 17 were reported to have progressive disease following Catrix® therapy. No relationship could be established between Catrix® dose and tumor response in this study.

The third published study of cartilage as a treatment for cancer was a phase I/II trial that tested the safety and the efficacy of orally administered Cartilade®, a commercially available powdered preparation of shark cartilage, in 60 patients with various types of advanced solid tumors.[10] All but one patient in this trial had been treated previously with conventional therapy. According to the design of the study, no additional anticancer treatment could be given concurrently with Cartilade® therapy. No complete responses or partial responses were observed among 50 evaluable patients who were treated with Cartilade® for at least 6 weeks. However, stable disease that lasted 12 weeks or more was reported for 10 of the 50 patients. All 10 of these patients eventually experienced progressive disease.

Partial results of three other clinical studies of powdered shark cartilage are described in two abstracts submitted for presentation at scientific conferences,[11,12] but complete results of these studies have not been published in peer-reviewed, scientific journals. All three studies were phase II clinical trials that involved patients with advanced disease; two of the studies were conducted by the same group of investigators.[11] These three studies enrolled 20 patients with breast cancer,[11] 12 patients with prostate cancer,[11] and 12 patients with primary brain tumors.[12] All patients had been treated previously with conventional therapy. No other anticancer treatment was allowed concurrently with cartilage therapy. In two of the studies,[11] the name of the cartilage product was not identified; however, in the third study,[12] the commercially available product BeneFin® was used. Ten patients in each study completed at least 8 weeks of treatment and were, therefore, considered evaluable for response. No complete responses or partial responses were observed in any of the studies. Two patients in each study were reported to have stable disease that lasted 8 weeks or more.

The safety and the efficacy of AE-941/Neovastat®, , have also been examined in clinical studies.[6-9, reviewed in 15,16] However, results of these studies have been described only in abstracts presented at scientific conferences and in press releases by the manufacturer and not in peer-reviewed, scientific journals.

The exact number of clinical studies of AE-941/Neovastat® is difficult to determine because of inconsistencies in the information that is available. It appears that at least two clinical studies have been conducted: 1) a phase I/II trial of oral AE-941/Neovastat® as a single agent in 80 patients with advanced lung cancer and 72 patients with advanced prostate cancer, and 2) a study of oral AE-941/Neovastat® plus chemotherapy and/or radiation therapy in 126 patients with various types of solid tumors.[7-9,15,16] The phase I/II trial has been variously described as a single phase I/II study,[7-9,16] two phase I studies,[15,16], two phase II studies,[16] a study that involved only patients with advanced lung cancer,[7,8,16] and a study that involved both patients with advanced lung cancer and patients with advanced prostate cancer.[9]

On the basis of laboratory, animal, and human data provided by the manufacturer, two randomized phase III trials of AE-941/Neovastat® in patients with advanced cancer have been approved by the FDA. In one trial, treatment with oral AE-941/Neovastat® plus chemotherapy and radiation therapy is being compared to treatment with placebo plus the same chemotherapy and radiation therapy in patients with stage III non-small cell lung cancer.[51] In the other trial, treatment with oral AE-941/Neovastat ® is being compared to treatment with placebo in patients with metastatic renal cell carcinoma[52] Both trials are currently enrolling patients.

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Adverse Effects
The side effects associated with cartilage therapy are generally described as mild-to-moderate in severity. Inflammation at injection sites, dysgeusia, fatigue, nausea, dyspepsia, fever, dizziness, and edema of the scrotum have been reported after treatment with the bovine cartilage product Catrix®.[2-4] Nausea, vomiting, abdominal cramping and/or bloating, constipation, hypotension, hyperglycemia, generalized weakness, and hypercalcemia have been associated with the use of powdered shark cartilage.[10-12] The high level of calcium in shark cartilage may contribute to the development of hypercalcemia.[11,18] In addition, one case of hepatitis has been associated with the use of powdered shark cartilage.[71] Nausea and vomiting are the most commonly reported side effects following treatment with AE-941/Neovastat ®, the aqueous extract of shark cartilage.[7-9]

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