Chemistry and Form

Coenzyme Q10 (coQ10) belongs to a family of compounds known as ubiquinones, all of which are characterized by a functional group known as a benzoquinone . Ubiquinones are fat-soluble molecules with between 1 and 12 isoprene (5-carbon) units. Among the 10 naturally occurring coenzyme Q compounds, the ubiquinone found in humans is known as coenzyme Q10 because of the distinctive “tail” of 10 isoprene units (containing 50 carbons in toto) attached to its benzoquinone “head.”

Physiology and Function

In humans, coQ10 is synthesized in most tissues throughout the body. Three major steps are involved in the endogenous synthesis of coQ10: (1) synthesis of the benzoquinone structure from tyrosine or phenylalanine, (2) synthesis of the isoprene side chain from acetyl coenzyme A (CoA) via the mevalonate pathway, and (3) the condensation or merging of these two structures. 3-Hydroxy-3-methylglutaryl-CoA (HMG-CoA) reductase is the critical enzyme regulating coQ10 synthesis as well as cholesterol synthesis.

Coenzyme Q is highly soluble in lipids and is found in virtually all cell membranes, as well as lipoproteins. The primary biochemical action of coQ10 is as a coenzyme for numerous enzymes in the electron transport chain, a series of oxidation-reduction (redox) reactions involved in cellular respiration, where the presence of coQ in the inner mitochondrial membrane is required for the conversion of energy from carbohydrates and fats in the synthesis of adenosine triphosphate (ATP). Within the mitochondrial electron transport chain, coQ accepts electrons from reducing equivalents generated during fatty acid and glucose metabolism and transfers them to electron acceptors. Simultaneously, a proton gradient across that membrane results when coQ transfers protons outside the inner mitochondrial membrane. When the protons subsequently flow back into the mitochondrial interior, energy is released to form ATP.

Coenzyme Q10 has dual potential to enhance energy production by bypassing defective elements of the respiratory energy production chain and through its function as an antioxidant. Coenzyme Q can exist in three oxidation states: (1) the fully reduced ubiquinol form (CoQH2), (2) the radical semiquinone intermediate (CoQH), and (3) the fully oxidized ubiquinone form (CoQ). Thus, in its central role as a pro-oxidant within mitochondria, coQ10 enables aerobic energy gain, promotes unilateral proton accumulation, and generates reactive oxygen species (ROS) involved in physiological signaling. Ubiquinone can execute reversible addition of single electrons and protons. Lysosomal membranes critical to cellular detoxification and recycling contain particularly high concentrations of coQ. Recent research indicates that lysosomal ubiquinone maintains the optimal pH for cellular recycling through its double function as proton translocator and radical source, particularly under certain metabolic conditions such as an acid pH. Alternately, a range of research demonstrates a pervasive and potent role of coenzyme Q10 in protecting membranes and DNA from oxidative damage from free radicals directly and through suppression of the formation of oxidized lipids and the consumption of alpha-tocopherol. As a lipophilic molecule, the reduced form of coQ, coQH2, along with enzymes that are capable of reducing oxidized coQ back to coQH2, is particularly concentrated in mitochondrial cell membranes, where it acts as a key cellular antioxidant and provides protection against free-radical damage. However, the type of biomembrane where ubiquinone exerts its free-radical, chain reaction–breaking activity can significantly affect this action’s efficiency. Furthermore, coQH2regenerates alpha-tocopherol radicals back to the chain-breaking (i.e., antioxidant) form of vitamin E and thereby further contributes to the control of lipid peroxidation. This ability to counteract oxidative stress is particularly evident in its support of healthy cardiac tissue and its protection of endothelial function. Thus, coQ10’s unique chemistry enables it to function both as a pro-oxidant and as an antioxidant.

Known or Potential Therapeutic Uses

Coenzyme Q10 can be synthesized in vivo by all living organisms, including humans, and thus is not defined as a vitamin. However, in some situations, the need for coQ10 may surpass the body’s ability to synthesize it, so it may be regarded as “conditionally essential.” CoQ10 is well absorbed by oral administration, as evidenced by significant increases in serum, plasma, and lipoprotein concentrations of coQ10 after oral intake. ^1,2However, evidence from animal and human research is mixed as to the degree to which oral intake elevates levels in various target tissues, and how that effect might vary depending on state of health, influence of aging, and presence of dysfunction, depletion, or pathology in particular tissues and systems. ^3-7

In 1958, Professor Karl Folkers elucidated the chemical structure of coQ10 and noted its potential in the treatment of cardiovascular disease. However, his employer, Merck, chose to sell the formula and patent to a Japanese firm in favor of promoting Diuril, a new product at the time aimed at the cardiovascular drug market. Thus, although coQ10 developed a strong presence in medical and supplement markets in Japan, its entry into clinical use in the United States has been delayed but is steady growing.

Possible Uses

Alzheimer’s disease, angina, arrhythmia, breast cancer, cardiac bypass surgery, cardiomyopathy, cardiovascular disease, cerebellar ataxia (familial), chemotherapy support, chronic fatigue, chronic obstructive pulmonary disease (COPD), congestive heart failure (CHF), diabetes mellitus, diastolic dysfunction, fibromyalgia, gingivitis, human immunodeficiency virus (HIV) support, Huntington’s disease, hypertension, immune deficiencies, insulin resistance syndrome, ischemia, lung cancer, male infertility, mitochondrial diseases, mitral valve prolapse, muscular dystrophies, myocardial infarction, neurodegenerative diseases, Parkinson’s disease, periodontal disease, prostate cancer, renal failure, rhabdomyolysis.

Oral administration may also enhance aerobic capacity and muscle performance, especially in sedentary and elderly individuals. Conclusive evidence from large clinical trials has yet to be carried out to investigate this proposed action.

Deficiency Symptoms

The deficiency pattern associated with coQ10 has not been clearly defined, and it is widely assumed that endogenous production and a varied diet provide adequate coQ10 for most individuals. A deficiency may result from impaired synthesis caused by nutritional deficiencies, acquired defect in synthesis or utilization, or increased tissue needs resulting from illness. Most coQ10 in humans is internally synthesized. Genetic defects in coQ10 synthesis and metabolism are considered rare at this time. Deficiency can be caused or aggravated by depletion or deficiency of any of the many nutrients required within this 17-stage synthetic pathway, including riboflavin (vitamin B2), niacinamide (vitamin B3), pantothenic acid (vitamin B5), pyridoxine (vitamin B6), cobalamin (vitamin B12), folic acid, vitamin C, and several trace elements. As might be expected, given the central role of the HMG-CoA reductase enzyme in the coQ10 synthetic pathway, HMG-CoA reductase inhibitors (“statins”), which are widely prescribed for management of dyslipidemias and cardiovascular disease, have been implicated as an iatrogenic cause of coQ10 deficiencies.

CoQ10 concentrations in various tissues decline with advancing age, and elderly individuals are known generally to have lower levels of coQ10. ^8,9Likewise, researchers have observed that the patient populations exhibiting many of the conditions coQ10 is used to treat more often demonstrate low levels of coQ10; these include cardiomyopathy, gingivitis and periodontal disease, heart failure, and HIV/AIDS. Many researchers and clinicians consider at least a CHF subset to represent a coQ10 deficiency disease, to a significant degree. Decreased plasma levels of coQ10 have also been observed in individuals with diabetes and cancer. Lastly, individuals with the genetic polymorphisms called the LPL and NQO1 genotypes exhibit decreased coQ10 redox ratios, reflective of impaired ability to convert ubiquinone to ubiquinol. ¹⁰

Dietary Sources

Coenzyme Q10 is widely distributed in foods but in such small amounts that extraordinary serving sizes would be required to obtain intake levels typically provided by commercial preparations (e.g., 100 mg daily).

Organ meats (e.g., heart, liver), meat, poultry, and fish are the richest dietary sources of coenzyme Q10. Nuts provide relatively high levels, as do soybean and canola oils. Vegetables, fruits, eggs, and dairy products contain moderate levels of coQ10, with broccoli and spinach being relatively richer.

Studies in Denmark conducted during the 1990s found that average dietary intake of coQ10 was 3 to 5 mg per day. ^11,12Overall, dietary sources appear to provide most individuals with less than 10 mg/day. Foods are estimated to provide an average of 25% of plasma coQ10 in most individuals. Boiling appears to have little adverse effect, but frying destroys 14% to 32% of coQ10 in foods thus prepared. The precise dietary contribution to plasma coQ10 concentration is unknown in any given individual but is estimated to be approximately 25%.

Nutrient Preparations Available

Microcrystalline cellulose-coQ10 complex.

Complexing coenzyme Q10 with alpha-cyclodextrin may enhance bioavailability of coQ10 by approximately 35% compared to a microcrystalline cellulose-coQ10 complex. ¹³

Ubiquinol (QH) is the converted active form of coQ10. The conversion rate of coQ10 (ubiquinone) to ubiquinol tends to decline with age, rendering lowered serum levels of ubiquinol. Furthermore, LPL and NQO1 genotypes are associated with impaired ability to conduct this conversion. ¹⁰ However, outside the body, ubiquinol is extremely unstable without certain stabilizing procedures because it will convert to coQ10 on exposure to oxygen. ¹⁴ Since ubiquinone must be reduced to become active, oral ubiquinol may provide bioavailability up to eight times as great as that of oral ubiquinone.

Dosage Forms Available

Powder-filled hard-shell capsule, soft-gel capsule, liposomal spray, tablet, chewable wafer.

Oral coenzyme Q10 should be taken with a meal with some fat content since it is fat-soluble. Absorption decreases in the absence of lipid. Some experts suggest taking coQ10 with a small amount of olive oil to increase absorption. There is some evidence that coQ10 in oil suspension provides better bioavailability than granular form. ^15-17Chewable forms may also provide greater bioavailability than capsules or tablets.

Source Materials for Nutrient Preparations

Yeast fermentation, or semisynthetic process.

Kaneka Corporation of Japan, which is the only company to use yeast fermentation in the production of coQ10, produces the natural all- trans Q, which is identical to the coQ10 occurring in nature and has succeeded in obtaining “generally recognized as safe” (GRAS) status from the U.S. Food and Drug Administration (FDA). ¹⁸

Dosage Range

Adult

Dietary: No level has been established for optimal dietary intake of coenzyme Q10.

Supplemental/Maintenance: 25 to 60 mg twice daily.

Pharmacological/Therapeutic: Ranging from 30 to 60 mg twice daily to 50 to 100 mg two to three times daily, depending on condition and in concert with a health care professional trained in nutritional therapies. Daily dosage levels of 300 to 600 mg have been used in clinical and research settings in the treatment of conditions such as severe cardiovascular disease and advanced breast cancer. Administration of 60 to 100 mg per day will usually double plasma levels of coQ10 in adults. Evidence indicates that oral intake does not impair endogenous coQ10 synthesis.

Toxic: None established.

Pediatric (<18 Years)

Coenzyme Q10 is usually not prescribed for infants or children.

Laboratory Values

Plasma and lymphocyte coenzyme Q10 and coenzyme Q10H2levels.

Overview

All available evidence indicates that coenzyme Q10 is generally safe. No significant adverse effects or toxicities have been reported as being associated with oral intake of coQ10. CoQ10 in doses up to 900 mg daily is safe and well tolerated in healthy adults for 4 weeks. ¹⁹ Even continued doses of 600 mg/day for 30 months and 1200 mg/day for up to 16 months have not been associated with significant adverse effects. ^20,21

Nutrient Adverse Effects

General Adverse Effects

Occasional reports of mild nausea, gastrointestinal (GI) discomfort, anorexia, or skin eruptions have been reported with oral intake of coQ10. Other reported adverse effects include fatigue, insomnia, headache, dizziness, irritability, photosensitivity, dyspepsia, vomiting, diarrhea, dermatitis, or flulike symptoms. Reported adverse effects typically receded when oral coQ10 was stopped or dosage levels or format were modified. Dividing daily intake into two or three dosages may eliminate adverse effects, especially if more than 100 mg/day is being used.

Pregnancy and Nursing

Adverse effects are not predicted, and reports are lacking. However, the lack of controlled studies involving pregnant or lactating women precludes claims of safety and suggests that oral intake should be avoided during such life cycles.

Infants and Children

Adverse effects are not predicted, and reports are lacking. CoQ10 administration is not recommended unless otherwise indicated as essential.

Contraindications

No contraindications have been established for coQ10.

Precautions and Warnings

No precautions or warnings are known at this time for healthy individuals. Individuals with CHF or other serious cardiovascular conditions should only discontinue coQ10 under the supervision of the prescribing health care professional; withdrawal of coQ10 intake could potentially contribute to relapse.

Cautions have been voiced regarding coQ10 use by individuals with diabetes, hypoglycemia, hypertension, or liver disease. Evidence to substantiate clinically significant adverse events is limited. Supervision and appropriate monitoring are usually adequate in most cases.

Strategic Considerations

The primary clinical uses of coenzyme Q10 supported by human trials are in the treatment of CHF, angina pectoris, mitochondrial encephalopathies, mitochondrial cytopathies, chronic myalgic conditions, dystrophies, fibromyalgia, and Parkinson’s disease. In such conditions characterized by mitochondrial dysfunction, the functions of coQ10 in mitochondrial bioenergetics and protection against oxidative stress appear to be paramount. CoQ10’s strong antioxidant activity also enables it to function as an effective therapeutic ally when administered in conjunction with medications, such as doxorubicin, that cause adverse effects as a result of inducing oxidative damage. Virtually all antioxidants are capable of functioning as pro-oxidants, either when present in overwhelming quantity (e.g., high-dose intravenous ascorbate) or when present with inadequate antioxidant network partners in an environment of high oxidative stress (e.g., smokers with poor dietary antioxidant intake who are supplemented with synthetic beta-carotene). Perhaps the unique aspect of coQ10 is that it functions physiologically both as a pro-oxidant and antioxidant and can be regenerated back to its reduced or antioxidant form through normal cellular enzymatic processes.

Many pharmacological agents inhibit coQ10 synthesis, interfere with its function, and induce coQ10 deficiency states. In such circumstances, coadministration of coQ10 can prevent or reverse adverse drug effects, often in a manner that enhances therapeutic efficacy and improves clinical outcomes. In these situations, coQ10 carries no significant risks, and controversy as to its use is minimal.

Coenzyme Q10 is most widely used in the prevention and treatment of heart disease, more recently incorporated into acute cardiac care. For example, in an innovative placebo-controlled randomized trial involving 49 patients, Damian et al. ²² found that combining liquid coQ10 (250 mg followed by 150 mg three times daily for 5 days) with mild hypothermia immediately after out-of-hospital cardiac arrest and cardiopulmonary resuscitation (CPR) appears to improve survival and may prevent reperfusion injury and neurological damage in survivors. The astroglial protein S100 is an established biochemical marker of central nervous system (CNS) injury. Mean serum S100 protein 24 hours after CPR was significantly lower in the coQ10 group (0.47 vs. 3.5 ng/mL). Three-month survival in the coQ10 group was 68% versus 29% in the placebo group, and nine coQ10 patients survived with a Glasgow outcome scale of 4 or 5 (vs. five placebo patients). As for chronic cardiovascular conditions and attendant mortality risk, evidence is not unanimously in support of its efficacy, but as part of a lifestyle that includes regular exercise and a healthy diet (particularly omega-3 oils), coQ10 may help significantly decrease cardiovascular risk. ²³ In particular, chronic CHF has reached epidemic proportions and is the single most common cause for hospitalization among individuals over age 65 in the United States; in more than half these patients, impaired left ventricular (LV) diastolic function plays a major role. CoQ10 appears to provide particular benefit in reversing diastolic impairment, including adverse effects on LV diastolic function associated with atorvastatin therapy. ²⁴ This therapeutic action, as well as the broader role of coQ10 in the treatment of chronic cardiovascular conditions, leads directly into what may become a major controversy within medicine.

The issue of the interaction between statin drugs and coenzyme Q10 presents some of the most complex and timely clinical issues affecting coQ10 and its role in human health. HMG-CoA reductase inhibitors have demonstrated important and substantial cardiovascular clinical benefits, including reducing mortality; however, the impact of coQ10 depletion with long-term statin therapy (≥20 years) is only beginning to be considered in a substantive manner, particularly concerning patients with heart failure. Nevertheless, in the first clinical research addressing some of these concerns, Go et al. ²⁵ conducted a propensity-adjusted cohort study of all-cause death and hospitalization for heart failure during a median of 2.4 years of follow-up after initiation of statin therapy. They reported that among “adults diagnosed with heart failure who had no prior statin use, incident statin use was independently associated with lower risks of death and hospitalization among patients with or without coronary heart disease.” Although encouraging, the short duration of follow-up in this study precludes any substantive conclusions regarding long-term safety of statin therapy.

The medical literature currently portrays statin therapy as a virtual “panacea” for prevention and treatment of cardiovascular conditions (and a multitude of other pathologies), but the parameters of the statin discussion have yet to expand beyond cholesterol and inflammation and incorporate comprehensive functional assessment of all risk factors. In a paper with potentially disturbing implications, Getz et al. ²⁶ discussed the issue of estimating the high-risk group for cardiovascular disease in a well-defined Norwegian population according to European guidelines and the systematic coronary risk evaluation system. They raised concerns regarding the efficacy of applying the current cholesterol reduction goals (of total cholesterol below 180 mg/dL) being established as public policy in Europe and the United States. They noted that, in Norway, one of the world’s healthiest countries, 85% of the men and more than 20% of the women over age 40 would need to be treated for high cholesterol under the American recommendations. Thus, in this population with relatively low rates of heart disease, “implementation of the 2003 European guidelines on prevention of cardiovascular disease in clinical practice would classify most adult Norwegians at high risk for fatal cardiovascular disease.” ²⁶ These observations prompted provocative responses in the scientific literature questioning the necessity, safety, and prudence of broad-based implementation of aggressive lipid-lowering standards. In particular, Ravnskov et al. ²⁷ pointed out that application of these recommendations would result in the majority of the world’s adult population being treated with statin drugs; to which they added, “As the risk to benefit ratio for a more drastic lowering of low density lipoprotein cholesterol is unknown, we question the wisdom of this advice.” Notably, May et al. ²⁸ found that a total cholesterol level approaching 200 mg/dL is associated with higher survival in patients with heart failure than levels below 140 mg/dL.

Paradoxical evidence showing both reduced cardiovascular risk, including heart attack and stroke, and stress on cardiac tissue induced by the inherent action of HMG-CoA reductase inhibitors has yet to withstand the test of time over decades. Although 20 years may be required for ongoing inhibition of endogenous ubiquinone synthesis resulting in mitochondrial interference and diastolic dysfunction to manifest as impaired hepatic, neurological, and cardiac dysfunction or frank cardiomyopathy resulting in chronic CHF, long-term statin use could represent a significant iatrogenic risk factor for some patients, particularly those with baseline coQ10 levels that are suboptimal or compromised by aging, malnutrition, drug depletions, genotypic susceptibility, and other adverse influences. Thus, for example, Tsivgoulis et al. ²⁹ found that patients with asymptomatic neuromuscular disorders may have their condition precipitated by statin use.

Although statin therapy may reduce inflammation, as reflected by reduced C-reactive protein (CRP) concentrations, other critical cardiovascular risk factors such as lipoprotein(a), homocysteine, and fibrinogen are not modified to any significant degree by inhibition of HMG-CoA reductase. Moreover, preliminary research indicates that hypotheses of reduced atherosclerosis and calcific aortic stenosis through aggressive lipid-lowering therapies using statins may have been premature and overly optimistic in the face of mixed findings; in fact, statins appear to block the beneficial effects of exercise on intimal thickening. ^30,31Likewise, in the IDEAL study comparing high-dose atorvastatin with usual-dose simvastatin for secondary prevention after myocardial infarction (MI), Pedersen et al. ³² found that although aggressive lipid lowering significantly reduced the risk of other composite secondary endpoints and nonfatal acute MI, intensive lowering of low-density lipoprotein (LDL) cholesterol did not reduce coronary death or cardiac arrest with resuscitation, and that there were no differences in cardiovascular or all-cause mortality.

Thus far, the potential for integrative clinical strategies based on synergistic activities has been neglected and may be most deserving of thorough investigation. A thorough review of the literature of statin therapy that incorporates a frank appraisal of risk factors suggests that the growing enthusiasm for statin drugs over the past decade may eventually succumb to a harsh realization that they are appropriate for a relatively select patient population, specifically those with severe and recalcitrant hypercholesterolemia for whom other therapies have proved ineffectual. Notably, the issue of individual pharmacogenomic variability influencing efficacious or adverse responses to statin therapy is only beginning to be considered. ³³ Furthermore, until continued concerns about neuropathies, skeletal myopathies, and cardiomyopathies known or suspected to be associated with long-term statin therapy, as well as their potential for enhancing growth of subclinical malignancies through angiogenic and possibly immunomodulating mechanisms, are more fully investigated, the use of these widely prescribed, arguably overprescribed, medications should be more carefully considered, given the paucity of long-term studies of these agents, which, once instituted, will often be consumed for the lifetime of most patients. For example, in a retrospective case-control study, Wilke et al. ³⁴ found that CYP3A genotype was associated with increased severity of atorvastatin-induced muscle damage, but not an increased risk for development of such adverse effects, as indicated by elevated serum creatine kinase (CK) levels. Thus, individuals who were homozygous for CYP3A5^*3 demonstrated greater serum CK levels than patients who were heterozygous for CYP3A5^*3, when concomitant lipid-lowering agents (gemfibrozil with or without niacin) were sequentially removed from the analysis. Similarly, in comparing nine haplotypes in the gene that carries the code for HMG-CoA reductase within both Caucasian and African Americans, Krauss et al. ³⁵ found that treatment with simvastatin (40 mg) demonstrated significant genetic differences in statin response in lowering LDL cholesterol levels. Consequently, individuals who have a genetic problem with metabolizing statins could have a larger depletion of coQ10 (because of a higher level of the statin drug) and thus could have more problems. conversely, individuals who tolerate statins better may be metabolizing them faster, and thus their Q10 may not become as depleted. Moreover, half of all individuals who have heart attacks do not have hypercholesterolemia.

Meanwhile, other methods of cardiovascular disease risk reduction, such as a healthy and balanced diet, regular exercise, and omega-3 fatty acid supplementation, should be pursued vigorously as a coordinated broad response to multiple risk factors. In such an integrative approach, for example, the therapeutic benefits of statin therapy can be complemented or enhanced through coadministration of fish oil orL-carnitine. ^36-43Nevertheless, when Studer et al. ²³ conducted a review of data on the efficacy and safety of different antilipidemic agents and diets on mortality, they found that fish oil and statins were the most effective interventions for lowering cardiac mortality risk, fish oil being superior to statin therapy in terms of lowering all-cause mortality, despite very modest effects on lipids.

However, other evidence has emerged that could complicate the picture. In a 6-year, randomized, controlled trial involving 140 middle-aged men, Rauramaa et al. ³⁰ found that men undergoing statin treatment are significantly less likely to exhibit benefit from exercise in slowing atherosclerosis than those exercising but not taking statins. Intermittent exercise enhances coQ10 biosynthesis, resulting in higher coQ10 levels, and this could be a factor in the well-known health benefits of exercise. The findings from this study suggest that statins may neutralize the beneficial effect of exercise, at least in part, through their blocking of coQ10 biosynthesis. Levy and Kohlhaas ⁴⁴ conducted a review of studies examining the effects of statin drugs, prescribed for reduction of cholesterol levels, on plasma concentrations of coQ10 and considerations regarding coadministration of coQ10 and concluded that “statin drug therapy does indeed reduce blood concentrations of coenzyme Q10.” However, the authors determined that “due to the small number and dissimilar nature of studies available, the ability of the reviewers to draw any strong conclusions was limited.” Nevertheless, “results from isolated studies suggest that statin drugs may induce mitochondrial dysfunction.” Furthermore, “limited data suggest that supplementation with coenzyme Q10 may be beneficial in patients taking statin drugs who 1) have a family history of elevated cholesterol levels, or 2) have a family history of heart failure, or 3) are over 65 years of age. Further studies investigating the effects of statin drugs on the development of myotoxicity are warranted, particularly among high-risk populations.” ⁴⁴ Continued research is needed to investigate the long-expressed hypothesis that many of the other adverse effects associated with statins derive from its interference with coQ10 synthesis and function.

Administration of coQ10 alone or in conjunction with other agents, as part of an integrative therapeutic strategy, offers significant potential for enhancing clinical outcomes in individuals with a range of cardiovascular conditions. In particular, numerous researchers and clinicians have reported many cases of extraordinary clinical improvement in individuals with conditions such as CHF in which the expected progression is characterized by steady worsening and morbidity within 2 years under conventional therapy. At the least, incorporation of coQ10 into the therapeutic repertoire presents an opportunity to correct myocardial deficiency of coQ10 and enhance synthesis of coQ10-requiring enzymes, thereby extending the duration and enhancing the quality of life of such patients.

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