Chronic and Acute Illness

Document Sample
Chronic and Acute Illness Powered By Docstoc
					              SECTION




              2
Chronic and Acute
           Illness
CHAPTER
CHAPTER
          5      Insulin Resistance and the
                 Metabolic Syndrome




    Chapter Topics
                 Introduction
                 Insulin Resistance and the Metabolic Syndrome
                 Risk Factors, Prevention, and Management of the Metabolic Syndrome
                 The Role of Hyperinsulinemia in the Metabolic Syndrome
                 Causes and Management of Gout
                 Causes and Management of the Polycystic Ovary Syndrome
                 Medication Issues with Insulin Resistance
                 The Role of the Nurse or Other Health Care Professional in Prevention and Management of
                      the Metabolic Syndrome

    Objectives
                 After completing this chapter, you should be able to:
                 ■   Describe the metabolic syndrome.
                 ■   Identify individuals at risk for the metabolic syndrome.
                 ■   Recognize an appropriate lifestyle plan for preventing and managing insulin resistance.
                 ■   Explain the application of the Dietary Guidelines in managing insulin resistance.

    Terms to Identify
                 Acanthosis nigricans             Glucagon                        Lipoprotein lipase
                 Androgens                        Glycemic index                  Metabolic obesity
                 Atherosclerosis                  Gout                            Nonalcoholic fatty liver
                 C-peptide                        Hirsutism                         disease
                 C-reactive protein (CRP)         Hyperglycemia                   Oral glucose tolerance test
                 Central obesity                  Hyperinsulinemia                  (OGTT)
                 Cutaneous papilloma              Hypoglycemia                    Polycystic Ovary Syndrome
                                                                                    (PCOS)
                 Dyslipidemia                     Impaired fasting glucose
                                                                                  Prediabetes
                 Endometrial hyperplasia          Impaired glucose tolerance
                                                                                  Thrifty gene
                 Ferritin                         Insulin resistance




                                                                                                           151
152    SECTION 2      Chronic and Acute Illness


INTRODUCTION
         It has been over 10 years since the metabolic syndrome received official recognition.
         It was considered a theory before then. The metabolic syndrome, also known as the
         insulin resistance syndrome, was initially called Syndrome X.
              Insulin resistance describes a condition in which the body cells resist the action
         of insulin, leading to poor use of blood glucose at the cellular level. Various causes
         have been suggested, from hormonal and enzymatic factors to issues of
         inflammation and problems with cellular structures. It is now well recognized that
         lifestyle and diet exert their influence on individuals with a genetic tendency
         toward insulin resistance. Obesity and lack of physical activity are known to
         worsen the genetic predisposition to insulin resistance.
              The metabolic syndrome is often discussed in terms of the common gene theory
         because it is commonly found. An estimated 40% of U.S. adults between the ages of
         40 and 74 have prediabetes (see later section). The rate of insulin resistance in some
         populations is as high as 60%. Insulin resistance is also associated with the common
         gene theory because it is the underlying cause of many chronic health problems.
              About one third of persons with insulin resistance go on to develop type 2
         diabetes. Most individuals with type 2 diabetes still have hyperinsulinemia.
         However, the amount of insulin produced is not adequate to overcome the
         resistance at the cellular level. The result is high blood glucose levels or diabetes
         mellitus (see Chapter 8). The World Health Organization (WHO) has estimated that
         there will be around 300 million persons with diabetes by 2025. It is anticipated that
         Asia will be at the forefront because of a genetic tendency for insulin resistance
         along with changing lifestyles.
              Obesity is now an epidemic throughout the world and is found with the health
         problems of the metabolic syndrome, including type 2 diabetes, hypertension, and
         hyperlipidemia (see Chapter 7). The medical community faces an emerging epidemic
         of type 2 diabetes in children and adolescents as the obesity epidemic continues
         (Miller and Silverstein, 2005). It is further predicted there will be an epidemic of
         early cardiovascular morbidity and mortality in years to come unless the epidemic
         of obesity is stemmed (Pontiroli, 2004).
              This chapter provides an overview of the metabolic syndrome. Other chapters
         in Section Two expand on the specific health problems associated with this
         syndrome, including central obesity, coronary heart disease, and diabetes, with the
         resulting adverse effects on the kidneys. Research is expanding on other health
         conditions associated with the metabolic syndrome, such as certain forms of cancer.
         As this section points out, the health problems associated with insulin resistance are
         realized only through environmental factors, with diet playing a large role.

WHAT IS THE METABOLIC SYNDROME?
          The National Cholesterol Education Program’s Adult Treatment Panel III definition
          uses easily measured clinical findings of increased abdominal circumference,
          elevated triglycerides, low levels of high-density–lipoprotein cholesterol (HDL-C),
          elevated fasting blood glucose, and/or elevated blood pressure. Three of these
          five are required for diagnosis of the syndrome. Gout (a condition related to high
          levels of uric acid; see later in this chapter) is often found with the metabolic
          syndrome as well.
                               Insulin Resistance and the Metabolic Syndrome   CHAPTER 5        153


                    There are different definitions of the criteria to use in making the diagnosis of
               the metabolic syndrome. The American Association of Clinical Endocrinologists
               has identified the following risk factors:
                  ■ Obesity or overweight body mass index (BMI) >25 (especially with central

                    obesity or metabolic obesity—carrying weight in the abdomen or having a
                    high waist-to-hip ratio; see Chapter 6)
                  ■ Elevated triglycerides: 150 mg/dL (1.69 mmol/L)

                  ■ Low HDL cholesterol

                    Men <40 mg/dL (1.04 mmol/L)
                    Women <50 mg/dL (1.29 mmol/L)
                  ■ Elevated blood pressure ≥130/85 mm Hg

                  ■ 2-Hour postglucose challenge >140 mg/dL (199 mg/dL; prediabetes)

                  ■ Fasting glucose between 110 and 126 mg/dL (6.15 and 7.05 mmol/L; prediabetes)

                  ■ Other risk factors:

                    Family history of type 2 diabetes, hypertension, or cardiovascular disease (CVD)
                    Polycystic ovary syndrome (PCOS): a clinical diagnosis based on high levels of
                         male hormones, male pattern hair growth, and ovarian cysts (see later in
                         this chapter)
                    Sedentary lifestyle
                    Advancing age
                    Ethnic groups having high risk for type 2 diabetes or CVD
                    Diagnosis depends on clinical judgment based on risk factors.
                    One condition found with the metabolic syndrome includes atherosclerosis (a
               buildup of plaque in the arteries and blood vessels; see Chapter 7). Although there
               are a variety of causes of atherosclerosis, an association with diabetes is well
               known. Because atherosclerosis generally is noted before the diagnosis of diabetes,
               it is believed that excess insulin related to insulin resistance promotes the plaque
               buildup. An increased tendency to form clots is also found with the metabolic
               syndrome and type 2 diabetes and can cause a variety of circulatory problems.
               Therefore persons with the metabolic syndrome are at increased risk of heart disease.
                    Certain cancers have been associated with the metabolic syndrome. Known
               cancers related to the metabolic syndrome include cancers of the breast, pancreas,
               liver, and colon and uterine (endometrial) cancer. An epidemic pattern of colon
               cancer and type 2 diabetes among Japanese persons has been noted. However, rates
               for colon cancer among Japanese in the United States are even higher than among
               those living in Japan. It is believed that the rise of colon cancer reflects the
               westernization of food intake (Kuriki et al., 2004). Newer research has linked
               prostate and ovarian cancers with the metabolic syndrome (see Chapter 10).
                    Other health problems that have recently been connected with the metabolic
               syndrome and insulin resistance include Nonalcoholic fatty liver disease—a
               condition of fat buildup in the liver (Brea et al., 2005) and hypothyroidism (Dessein
               et al., 2004).

WHAT MEASUREMENTS CAN HELP DIAGNOSE INSULIN RESISTANCE?
        A fasting blood glucose between 100 and 125 mg/dL is referred to as impaired
        fasting glucose and is indicative of prediabetes. Another test that can help diagnose
        prediabetes is the 2-hour oral glucose tolerance test (OGTT) (blood glucose test
154     SECTION 2      Chronic and Acute Illness


                performed 2 hours after a 75-g carbohydrate drink). An OGTT blood glucose level
                of 140 to 199 mg/dL is referred to as impaired glucose tolerance and is indicative
                of insulin resistance and prediabetes.
                     As hyperinsulinemia is found with insulin resistance, measurements of insulin
                levels can help confirm the diagnosis of the metabolic syndrome. Insulin is measured
                using different techniques. One is the ratio of fasting glucose levels to fasting insulin
                levels. It has been found that a fasting glucose-to-insulin ratio less than 7 may serve
                as an early identification of children at risk for complications of insulin resistance
                (Silfen et al., 2001). One indirect measure of insulin production is C-peptide.
                     Another lab value increasingly taken into account is the level of C-reactive
                protein (CRP) (a type of protein found with inflammation). Low-grade chronic
                inflammation reflected by increased CRP can identify those at risk for type 2 diabetes
                and coronary heart disease. Over one third of children and adolescents with the
                metabolic syndrome have been found to have high levels of CRP (Ford et al., 2005).
                Overweight children and adolescents with a BMI over the 85th percentile (see
                Chapters 6 and 12) have been found to have elevated CRP and fasting insulin levels
                (Kelly et al., 2004). Women with PCOS (see section later in this chapter) are often
                insulin resistant with increased risk for type 2 diabetes and coronary heart disease.
                Women with PCOS have shown significantly elevated CRP concentrations (Kelly
                et al., 2001).
                     Research is linking high levels of ferritin (a substance that holds iron in the
                blood) with insulin resistance. High iron stores have been linked to the metabolic
                syndrome (Jehn et al., 2004). The association between heme iron and diabetes risk
                may be a result of a relationship between hepatic iron overload and insulin
                resistance (Piperno et al., 2004). High hemoglobin levels are associated with excess
                weight, hypertension, hyperlipidemia (see Chapter 7), and hyperinsulinemia (Choi
                et al., 2003). Heme-iron intake from red meat sources has been positively associated
                with the risk of type 2 diabetes (Jiang et al., 2004).
                     Body weight measurement is another means of assessment. Individuals in the
                upper normal weight range (BMI over 23) and mildly overweight range (BMI over
                25) are at increased risk for having the metabolic syndrome, and screening is
                advised to help prevent diabetes and cardiovascular disease (St-Onge et al., 2004).

What Do We Know about Risks for Insulin Resistance?
             Historically, thinking has generally focused on the development of obesity as the
             cause of insulin resistance and the listed health conditions. This is reflected in
             warnings that obesity can cause diabetes. However, research continues to indicate
             that insulin resistance has a strong genetic link. Thus, not everyone with obesity
             will develop diabetes.
                  Persons who have inherited a genetic predisposition to insulin resistance
             probably have ancestors who survived repeated bouts of famine. It is likely that
             several thousands of years ago, before there were restaurants, corner grocery stores,
             refrigeration, and transportation, many of our ancestors faced continual cycles of
             famine. Those who were able to survive likely had the ability to be thrifty with food
             kilocalories. In fact, insulin resistance is often referred to as the thrifty gene theory
             (being thrifty in calorie expenditure; see Chapter 6 for management of obesity
             related to insulin resistance).
                                Insulin Resistance and the Metabolic Syndrome   CHAPTER 5          155


                     Many of us have the genetic legacy of those survivors of famine, in that persons
                who inherit the thrifty gene gain body fat easily in times of plenty. They also tend to
                have a difficult time losing weight, whether through self-imposed dieting or
                environmental factors that reduce the food supply. This would have been a survival
                advantage before a stable food intake could be relied on, but in current times it can
                result in obesity, type 2 diabetes, and other health problems found with the metabolic
                syndrome.
                     The Pima Indians of Arizona are the classic example of why it is believed
                genetic predisposition and environmental conditions allow for the development of
                the metabolic syndrome. The Pima Indians in the Southwest United States have the
                highest reported occurrence of obesity and non–insulin-dependent diabetes
                mellitus in the world. This situation developed only about 100 years ago with the
                abrupt changes in lifestyle accompanying the rerouting of the Gila River to provide
                irrigation waters for California. As these Pimas could no longer grow their own
                foods and their activity levels went down, their lifestyles and dietary intake
                drastically changed. This has resulted in an epidemic of obesity and diabetes.
                However, this is in contrast to the low rates of obesity and diabetes among the
                Pimas living in Mexico (Valencia et al., 2005). The lower rate of diabetes among the
                Mexican Pimas is attributed to their higher physical activity levels and maintenance
                of a more traditional diet that emphasizes high-fiber foods and low reliance on
                meat and processed foods.
                     There is some evidence that the risk of the metabolic syndrome may be set in
                utero. Large babies who were exposed prenatally to their mother’s gestational
                diabetes or obesity have been noted to be at increased risk for developing the
                metabolic syndrome in later childhood (Boney et al., 2005). Excess kilocalorie intake
                during pregnancy is suspected to predispose the infant to later development of the
                metabolic syndrome (Armitage et al., 2005). Therefore counseling women during
                pregnancy to avoid excess weight gain and having screening for gestational
                diabetes with appropriate management may help reduce the rate of diabetes for
                future generations. See Chapter 11 for pregnancy guidelines.

What Population Groups Are Known to Have High Levels of Insulin Resistance?
              Genetically, certain population groups are known to have high rates of insulin
              resistance. Native Americans, in general, have a high prevalence of type 2 diabetes.
              South Pacific Islanders are also at high risk for insulin resistance. Other known
              groups with high rates of the insulin resistance syndrome include persons with
              Spanish (i.e., Hispanic and Latino) and South Asian heritage. In Mexico there is an
              epidemic of obesity, type 2 diabetes, and cardiovascular disease linked with the
              metabolic syndrome (Sanchez-Castillo et al., 2004). Asian populations may become
              more susceptible to the metabolic syndrome as a Western diet and lifestyle are
              adopted. WHO Expert Consultation has advised a BMI (see Chapter 6) of 22 to 25
              among the Asian population to reduce the adverse health outcomes of the
              metabolic syndrome (Rakugi and Ogihara, 2005). Persons with African heritage
              have a high rate of insulin resistance. Among African-American children a higher
              rate of type 2 diabetes, along with hyperinsulinemia, obesity, acanthosis nigricans
              (a skin condition with dark patches related to diabetes—see Figure 5-1 and Chapter
              8), and family history of diabetes has been noted as compared to their Caucasian
    156   SECTION 2    Chronic and Acute Illness




                                                                                                                   B




                                                      Figure 5-1 Acanthosis nigricans causes dark patches to
A
                                                      occur on the skin, often in the underarm area as
                                                      shown, or on the neck; cutaneous papillomas or “skin
                                                      tags” are also commonly found with insulin resistance
                                                      and diabetes.




               counterparts (Arslanian, 2002). Cutaneous papillomas or skin tags are also found
               with insulin resistance and type 2 diabetes (Figure 5-1).
                    There is a general trend for higher rates of insulin resistance among persons
               with heritage from regions nearer the equator, such as the Pacific Islanders. There
               are exceptions to this because insulin resistance is known to occur in all ethnic
               groups. Finland is one northern country with a relatively high rate of diabetes
               (Ilanne-Parikka et al., 2004). Among an Irish population the prevalence of glucose
               intolerance and type 2 diabetes was noted to be almost 15% (Smith et al., 2003). In a
               study of French families, the metabolic syndrome was found to increase with age
               (Maumus et al., 2005).

               Native Hawaiians have been advocating a return to more traditional diets and lifestyles. This
               is a result, in part, of the recognition of high numbers of chronic illnesses including diabetes,
               obesity, hypertension, heart disease, and cancer. Family is very important to native
               Hawaiians, along with respect for one’s ancestors. As part of this, traditional foods are
               viewed with respect. Arguments or negative comments about traditional foods, such as poi,
               are frowned on as being disrespectful to ancestors. Attempts to improve the health of native
                                 Insulin Resistance and the Metabolic Syndrome    CHAPTER 5            157


                Hawaiians is best done from a family perspective, rather than an individual one, and should
                include exercise, cooking, and eating together. ■

How Can the Metabolic Syndrome Be Prevented or Managed?
             Genetically, a family history of type 2 diabetes and the other health conditions
             found with the metabolic syndrome increase one’s own risk of developing
             diabetes. However, even though there may be an increased genetic risk, there are
             ways to minimize this. Physically active, nonsmoking persons of normal weight
             with moderately low intake of carbohydrate and alcohol have been found to have a
             lower risk of developing the metabolic syndrome (Zhu et al., 2004). Lifestyle
             changes have shown prevention of diabetes by over 40% among persons with
             prediabetes (Orchard et al., 2005). One study found that individuals who increased
             their level of physical activity were about 65% less likely to develop diabetes
             (Laaksonen et al., 2005). The nutritional factors to lower risk for developing the
             health conditions found with insulin resistance are summarized as follows:
               ■ Aim for meals with lower glycemic index and glycemic load (McKeown et al.,

                 2004).
               ■ Include at least 20 g of dietary fiber daily, with emphasis on soluble fiber (Davy

                 and Melby, 2003).
               ■ Aim for six meals daily to lower insulin release (Farshchi et al., 2005).

               ■ Reduce intake of sweetened beverages to control kilocalories (Schulze et al.,

                 2004; Yoo et al., 2004).
               ■ Avoid excess intake of high-fructose corn syrup as found in commercially

                 sweetened products to control triglyceride levels (Basciano et al., 2005).
               ■ Include magnesium-rich foods to reduce inflammation (McCarty, 2005).

               ■ Increase foods rich in vitamin C and beta carotene to lower CRP levels

                 (Fredrikson et al., 2004).
               ■ Include folate and vitamin B12 to improve insulin resistance (Setola et al., 2004).

               ■ Emphasize nuts and olive oil versus a low-fat diet, but within a controlled

                 kilocalorie intake (Esposito et al., 2004).
               ■ Limit intake of saturated fats and trans fats (Musso et al., 2005; Schulze and Hu,

                 2005).
               ■ Increase the amount of omega-3 fats to lower blood pressure, serum insulin,

                 and triglycerides (Aguilera et al., 2004; Hulbert et al., 2005).
               ■ Aim for weight loss as needed, physical activity, and a diet moderate in fat and

                 carbohydrate, with emphasis on monounsaturated fats and omega-3 fatty acids
                 to control triglyceride and blood glucose levels (Carson, 2003).
               ■ For those who already drink, include moderate amounts (Carnethon et al.,

                 2004; Djousse et al., 2004).

What Is the Role of Magnesium in Controlling Insulin Resistance?
               Insulin resistance may be promoted by magnesium deficiency because of adverse
               changes to metabolic enzymes (Higashiura and Shimamoto, 2005). As reviewed in
               Chapter 3, magnesium is related to the production of 300 metabolic enzymes.
                    Hyperinsulinemia, as generally found with insulin resistance, promotes excess
               loss of magnesium. Severe magnesium deficiency has been shown to cause a
               clinical inflammatory syndrome that can be controlled with increasing intake of
158    SECTION 2      Chronic and Acute Illness


               magnesium. Magnesium deficiency contributes to conditions found with the
               metabolic syndrome, including hyperlipidemia, and hypertension related to
               cardiovascular disease and cancer (Rayssiguier and Mazur, 2005). Magnesium is
               found in dark green, leafy vegetables, as it is part of the chlorophyll molecule, and
               is also found in high amounts in legumes, the germ portion of whole grains, nuts,
               milk and milk products, and fish.


               FALLACY: A person with a strong family history of diabetes is doomed to develop this
               condition.
               FACT: Studies show that groups at risk of developing diabetes can help prevent or delay the
               development of type 2 diabetes if there is regular physical activity, maintenance of a healthy
               weight, and emphasis on foods high in fiber and low in saturated fat. ■


WHAT IS THE ROLE OF HYPERINSULINEMIA IN THE INSULIN
RESISTANCE SYNDROME?
          A person with a genetic predisposition to insulin resistance tends to have an altered
          insulin response. With insulin resistance there is often a delayed production of
          meal-related insulin. This can result in a transient state of hyperglycemia (high
          levels of blood glucose). When the body does respond to the hyperglycemia, it is
          often with excess insulin production over a prolonged period. Persons with insulin
          resistance have been noted to produce up to 10 times the amount of insulin to
          control blood glucose levels as compared with other insulin-sensitive individuals.
          This hyperinsulinemia can result in symptoms of hypoglycemia (low levels of
          blood glucose; see Chapter 8) if meals are delayed.
               The symptoms of reactive hypoglycemia are common among persons with
          insulin resistance, but medically the condition is rarely diagnosed. The blood
          glucose criteria for diagnosis of reactive hypoglycemia are more stringent than for
          persons with diabetes on medication. Physicians generally will not make the
          diagnosis unless blood glucose levels are below 50 mg/dL. Symptoms of hypo-
          glycemia, however, may occur years before the onset of diabetes and are likely
          because of hyperinsulinemia and excess release of counterregulatory hormones (see
          Chapter 4).
               Counterregulatory hormones correct hypoglycemia by causing the liver to
          release its stored sugar, called glycogen. The symptoms that occur because of these
          hormones, however, can be unpleasant. Altered glucagon (a counterregulatory
          hormone that is the first one produced in response to low levels of blood glucose)
          secretion has been noted in reactive hypoglycemia. Glucagon in excess leads to
          feelings of nausea. Glucagon release is inhibited with hyperinsulinemia. It may be
          for this reason that persons with insulin resistance experience the symptoms of
          hypoglycemia as the body needs to release other counterregulatory hormones such
          as adrenalin (epinephrine). Adrenalin causes an increased heart rate and physical
          tremors, which is an unpleasant and potentially frightening experience if the
          person has not associated it with the need to eat a carbohydrate source.
               The symptoms of hypoglycemia do affect the quality of life. However, most
          persons with hypoglycemia symptoms are not in an immediate health emergency.
                Insulin Resistance and the Metabolic Syndrome   CHAPTER 5           159


Severe hypoglycemia requiring medical assistance is usually limited to persons taking
insulin or insulin-stimulating medications such as the sulfonylurea medications (see
Chapter 8).
     Hyperinsulinemia is found with central obesity. It is still, however, a bit of a
chicken-and-egg question. Which came first? Hyperinsulinemia and central obesity
are known to worsen insulin resistance. However, it may be that the genetic
predisposition to insulin resistance is what first sets up excess production of insulin
in relation to carbohydrate intake. Some health care professionals suggest that
hyperinsulinemia encourages the gain of abdominal weight in the first place. This is
the basis of the low-carbohydrate diets (see Chapter 6).
     Within a group of obese children, 40% were found to have hyperinsulinemia,
and over 10% had impaired glucose tolerance as based on an OGTT. About one
third of obese children had dyslipidemia (disordered fats in the blood; generally
referring to elevated triglycerides and low levels of HDL-C) and hypertension.
The metabolic syndrome was found in 30% of children under 12 years of age
(Viner et al., 2005).
     With regard to dyslipidemia (see Chapter 7), it has been clearly shown that the
enzyme lipoprotein lipase (an enzyme that helps the breakdown of triglycerides) is
altered in the presence of hyperinsulinemia. This results in reduced breakdown of
triglycerides, leading to high serum triglyceride levels. Thus elevated triglyceride
levels in the blood are generally associated with hyperinsulinemia, especially if
the person also has central obesity. This occurs even in childhood, with triglyceride
levels correlating with insulin levels in children (Reinehr et al., 2005). Reduction in
hyperinsulinemia generally improves dyslipidemia. One study showed that an
intake of 250 mg EPA/DHA omega-3 fats for only 6 weeks significantly decreased
both fasting and postprandial triglyceride levels (Brady et al., 2004).
     Hypertension is now a well-recognized aspect of insulin resistance and the
metabolic syndrome. There are still unanswered questions regarding the specific
mechanism related to hypertension and the underlying cause of insulin resistance.
The role of hyperinsulinemia is being suggested as the link, as a result of altered
vasodilation. Therefore advice to follow a low-glycemic index diet may contribute
to management of hypertension (Kopp, 2005). A person with central obesity and
hypertension likely has insulin resistance (Figure 5-2).
     Hyperinsulinemia is now believed to be related to early heart disease, because
of the incidence of heart disease occurring before the diagnosis of diabetes. It is well
known that diabetes is associated with increased risk of atherosclerosis (see
Chapter 7).
     Type 2 diabetes is described as a relative insufficiency of insulin production.
Hyperinsulinemia is usually present with type 2 diabetes; there just is not enough
insulin for the demand or to overcome severe insulin resistance at the cellular level.
However, hyperinsulinemia can worsen insulin resistance, making it more difficult
for the body to regulate blood glucose levels.
     Certain cancers are found with the metabolic syndrome. Middle-aged men
with the metabolic syndrome were found to be more likely to develop prostate cancer
(Laukkanen et al., 2004). Excess weight in women is found with hyperinsulinemia,
low HDL-C, increased levels of estrogen, and breast cancer (Furberg et al., 2005). See
Chapter 10 for more on the role of hyperinsulinemia in the development of cancer.
160     SECTION 2     Chronic and Acute Illness




                       Figure 5-2 Hypertension is commonly found with excess abdominal weight.



WHAT IS GOUT, AND WHAT ARE ITS RISK FACTORS AND
MANAGEMENT?
          Gout is the medical condition related to high levels of uric acid. The buildup of uric
          acid causes crystals to form. Uric acid crystals can cause severe pain in various
          joints in which the crystals tend to collect. Commonly the big toe is involved, but
          other joints may be affected. Damage to the kidneys is known to occur with uric
          acid deposition in this organ. The incidence of gout is increasing, especially with
          older adults, with men having this condition three to four times more frequently
          than women (Wallace et al., 2004).
              A high level of uric acid is associated with insulin resistance (Cohn et al., 2005).
          Historically, higher uric acid levels are believed to have been helpful to maintain
          adequate blood pressure levels when intake of sodium was too low. As the
          Westernized diet has become increasingly prevalent, there has been an increase in
          both hypertension and gout (Johnson et al., 2005).
              Traditional medical nutritional therapy for gout has been aimed at lowering
          intake of purines as found in legumes and other protein-based foods. Generally the
          use of medications such as allopurinol and colchicines is the primary intervention.
          With the newer recognition of gout as part of the metabolic syndrome, the goals of
          medical nutrition therapy (MNT) for managing insulin resistance may be more
          effective. Moderate amounts of legumes may be tolerated and help meet the goal
                                Insulin Resistance and the Metabolic Syndrome     CHAPTER 5            161


               for increased intake of fiber and magnesium. Slow weight loss, avoidance of excess
               alcohol, and good fluid intake can be of help. Data from the Third National Health
               and Nutrition Examination Survey were analyzed and showed that total protein
               intake was not related to the serum uric acid levels. However, meat and seafood
               intake appears to increase levels, whereas milk and yogurt consumption was
               related to lower levels (Choi et al., 2005).

WHAT IS THE POLYCYSTIC OVARY SYNDROME, AND WHAT IS ITS
MANAGEMENT?
          PCOS can be related to hyperinsulinemia. There are different causes of PCOS.
          When PCOS is found in conjunction with central obesity and other risk factors for
          insulin resistance, hyperinsulinemia is the most likely cause. In the presence of
          excess levels of insulin, male-type hormones, called androgens, may be formed.
          This results in the masculinization of some women, leading to hirsutism (excessive
          male-type body hair), ovarian cysts, and irregular menstrual cycles.
               In one outpatient adolescent clinic 5% were diagnosed with PCOS including
          excess androgen levels, hirsutism, acanthosis nigricans (a skin condition; see Figure
          5-1), and obesity (Omar et al., 2004). Of women with unwanted hair growth, it was
          found that about half had excess androgen levels and PCOS. Women with
          hirsutism are advised to have ovulatory function assessed even if the menstrual
          cycle is normal (Souter et al., 2004).
               Women with PCOS are at high risk for impaired glucose tolerance and type 2
          diabetes. This is especially true of minority women. A 2-hour OGTT for screening
          women with PCOS at high risk for diabetes, rather than fasting glucose levels
          alone, can better identify health risk. An increased potential for endometrial
          hyperplasia (thickening of the endometrial layer of the uterus) and cancer is
          associated with anovulation (Richardson, 2003). This underscores the need for
          prompt identification and treatment of PCOS.
               Women with PCOS generally benefit with the same goals of MNT to control
          insulin resistance as described earlier in the chapter. One area of concern, however,
          is normalizing food intake. A higher prevalence of bulimia nervosa (see Chapter 12)
          and greater cravings for sweets has been noted with PCOS. This may be related to
          impaired release of the satiety factor, cholecystokinin (Hirschberg et al., 2004). As
          discussed previously, an increased intake of unsaturated fats is a positive goal in
          the management of the metabolic syndrome and can help increase cholecystokinin
          levels. Individuals who follow very-low–kilocalorie diets may also have episodes
          of binge eating and crave sweets. Small, frequent meals with low glycemic index
          can be very helpful in controlling PCOS.



               FALLACY: Children instinctively know how to make food choices to stay healthy.
               FACT: Children need the guidance of adults in selecting foods. The insulin resistance
               syndrome includes many chronic diseases, such as obesity, heart disease, and high blood
               pressure, that can start in childhood as a result of poor food choices. Using the MyPyramid
               to teach children to eat more high-fiber plant foods, such as vegetables, fruits, and legumes
               (beans), is appropriate. ■
162    SECTION 2      Chronic and Acute Illness


WHAT ARE MEDICATION CONCERNS IN MANAGING INSULIN
RESISTANCE?
         There are multiple factors that can influence risk for the metabolic syndrome. It has
         been noted that persons with schizophrenia who take the medications clozapine or
         olanzapine are at increased risk for insulin resistance and should be monitored
         (Henderson et al., 2005). Medications that are known to cause weight gain, such as
         some antipsychotics, need to be used cautiously in persons at risk for the metabolic
         syndrome.
             Medications that serve a positive role include insulin sensitizers such as
         metformin, sold under the brand name of Glucophage. For PCOS, antiandrogen
         medications in combination with estrogen can restore regular menstrual cycles and
         reduce acne and hirsutism found with this syndrome (Homburg, 2005).
             Other medications exist to control insulin resistance, and more are expected to
         be developed. The insulin-sensitizing medication rosiglitazone was studied with
         severely insulin-resistant obese women who had PCOS. It was found that this
         medication improved insulin resistance and glucose tolerance, decreased ovarian
         androgen production, normalized insulin levels, and helped restore spontaneous
         ovulation (Sepilian and Nagamani, 2005).

WHAT IS THE ROLE OF THE NURSE OR OTHER HEALTH PROFESSIONAL
IN THE PREVENTION AND MANAGEMENT OF THE INSULIN RESISTANCE
SYNDROME?
          The nurse or other health professional should be aware of the common occurrence
          and risk factors of the metabolic syndrome. The nurse can help identify at-risk
          individuals through review of family history and health correlates of insulin
          resistance. Prompt identification can help to prevent early heart disease and diabetes.
               The nurse or other health care professional can provide lifestyle guidance. This
          might entail encouraging low-sugar beverages, such as seltzer water or iced tea, or
          recommending that a pitcher of water with lemon slices be kept in the refrigerator
          to increase its appeal. To encourage intake of vegetables and fiber, use of
          mayonnaise-based dressings or using olive oil to sauté vegetables can be suggested.
          To lower glycemic index of meals, it can be advised to “Eat fruit; don’t drink it.” It
          should be clarified, however, that 4 oz of juice (15 g of carbohydrates) is generally
          well tolerated; advice might be to drink juice the “European way” (mixed with
          seltzer water). Reviewing food labels for fiber content is a practical strategy that can
          empower individuals to reduce their risk of the metabolic syndrome. Increased
          physical activity should be promoted; walking, dancing, or other forms of exercise
          can be encouraged. For individuals with mobility issues, even chair exercises can be
          of help. Adolescents might be encouraged to play basketball or skip rope to help
          stem the epidemic of obesity and diabetes in our youth.




               1.   If you are working with an individual who has central obesity and hypertension,
                    is this individual at risk of diabetes? What laboratory values can help determine
                    this risk?
                  Insulin Resistance and the Metabolic Syndrome   CHAPTER 5        163


2. Ask students to raise their hands if they have experienced symptoms of
   hypoglycemia, such as feeling weak, shaky, or irritable, that are resolved with
   food.
3. Have students volunteer, as desired, their family history of insulin resistance
   correlates. Estimate the percentage of students in class who are at risk for the
   metabolic syndrome.
4. Assess the following menu for the questions that follow:
    BREAKFAST                  LUNCH                        DINNER

    Banana                     Hot dog on roll              Cheeseburger
    Corn flakes                Mustard and relish           French fries
    Whole milk                 Chocolate chip cookies       Coleslaw
    Sugar                      Coke                         Milkshake
    Toast, butter, and jelly

    Judge these meals based on a typical adult’s needs according to the new MyPyramid.
    Identify the foods or beverages high in sugar and saturated fat.
    What suggestions would you make to change this menu to lower the risk of developing
      the metabolic syndrome?




Royce had been on a very-low–fat diet since his open heart surgery 2 years before.
He was now being advised by the nurse practitioner that he had prediabetes and
should include more fat and fiber with moderate amounts of carbohydrate. It was a
bit confusing, but it seemed to make sense. He had said he would be delighted to
put real olive oil on his salads, instead of the fat-free dressings he had been using.
He certainly loved nuts and was willing to try natural peanut butter on his toast. He
had been getting hungry right after breakfast when he just used jam. And being
advised to eat sardines was particularly easy; that took him back to his childhood
when he sat on his grandfather Sean’s lap while the two of them ate sardines
together. The advice to eat beans wasn’t new to him, either. He’d been eating his
grandmother’s baked beans for years, and even now his wife’s cooking included
beans. He and Nellie loved pinto beans and collards, and her mother had taught
them to like adzuki beans, along with her specialty of succotash. Thinking about all
this food made him hungry. He didn’t like to cook, so he got out the can of kidney
beans and prepared to add the vinegar and pinch of sugar. He loved eating cold
beans from the can. Then he was going for a walk, he told himself. He was
motivated, since he’d learned he had prediabetes. And he was very thankful for being
able to walk, since his car accident had put him in the hospital a number of years
back. Yes, life was okay.

Critical Thinking Applications
1. What laboratory value(s) must Royce have to diagnose prediabetes?
2. What is known about the prevention of diabetes? How does this relate to the
     advice given by the nurse practitioner?
3. What factors in Royce’s diet help meet the nutritional guidelines to manage the
     metabolic syndrome and help prevent diabetes?
164   SECTION 2      Chronic and Acute Illness


             4. Why would the nurse practitioner advise eating more monounsaturated fats
                and fewer carbohydrates?
             5. What is in sardines, and how might they help Royce?
             6. If Royce needs 2000 kcal, how many grams of carbohydrate would be advised?
                How many grams of fat?
             7. In doing a diet history, what foods and nutrients are important to assess?

REFERENCES
             Aguilera AA, Diaz GH, Barcelata ML, Guerrero OA, Ros RM: Effects of fish oil on hypertension,
                 plasma lipids, and tumor necrosis factor-alpha in rats with sucrose-induced metabolic
                 syndrome, J Nutr Biochem 15(6):350-357, 2004.
             Armitage JA, Taylor PD, Poston L: Experimental models of developmental programming:
                 consequences of exposure to an energy rich diet during development, J Physiol
                 565(pt1):3-8, 2005.
             Arslanian SA: Metabolic differences between Caucasian and African-American children and
                 the relationship to type 2 diabetes mellitus, J Pediatr Endocrinol Metab 15(suppl 1):509-
                 517, 2002.
             Basciano H, Federico L, Adeli K: Fructose, insulin resistance, and metabolic dyslipidemia,
                 Nutr Metab (Lond) 2(1):5, 2005.
             Boney CM, Verma A, Tucker R, Vohr BR: Metabolic syndrome in childhood: association with
                 birth weight, maternal obesity, and gestational diabetes mellitus, Pediatrics 115(3):e290-e296,
                 2005.
             Brady LM, Lovegrove SS, Lesauvage SV, Gower BA, Minihane AM, Williams CM, Lovegrove
                 JA: Increased n-6 polyunsaturated fatty acids do not attenuate the effects of long-chain
                 n-3 polyunsaturated fatty acids on insulin sensitivity or triacylglycerol reduction in
                 Indian Asians, Am J Clin Nutr 79(6):983-991, 2004.
             Brea A, Mosquera D, Martin E, Arizti A, Cordero JL, Ros E: Nonalcoholic fatty liver disease is
                 associated with carotid atherosclerosis: a case-control study, Arterioscler Thromb Vasc Biol
                 25(5):1045-1050, 2005.
             Carnethon MR, Loria CM, Hill JO, Sidney S, Savage PJ, Liu K: Risk factors for the metabolic
                 syndrome: the Coronary Artery Risk Development in Young Adults (CARDIA) study,
                 1985-2001, Diabetes Care 27(11):2707-2715, 2004.
             Carson JA: Nutrition therapy for dyslipidemia, Curr Diab Rep 3(5):397-403, 2003.
             Choi HK, Liu S, Curhan G: Intake of purine-rich foods, protein, and dairy products and
                 relationship to serum levels of uric acid: the Third National Health and Nutrition
                 Examination Survey, Arthritis Rheum 52(1):283-289, 2005.
             Choi KM, Lee J, Kim YH, Kim KB, Kim DL, Kim SG, Shin DH, Kim NH, Park IB, Choi DS,
                 Baik SH; Koreans-Southwest Seoul (SWS) Study: Relation between insulin resistance
                 and hematological parameters in elderly Koreans, Diabetes Res Clin Pract 60(3):205-212,
                 2003.
             Cohn GS, Kittleson MM, Blumenthal RS: Toward an improved diagnosis of the metabolic
                 syndrome: other clues to the presence of insulin resistance, Am J Hypertens 18(8):1099-1103,
                 2005.
             Davy BM, Melby CL: The effect of fiber-rich carbohydrates on features of Syndrome X, J Am
                 Diet Assoc 103(1):86-96, 2003.
             Dessein PH, Joffe BI, Stanwix AE: Subclinical hypothyroidism is associated with insulin
                 resistance in rheumatoid arthritis, Thyroid 14(6):443-446, 2004.
             Djousse L, Arnett DK, Eckfeldt JH, Province MA, Singer MR, Ellison RC: Alcohol
                 consumption and metabolic syndrome: does the type of beverage matter? Obes Res
                 12(9):1375-1385, 2004.
             Esposito K, Marfella R, Ciotola M, Di Palo C, Giugliano F, Giugliano G, D’Armiento M,
                 D’Andrea F, Giugliano D: Effect of a Mediterranean-style diet on endothelial dysfunction
                 and markers of vascular inflammation in the metabolic syndrome: a randomized trial,
                 JAMA 292(12):1440-1446, 2004.
                 Insulin Resistance and the Metabolic Syndrome       CHAPTER 5            165


Farshchi HR, Taylor MA, Macdonald IA: Beneficial metabolic effects of regular meal
     frequency on dietary thermogenesis, insulin sensitivity, and fasting lipid profiles in
     healthy obese women, Am J Clin Nutr 81(1):16-24, 2005.
Ford ES, Ajani UA, Mokdad AH: The metabolic syndrome and concentrations of C-reactive
     protein among U.S. youth, Diabetes Care 28(4):878-881, 2005.
Fredrikson GN, Hedblad B, Nilsson JA, Alm R, Berglund G, Nilsson J: Association between
     diet, lifestyle, metabolic cardiovascular risk factors, and plasma C-reactive protein
     levels, Metabolism 53(11):1436-1442, 2004.
Furberg AS, Jasienska G, Bjurstam N, Torjesen PA, Emaus A, Lipson SF, Ellison PT, Thune I:
     Metabolic and hormonal profiles: HDL cholesterol as a plausible biomarker of breast
     cancer risk. The Norwegian EBBA Study, Cancer Epidemiol Biomarkers Prev 14(1):33-40,
     2005.
Henderson DC, Cagliero E, Copeland PM, Borba CP, Evins E, Hayden D, Weber MT,
     Anderson EJ, Allison DB, Daley TB, Schoenfeld D, Goff DC: Glucose metabolism in
     patients with schizophrenia treated with atypical antipsychotic agents: a frequently
     sampled intravenous glucose tolerance test and minimal model analysis, Arch Gen
     Psychiatry 62(1):19-28, 2005.
Higashiura K, Shimamoto K: Magnesium and insulin resistance, Clin Calcium 15(2):251-254,
     2005.
Hirschberg AL, Naessen S, Stridsberg M, Bystrom B, Holtet J: Impaired cholecystokinin
     secretion and disturbed appetite regulation in women with polycystic ovary syndrome,
     Gynecol Endocrinol 19(2):79-87, 2004.
Homburg R: Polycystic ovary syndrome in adolescence. New insights in pathophysiology
     and treatment, Endocr Dev 8:137-149, 2005.
Hulbert AJ, Turner N, Storlien LH, Else PL: Dietary fats and membrane function: implications
     for metabolism and disease, Biol Rev Camb Philos Soc 80(1):155-169, 2005.
Ilanne-Parikka P, Eriksson JG, Lindstrom J, Hamalainen H, Keinanen-Kiukaanniemi S,
     Laakso M, Louheranta A, Mannelin M, Rastas M, Salminen V, Aunola S, Sundvall J, Valle
     T, Lahtela J, Uusitupa M, Tuomilehto J; Finnish Diabetes Prevention Study Group:
     Prevalence of the metabolic syndrome and its components: findings from a Finnish
     general population sample and the Diabetes Prevention Study cohort, Diabetes Care
     27(9):2135-2140, 2004.
Jehn M, Clark JM, Guallar E: Serum ferritin and risk of the metabolic syndrome in U.S.
     adults, Diabetes Care 27(10):2422-2428, 2004.
Jiang R, Ma J, Ascherio A, Stampfer MJ, Willett WC, Hu FB: Dietary iron intake and blood
     donations in relation to risk of type 2 diabetes in men: a prospective cohort study, Am J
     Clin Nutr 79(1):70-75, 2004.
Johnson RJ, Titte S, Cade JR, Rideout BA, Oliver WJ: Uric acid, evolution and primitive
     cultures, Semin Nephrol 25(1):3-8, 2005.
Kelly AS, Wetzsteon RJ, Kaiser DR, Steinberger J, Bank AJ, Dengel DR: Inflammation, insulin,
     and endothelial function in overweight children and adolescents: the role of exercise,
     J Pediatr 145(6):731-736, 2004.
Kelly CC, Lyall H, Petrie JR, Gould GW, Connell JM, Sattar N: Low-grade chronic
     inflammation in women with polycystic ovarian syndrome, J Clin Endocrinol Metab
     86(6):2453-2455, 2001.
Kopp W: Pathogenesis and etiology of essential hypertension: role of dietary carbohydrate,
     Med Hypotheses 64(4):782-787, 2005.
Kuriki K, Tokudome S, Tajima K: Association between type II diabetes and colon cancer among
     Japanese with reference to changes in food intake, Asian Pac J Cancer Prev 5(1):28-35,
     2004.
Laaksonen DE, Lindstrom J, Lakka TA, Eriksson JG, Niskanen L, Wikstrom K, Aunola S,
     Keinanen-Kiukaanniemi S, Laakso M, Valle TT, Ilanne-Parikka P, Louheranta A,
     Hamalainen H, Rastas M, Salminen V, Cepaitis Z, Hakumaki M, Kaikkonen H,
     Harkonen P, Sundvall J, Tuomilehto J, Uusitupa M; Finnish diabetes prevention study:
     Physical activity in the prevention of type 2 diabetes: the Finnish diabetes prevention
     study, Diabetes 54(1):158-165, 2005.
166   SECTION 2   Chronic and Acute Illness


           Laukkanen JA, Laaksonen DE, Niskanen L, Pukkala E, Hakkarainen A, Salonen JT: Metabolic
                syndrome and the risk of prostate cancer in Finnish men: a population-based study,
                Cancer Epidemiol Biomarkers Prev 13(10):1646-1650, 2004.
           Maumus S, Marie B, Siest G, Visvikis-Siest S: A prospective study on the prevalence of
                metabolic syndrome among healthy French families: two cardiovascular risk factors
                (HDL cholesterol and tumor necrosis factor-α) are revealed in the offspring of parents
                with metabolic syndrome, Diabetes Care 28(3):675-682, 2005.
           McCarty MF: Magnesium may mediate the favorable impact of whole grains on insulin
                sensitivity by acting as a mild calcium antagonist, Med Hypotheses 64(3):619-627,
                2005.
           McKeown NM, Meigs JB, Liu S, Saltzman E, Wilson PW, Jacques PF: Carbohydrate nutrition,
                insulin resistance, and the prevalence of the metabolic syndrome in the Framingham
                Offspring Cohort, Diabetes Care 27(2):538-546, 2004.
           Miller JL, Silverstein JH: The management of type 2 diabetes mellitus in children and
                adolescents, J Pediatr Endocrinol Metab 18(2):111-123, 2005.
           Musso G, Gambino R, De Michieli F, Cassader M, Rizzetto M, Durazzo M, Faga E, Silli B,
                Pagano G: Dietary habits and their relations to insulin resistance and postprandial
                lipemia in nonalcoholic steatohepatitis, Hepatology 37(4):909-916, 2003.
           Omar HA, Logsdon S, Richards J: Clinical profiles, occurrence, and management of
                adolescent patients with HAIR-AN syndrome, ScientificWorldJournal 4:507-511, 2004.
           Orchard TJ, Temprosa M, Goldberg R, Haffner S, Ratner R, Marcovina S, Fowler S; Diabetes
                Prevention Program Research Group: The effect of metformin and intensive lifestyle
                intervention on the metabolic syndrome: the Diabetes Prevention Program randomized
                trial, Ann Intern Med 142(8):611-619, 2005.
           Piperno A, Vergani A, Salvioni A, Trombini P, Vigano M, Riva A, Zoppo A, Boari G, Mancia
                G: Effects of venesections and restricted diet in patients with the insulin-resistance
                hepatic iron overload syndrome, Liver Int 24(5):471-476, 2004.
           Pontiroli AE: Type 2 diabetes mellitus is becoming the most common type of diabetes in
                school children, Acta Diabetol 41(3):85-90, 2004.
           Rakugi H, Ogihara T: The metabolic syndrome in the Asian population, Curr Hypertens Rep
                7(2):103-109, 2005.
           Rayssiguier Y, Mazur A: Magnesium and inflammation: lessons from animal models, Clin
                Calcium 245-248, 2005.
           Reinehr T, Kiess W, Andler W: Insulin sensitivity indices of glucose and free fatty acid
                metabolism in obese children and adolescents in relation to serum lipids, Metabolism
                54(3):397-402, 2005.
           Richardson MR: Current perspectives in polycystic ovary syndrome, Am Fam Physician
                68(4):697-704, 2003.
           Sanchez-Castillo CP, Pichardo-Ontiveros E, Lopez-RP: The epidemiology of obesity, Gac Med
                Mex 140(suppl 2):S3-S20, 2004.
           Schulze M, Hu FB: Primary prevention of diabetes: what can be done and how much can be
                prevented? Annu Rev Public Health 26:445-467, 2005.
           Schulze MB, Manson JE, Ludwig DS, Colditz GA, Stampfer MJ, Willett WC, Hu FB: Sugar-
                sweetened beverages, weight gain, and incidence of type 2 diabetes in young and
                middle-aged women, JAMA 292(8):927-934, 2004.
           Sepilian V, Nagamani M: Effects of rosiglitazone in obese women with polycystic ovary
                syndrome and severe insulin resistance, J Clin Endocrinol Metab 90(1):60-65, 2005.
           Setola E, Monti LD, Galluccio E, Palloshi A, Fragasso G, Paroni R, Magni F, Sandoli EP,
                Lucotti P, Costa S, Fermo I, Galli-Kienle M, Origgi A, Margonato A, Piatti P: Insulin
                resistance and endothelial function are improved after folate and vitamin B12 therapy in
                patients with metabolic syndrome: relationship between homocysteine levels and
                hyperinsulinemia, Eur J Endocrinol 151(4):483-489.
           Silfen ME, Manibo AM, McMahon DJ, Levine LS, Murphy AR, Oberfield SE: Comparison of
                simple measures of insulin sensitivity in young girls with premature adrenarche: the
                fasting glucose-to-insulin ratio may be a simple and useful measure, J Clin Endocrinol
                Metab 86(6):2863-2868, 2001.
                 Insulin Resistance and the Metabolic Syndrome     CHAPTER 5            167


Smith SM, Holohan J, McAuliffe A, Firth RG: Irish diabetes detection programme in general
    practice, Diabet Med 20(9):717-722, 2003.
Souter I, Sanchez LA, Perez M, Bartolucci AA, Azziz R: The prevalence of androgen excess
    among patients with minimal unwanted hair growth, Am J Obstet Gynecol 191(6):1914-1920,
    2004.
St-Onge MP, Janssen I, Heymsfield SB: Metabolic syndrome in normal-weight Americans:
    new definition of the metabolically obese, normal-weight individual, Diabetes Care
    27(9):2222-2228, 2004.
Valencia ME, Weil EJ, Nelson RG, Esparza J, Schulz LO, Ravussin E, Bennett PH: Impact of
    lifestyle on prevalence of kidney disease in Pima Indians in Mexico and the United
    States, Kidney Int Suppl 97:S141-S144, 2005.
Viner RM, Segal TY, Lichtarowicz-Krynska E, Hindmarsh P: Prevalence of the insulin
    resistance syndrome in obesity, Arch Dis Child 90(1):10-14, 2005.
Wallace KL, Riedel AA, Joseph-Ridge N, Wortmann R: Increasing prevalence of gout and
    hyperuricemia over 10 years among older adults in a managed care population, J Rheumatol
    31(8):1582-1587, 2004.
Yoo S, Nicklas T, Baranowski T, Zakeri IF, Yang SJ, Srinivasan SR, Berenson GS: Comparison
    of dietary intakes associated with metabolic syndrome risk factors in young adults: the
    Bogalusa Heart Study, Am J Clin Nutr 80(4):841-848, 2004.
Zhu S, St-Onge MP, Heshka S, Heymsfield SB: Lifestyle behaviors associated with lower risk
    of having the metabolic syndrome, Metabolism 53(11):1503-1511, 2004.

				
DOCUMENT INFO
Shared By:
Categories:
Tags:
Stats:
views:12
posted:11/13/2011
language:English
pages:20