IBDanswers

By Laurel Garwin, NC
June 21, 2001

This paper is for educational purposes only. It is not meant to diagnose, treat, or cure ulcerative colitis. This paper is not a substitute for medical care. For medical diagnosis or to treat the disease, please consult a medical physician or other qualified health practitioner.

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This article is only one of a 3 part series. Be sure to read all 3:

• Ulcerative Colitis and Nutrition (this document)
• Appendix A - Clinical Definition of Leaky Gut Syndrome
• Appendix B - The Specific Carbohydrate Diet

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ABSTRACT

Ulcerative colitis is an inflammatory disease of the large intestine. The etiology of the disease is unknown, however theories suggest genetics, microbial pathogens, dietary causes or immune system malfunction as to its cause. The disease may present with symptoms such as diarrhea with blood and mucus, severe bowel urgency, tiredness, weight loss, malaise, or fever. Complications of ulcerative colitis include stricture, toxic megacolon, and cancer. Ulcerative colitis is also associated with extra intestinal diseases such as peripheral arthritis, erythema nodosum, uveites, oral aphthous, sclerosing choangitis, ankylosing spondylitis, and pyoderma gangrenosum. Conventional medicine treats ulcerative colitis with medications designed to suppress the body's immune response, or in severe cases, surgery. This paper explores ulcerative colitis, conventional treatment, and nutritional support for the disease.

Ulcerative Colitis and Nutrition

Ulcerative colitis is a disease that has been sending people running for the bathroom for over 140 years. Ulcerative colitis is far more prevalent and costly than one might think with an estimated one million Americans suffering from this disease and an annual medical cost of a half billion dollars spent in treatment (Stien, Rood, 1999, p.32; Friedman et al., 1996, p.95). It was first recognized as a distinct disease in 1859 by Samuel Wilks, a physician at Guy's Hospital in London. The cause of the disease is still not understood, yet theories abound. Ulcerative colitis is an inflammatory bowel disease (IBD) which affects the large intestine. The disease results in intestinal inflammation and discomfort, diarrhea, and may be accompanied by skin, eye, mouth, joint, or liver diseases as well as an increased risk of colon cancer. Traditional medicine treats ulcerative colitis with drugs aimed at inhibiting the inflammatory response, and in severe cases, surgery. Ulcerative colitis may also be addressed through a nutritional program designed to prevent the occurrence and extent of inflammatory responses. It appears that as one addresses the issue of intestinal permeability, ulcerative colitis is often brought into remission. This paper will describe ulcerative colitis, it's etiology, accompanying diseases and complications, the conventional medical treatment, and explore nutrition as an alternative approach. Since intestinal permeability plays a strong role in the activity of the ulcerative colitis, an explanation of intestinal permeability, or leaky gut syndrome, is presented in appendix A. Appendix B presents a food plan designed to eliminate foods that may cause intestinal permeability or distress.

Ulcerative colitis occurs most commonly among young adults between the ages of 15 and 35, with a second smaller onset between the ages of 50 and 60 (Murray, Pizzorno, 1999, p. 1336, Stien, Rood, 1999, p.24). Statistics vary from men and women being equally affected to women having a 30% higher incidence rate of ulcerative colitis than men (Yamada et al., 1995, p. 1749).

Approximately 10% to 20% of ulcerative colitis patients have a first degree relative (first cousin or closer) afflicted by an IBD, most frequently ulcerative colitis (Feldman et al., 1997, p.1736). The estimates of developing an IBD over a lifetime among first-degree relatives of affected individuals is 8.9% for offspring, 8.8% for siblings, and 3.5% for parents (Yamada et al., 1995, p. 1749). Children frequently develop the disease at a much younger age than did their parents (Feldman et al., 1997, p.1736). The incidence of IBD amongst first degree relatives of IBD is 30 to 100 times that of the general population (Yamada et al., 1995, p. 1749).

Ulcerative colitis is three to eight times more common in Jews that non-Jews (Yamada et al., 1995, p. 1749). Interestingly, ulcerative colitis is rare in African blacks whereas, African-Americans have rates similar to that of Caucasian-Americans suggesting that environmental factors might be involved (Stien, Rood, 1999, p.24). However, Ashkenazic Jews (Eastern European ancestry) in America have higher rates of ulcerative colitis than Sephardic Jews (Spanish and North African ancestry) in America, thus implicating genetic factors (Stien, Rood, 1999, p.25). No clear conclusions have been drawn.

Definition/Description of Ulcerative Colitis

Ulcerative colitis is considered an inflammatory bowel disease (IBD) and specifically affects the large intestine. The large intestine has an average length of 4 to 5 feet and consists of several sections, the cecum, ascending colon, transverse colon, descending colon, sigmoid, rectum, and anus. The colon's primary functions are to absorb water and electrolytes and to propel its contents, including byproducts of digestion, unabsorbed fibers, and mucus, out of the body. Unlike the stomach and small intestine, which are relatively sterile environments, the colon harbors large amounts of bacteria in the lumen (hollow space inside the intestine). Beneficial bacteria aid in digestion, vitamin synthesis (folic acid and other B vitamins), and inhibit the growth of toxic bacteria, viruses, fungi, yeast, and parasites (Pizzorno, 1998, p.138). Harmful bacteria may secrete enzymes which attack epithelial cell proteins causing damage to the intestinal and initiating an immune response.

Ulcerative colitis affects the large intestine and on rare occasions may affect the very lowest section of the small intestine (ileum). Inflammation begins at the rectum and extends upwards a certain distance and then stops abruptly. There is a clear demarcation line between the involved mucosa and uninvolved mucosa. Ulcerative colitis can cause inflammation over the entire large intestine and into the first few centimeters of small intestine. The inflammation generally affects only the first two layers of the lumen, the mucosa, which is innermost layer and absorbs electrolytes and produces mucus, and the submucosa, which contains connective tissue, immune cells, and blood vessels. In severe cases, the ulceration may extend down to third layer, the muscularis, which contains two layers of muscles (Feldman et al, 1997, p.1741). The fourth layer, the serosa, is an outer membrane and is generally unaffected by ulcerative colitis.

The affected mucosa in an ulcerative colitis patient loses its normal folds and becomes flat, additionally, inflammatory polyps or pseudo polyps form. These pseudo polyps may physically resemble cancer. In active disease, mucus production is decreased, edema is present, and the lining of the intestinal tract becomes infiltrated with lymphocytes, macrophages, and other cells of the immune system.

In mild cases of ulcerative colitis there are superficial erosions, whereas in severe cases of the disease, there may be large ulcers or areas in which the mucosa is completely denuded. In chronic cases, the mucosa loses its normal folds, becoming flat and swollen. Most of the pathologic findings in ulcerative colitis are limited to the mucosa or submucosa layers, the muscularis propria is affected only in fulminant (sudden, severe, short duration). Active ulcerative colitis is marked by an intense infiltrate of immune cells, mucus depletion and mucosal edema. Vascular congestion with focal hemorrhage is seen in severe cases. Ulcers, if present, tend to be shallow, only penetrating the muscularis mucosa in severe disease. Signs of chronic activity include inflammatory infiltrate such as lymphoid aggregates, plasma cell, mast cells, and eosinophils in the lamina propria. In inactive ulcerative colitis, the inflammatory infiltrate is less intense than in active disease, however, the mucosa is still usually architecturally abnormal. Shortening and branching of the crypts is typical in all forms of ulcerative colitis. In the inactive disease, goblet cell mucin content is restored to normal. As ulcerative colitis heals, there is residual mucosal edema, absent vasculature, and post inflammatory polyps (Yamada, 1995, p.1769).

As the disease becomes more active the intestine loses it's protective coating because less mucus is produced. This results in an increase in antigens coming into contact with the intestinal lining. These antigens stimulate immune cells which infiltrate the intestinal lining. The immune cells respond to the antigen causing damage to the intestinal cells resulting in increased intestinal permeability. The antigens are then able to enter the body triggering more immune responses at the intestinal site and elsewhere. In this manner the disease builds in severity and may become systemic resulting in other extraintestinal complications which will be discussed later in this paper.

It is important to note that IBD diseases such as ulcerative colitis and Crohn's Disease are different from spastic colon or irritable bowel syndrome (IBS). IBD diseases are inflammatory where IBS is a gastrointestinal tract motility disorder. IBD and IBS bear no direct relationship with one another (Crohn's & Colitis Foundation Association (CCFA), online). IBD, although it's primary site is in the digestive tract, its effects can be systemic, involving the eyes, the skin, the musculoskeletal system, the immune system, as well as having psychological ramifications.

The four types of ulcerative colitis, symptoms of the disease, complications, and extraintestinal manifestations are now presented.

Types of Ulcerative Colitis

The four types of ulcerative colitis are categorized as follows (CCFA, online):

• Ulcerative Proctitis: Limited to the rectum.

  Symptoms include: Bloody stool, tenesmus (sense of bowel urgency and rectal irritation), diarrhea, mild pain in rectal area.

• Proctosigmoiditis: Affects the rectum and the sigmoid colon (the bottom segment of the colon before the rectum). 40% to 50% of ulcerative colitis patients will have the disease limited to the rectum and rectosigmoid colon (Feldman et al. ,1997, p.1740).

  Symptoms include: Bloody diarrhea, cramps, tenesmus, moderate pain on the lower left side of the abdomen when disease is active.

• Left-sided, Limited or Distal Colitis: Affects only the left side of the colon, There is continuos inflammation that starts at the rectum and extends as far as the splenic flexure (a bend in the colon, near the spleen). Left-sided colitis accounts for 30% to 40% of ulcerative colitis patients (Feldman et al. ,1997, p.1740).

  Symptoms include: Loss of appetite, weight loss, diarrhea, severe pain on the left side of the abdomen, bleeding.

• Pan-ulcerative Colitis or Pancolitis: Affects the entire colon. Present in about 20% of patients (Feldman et al. ,1997, p.1740).

  Symptoms include: Diarrhea, severe abdominal pain, cramps, extensive weight loss.

Symptoms

The symptoms of ulcerative colitis may be colonic or systemic.

Colonic symptoms:

• Diarrhea with blood and mucus
• Urgency, tenesmus (sense of bowel urgency and rectal irritation)
• Incontinence
• Lower abdominal cramps and pain with defecation

Systemic symptoms:

• Tiredness
• Weight loss
• Malaise
• Fever

At any point in time, 50% of patients are asymptomatic, 30% have mild symptoms, and 20% have moderate to severe symptoms (Ghosh et al, 2000, p.1119). Many patients have long periods of complete remission, but the cumulative probability of remaining free from relapse at two years is only 20%, decreasing to less than 5% at 10 years (Ghosh et al, 2000, p.1119).

The first symptom of ulcerative colitis is a progressive loosening of the stool. The stool is generally bloody and may be associated with crampy abdominal pain and severe urgency to have a bowel movement. The diarrhea may begin slowly or suddenly. Additionally, there may be skin lesions, pains in the joints, fever, weight loss, anorexia, and in children, failure to thrive (CCFA, online, Anderson et al, 1996 p.28).

Endoscopic evaluation usually reveals erythematous friable, boggy mucosa with loss of the delicate vascular pattern (Anderson et al, 1996 p.28). Biopsy reveals intense inflammatory infiltrate in the lamina propria and some crypts, causing crypt abscesses and in severe disease states, shallow ulceration and pseudo polyps (Anderson et al, 1996 p.29).

When ulceration is confined to the rectosigmoid, the stool may be normal or hard and dry, but rectal discharges of mucus loaded with red and white blood cells accompany or occur between bowel movements. Systemic symptoms are mild or absent. If ulceration extends proximally, stools become looser and the patient may have more than 10 bowel movements per day, often with severe cramps and distressing rectal tenesmus, without relief at night. The stools may be watery, may contain mucus, and frequently consist almost entirely of blood and pus. Malaise, fever, anemia, anorexia, and weight loss may be present with extensive active ulcerative colitis.

Complications

As ulcerative colitis progresses, complications may occur which include:

Stricture: Narrowing of the intestine. Most strictures are short, typically 2 to 3 cm in length although longer ones may occur (Yamada, 1995, p.1789). Strictures often develop in patients with extensive disease and continous symptoms without remission. They tend to occur late in the course of the disease, typically 5 and 25 years after disease onset. Strictures are frequently seen in the sigmoid colon and rectum (Yamada, 1995, p. 1789). Symptoms include an increase in diarrhea, and fecal incontinence (Yamada, 1995, p. 1789). Strictures have been associated with malignancies in ulcerative colitis and are therefore viewed as potentially malignant lesions (Yamada, 1995, p.1789). Surgical treatment may be required.

Toxic Megacolon: The colon loses its muscle tone, distends, and is in great danger of perforating. Symptoms include fever higher than 38.6 C (101.5 F), heart rate greater than 120 beats per minute, anemia, and neutrophil leukecytosis greater than 10,5000 cells/mm3 (Yamada, 1995, p.1789).

Perforation: A perforation occurs when an ulceration in the colon extends through the intestinal wall, causing a hole. This may result in allowing bacteria to enter the blood stream and cause a systemic infection. Most perforations occur in the left colon, particularly the sigmoid colon (Yamada, 1995, p. 1789). This condition requires immediate surgery, however it usually occurs in only severely ill patients and rarely in the early stages of the disease (Brandt et al., 1989, p.86).

Cancer: The risk of colon cancer becomes statistically greater with the severity and long term duration of the disease (Carson-DeWitt, 1999, p.2955):

• At 10 years, the risk of cancer is about 0.5-1%.
• At 15 years, the risk of cancer is about 12%.
• At 20 years, the risk of cancer is about 23%.
• At 24 years, the risk of cancer is about 42%.

Since the risk of cancer increases after a person has had the disease for 8 years, an annual surveillance colonoscopy is recommended (Stien, Rood, 1999, p.37).

Associated Diseases

Extraintestinal (non intestinal) complications occur in up to 45% of patients with ulcerative colitis (Stien, Rood, 1999, p.37). Complications may be related to disease activity or may be totally independent. Diseases related to the activity of the ulcerative colitis may proceed the disease and act as an early warning system. They may also become active prior to a flare up, again acting as a warning. The diseases which correlate with ulcerative colitis are as follows:

Peripheral arthritis occurs in approximately 10% to 12% of patients with ulcerative colitis (Anderson et al, 1996, p.248). It is an inflammatory condition of the large joints, particularly the knees, ankles, hips, and shoulders, followed by the wrists and elbows. The fingers and toes generally are not affected and are less likely to have any relation to the state of the disease activity (Stien, Rood, 1999, p.56, Anderson et al, 1996, p.29). Sore joints may precede a flare up of ulcerative colitis.

Erythema nodosum is a skin condition manifesting as tender bumps on the fronts of the lower legs and often on the thighs or arms, the lesions may resemble large red insect bites (Brandt, Steiner-Grossman, 1989, p.42). The bumps may be associated with fever and joint pains and may precede a change in bowel symptoms (Stein, Rood, 1999, p.59). These bumps may appear indicating an impending flare up of ulcerative colitis.

Uveitis is the most common type of eye inflammation associated with IBD (Brandt, Steiner-Grossman, 1989, p.46) which may occur in up to 12% of people with ulcerative colitis and occurs in about 50% of those ulcerative colitis patients who also suffer from spinal arthritis. Uveitis is an inflammation of the middle layer of the eye and left untreated may result in permanent damage including glaucoma, cataracts, or loss of vision. Ulcerative colitis patients should see an ophthalmologist immediately if they notice a change in their vision.

Oral aphthous are small oral ulcers surrounded by a reddening of the skin. These ulcers occur in at least 10% of ulcerative colitis patients and disappear when the disease goes into remission (Feldman et al., 1997, p.1749).

Complications or diseases commonly associated with ulcerative colitis, which are unrelated to the activity of the disease include:

Sclerosing cholangitis occurs in approximately 3% of ulcerative colitis patients (Feldman et al., 1997, p.1750). Sclerosing cholangitis is characterized by both inflammation and scarring of the bile ducts which can lead to chronic liver disease, cirrhosis, and liver failure, ultimately requiring a liver transplant (Stien, Rood, 1999, p.38).

Ankylosing Spondylitis or Spinal Arthritis occurs in roughly 1% to 6% of patients with ulcerative colitis (Anderson et al, 1996, p.30). The symptoms include lower back pain and morning stiffness that improves with activity and a restriction of chest and spinal movement (Anderson et al, 1996, p.30). The disease may lead to a fusion of the sacroiliac joints (located on each side of the lowest portion of the spine where it joins to the pelvic bones) resulting in permanent damage and lack of range of motion. Ulcerative colitis patients are encouraged to do stretching exercises such as yoga to keep the lower back flexible and the sacroiliac joints from fusing.

Pyoderma Gangrenosum is a severe skin problem which is characterized by a painful area of deep undermining ulceration surrounded by irregular heaped-up borders (Brandt, Steiner-Grossman, 1989, p.44). The problem begins as groups of small pimples or pustules that coalesce, widen and ulcerate (Brandt, Steiner-Grossman, 1989, p.44). Pyoderma occurs most commonly on the lower legs and feet, but may occur anywhere on the body (Brandt, Steiner-Grossman, 1989, p.44). Seek treatment immediately.

Diagnosis and Conventional Treatment

Diagnosis of ulcerative colitis is based on clinical signs, the results of barium x-ray films of the colon, and colonoscopy with biopsy. The disease is then rated in terms of severity to determine treatment. Disease severity as presented by Truelove and Witts (Feldman et al., 1997, p.1743; Yamada, 1995, p.1754):

• Mild: Less than four stools a day, with or without blood, no systemic disturbance, no fever, no elevated heart rate, mild anemia, and a normal erythrocyte sedimentation rate (ESR).
• Moderate: More than four stools daily, but with minimal systemic disturbance.
• Severe: More than six stools a day, with blood, marked abdominal tenderness, and evidence of systemic disturbance such as fever, increased heart rate (higher than 90 beats/minute), anemia (hemoglobin of 75 mg/dL or less compared to/with normal values, allowing for transfusions), or an ESR of more than 30 mm/h.

Conventional treatment consists of medications and surgery. The drugs typically used are corticosteroids, aminosalicylates, or immunomodulatory medicines. Corticosteroids, such as prednisone, alter the body's ability to create and maintain inflammatory responses. These medications are used in moderate to severe cases of ulcerative colitis (CCFA, online). Side effects of corticosteroid therapy include: increased appetite, weight gain, retention of salt and water, and increased susceptibility to infection (Murray, 1994, p.156). Side effects that result from long term use include: depression and other mental/emotional disturbances, high blood pressure, diabetes, peptic ulcers, acne, excessive facial hair in women, insomnia, muscle cramps and weakness, thinning and weakening of the skin, osteoporosis, and susceptibility to the formation of blood clots (Murray, 1994, p.156).

Aminosalicylates such as Asacol, 5-ASA, and Sufasalazine also alter the body's ability to create and maintain inflammation. These drugs are used in mild to moderate episodes of ulcerative colitis and to prevent relapse (CCFA, online). Common side effects of Asacol include diarrhea, dizziness, headache, nausea, rhinitis, stomach pain/cramps, vomiting, and unusual tiredness and weakness (medscape, online). Side affects of 5-ASA include nausea, vomiting, anorexia, headache, fever, rash, and abdominal discomfort (Yamada, 1995, p.1776). Sulfasalazine is known to inhibit folic acid absorption (Yamada, 1995, p.1777).

Immunomodulatory medicines such as 6-mercaptopurine (6-MP) inhibit immune cells from interacting in the inflammatory process. These drugs are used when other medications have been ineffective or when trying to wean a patient off of corticosteroids (CCFA, online). 6-MP may take as long as 3 to 6 months to become effective (Stien, Rood, 1999, p.35). Side effects usually occur within 3 weeks of taking drug and include allergic reactions, pancreatitis, and hepatitis (all reversible upon discontinuing the drug)(Stien, Rood, 1999, p.50). 6-MP can and often does lower the white blood counts and sometimes the platelet counts as well (Stien, Rood, 1999, p.50). Careful monitoring of blood counts is required when taking 6-MP.

Surgical treatment consists of removing all or part of the colon, resulting in either a resection, or an ostomy. An ostomy is when an alternative opening is created to rid the body of fecal matter. An ostomy renders the patient incontinent of stool and gas requiring that a pouch, to collect the fecal matter, be worn at all times. A colonectomy is where the colon is completely removed and is considered a curative procedure for ulcerative colitis (Yamada, 1995, p.1786). A colonectomy comes with its own set of problems which will not be discussed in this paper.

Theories as to the Cause of Ulcerative Colitis

There are four theories as to the cause of ulcerative colitis:

• Genetic Predisposition
• Microbial Pathogen
• Dietary Factor
• Immune System malfunction

Genetic Predisposition

No clear genetic predisposition has been identified. There seems to be an association between the HLA-DR2 gene and ulcerative colitis (Yamada et al., 1995, p.1750). There is also a study which found the allele 2 gene mutation more common in people with ulcerative colitis than those without (52% vs. 45%), however the association is minor and confers only a small risk (Carter et al., 2001, abstract). The search for specific genetic factors continues.

Microbial Pathogen

This theory suggests that a microbial pathogen is what causes ulcerative colitis. A microbial pathogen could be a bacteria, fungus, or parasite. Commonly known pathogens are candida and klebsiella. Other known and unknown pathogens might be involved in the etiology of this disease. The thought here is that a pathogen is present in the intestine and the body launches an immune response. However, the immune response is ineffective and as the body continues in its futile efforts to destroy the pathogen, many healthy intestinal cells are killed in the process. This continual immune response causes irritation, inflammation and ulceration of the intestinal tract. Theories abound as to who the culprit or pathogen could be, but there is no clear or decisive evidence implicating one over the other. One suspect is Bacteroides vulgatus. The pathogenic role of Bacteroides vulgatus in patients with ulcerative colitis was studied in Japan. High levels of antibodies to the 26-kDa protein, which is on the outer membrane of Bacteroides vulgatus, were found in the serum of the inflamed rectal mucosa of ulcerative colitis patients (Bamba, 1995, abstract). The researchers of this study believe that Bacteroides vulgatus is strongly implicated in the pathogenesis of ulcerative colitis (Bamba, 1995, abstract).

Dietary Factor

Food has been a suspect in the etiology of ulcerative colitis ever since 1942 when Andresen first suggested that this disease may be caused by an allergy to milk (Andresen, 1942, abstract). When a person has developed an allergy or a sensitivity to a food, the body launches an immune response against it when it comes into contact with the intestinal wall. As with the pathogen, this causes damage and inflammation and the wall becomes even more permeable to food and other antigens. A study of 24 ulcerative colitis patients reported a direct link between the onset of ulcerative colitis symptoms and the consumption of a meal in two thirds of the study participants (Swiatkowski et al., 1993, abstract). It has been said that "food represents the largest antigenic challenge confronting the immune system" (Murray and Pizzorno, 1998, p.467).

Immune System Malfunction

The immune system theory is that of an autoimmune disorder where the body actually attacks itself. The body mistakes itself for an antigen and launches an attack against its own healthy cells. Antibodies to epithelial cell associated protein 40-kd appear to be unique to ulcerative colitis (Feldman, 1997, p.1738). In a normal person, there is immune tolerance to this self antigen, but not in the ulcerative colitis patient for some unknown reason. Therefore, in the ulcerative colitis patient, the body is mistakenly destroying its own epithelial cells.

The cause of ulcerative colitis is not known and may be a combination of several of the above. For example, it may be due to genetics and a microbial pathogen. A study found that rats injected with the human gene HLA-B27 and then introduced to a bacterial cocktail containing Bacteroides (a common human intestinal bacteria) developed ulcerative colitis (Fackelmann, 1996, p.302). Scientists know that people who inherit the HLA-B27 gene have an increased risk of developing inflammatory diseases (Fackelmann, 1996, p.302). HLA-B27 is a normal gene and not a mutation, roughly 4% of people carry this gene (Fackelmann, 1996, p.302).

All of the proposed etiologies for ulcerative colitis result in increased intestinal permeability, which is a key factor in the disease activity. Some abnormalities specific to ulcerative colitis patients are now discussed.

Abnormalities Specific to Ulcerative Colitis Patients

There are several abnormalities specific to ulcerative colitis which are stated repeatedly throughout the literature. They are as follows:

1. Decreased levels of sIgA (Yamada et al, 1995, p 1751).

   sIgA is an immunoglobulin that binds antigens and escorts them out of the system so that they do not cause an immune reaction.

2. Decreased levels of mucus secreted by goblet cells when the disease is active (Murray and Pizzorno, 1998, p.592).

   Mucus protects the intestinal lining by trapping pathogens and flushing them out of the system. It works much the same way as when you have an allergy to pollen and your nose runs copiously trying to flush the irritant out.

3. Decreased levels of butyrate in the colon compared to normal (Duffy et al, 1998, abstract).

   Butyrate is produced by healthy bacteria and supplies food to the colonic intestinal cells. When butyrate levels are increased in rats, inflammation, occult blood, and mucosal hyperplasia are all reduced (Kanauchi et al, 1999, abstract).

4. Levels of Bacteroides Vulgatus six times as high as normal levels (Murray and Pizzorno, 1999, p.1340).

   Bacteroides Vulgatus and carrageenan are combined in laboratory animals to produce ulcerative colitis. This suggests that carrageenan, an additive found in ice-cream, and other processed foods, may exacerbate the disease.

5. Increased production and serum levels of IgG1 and IgG3 signifying increased sensitivity to protein and T-cell dependent antigens (Yamada et al., 1995, p.1751). This suggests that protein antigens, such as those found in food, may predominate the allergic response (in contrast, Crohn's disease has an increase in IgG2 markers which suggests a response to carbohydrates and many bacterial agents) (Yamada et al., 1995, p.1751).

All of the above stated factors help cause and culminate in the last, increased intestinal permeability.

1. Increased intestinal permeability (Den Hond et al., 1998, abstract).

   Increased intestinal permeability allows pathogens to enter the intestinal lining and results in an immune response.

Intestinal permeability results in an increase in the immune response which damages the cells lining the intestine. This results in increased intestinal permeability. "Many scientists believe that increased intestinal permeability is the critical dysfunctional mechanism that sets inflammatory bowel disease (IBD) into motion and modulates subsequent progression of the disease" (Great Smokies Diagnostic Laboratory, online). Reducing intestinal permeability appears to result in disease remission.

A brief look at the various causes of intestinal permeability follows. For a more complete discussion on the mechanism and causes of intestinal permeability or leaky gut syndrome, please see appendix A.

Causes of Intestinal Permeability

• Food allergies/sensitivities
• Coffee
• Giardia and other parasites
• Celiac disease
• Intestinal dysbiosis
• Alcohol
• Deficient levels of sIgA
• Antibiotics
• Deficient mucus secretion
• Malnutrition
• Pancreatic insufficiency
• Stress
• Deficient levels of HCl
• Intestinal infection
• Nonsteroidal anti-inflammatory drugs (NSAIDs) including aspirin

The challenge is to determine which factor or factors are causing the increased permeability and eliminate it or them. There are several tests which are useful in diagnosing the cause and extent of intestinal permeability.

Diagnostic Tools (tests)

Test	Diagnosis
Comprehensive Digestive Stool Analysis	Digestive Wellness
Enzyme-Linked Immunosorbent Assay/ALCAT	Food Allergies/Sensitivities
Food Challenge Tests	Food Allergies/Sensitivities
Lactulose/Mannitol Absorption Test	Intestinal Permeability

The Comprehensive Digestive Stool Analysis (CDSA) is a battery of laboratory tests which evaluate digestion, intestinal function, intestinal environment, and nutrient absorption by examining the stool. The test determines if proteins, carbohydrates and fats are being properly digested, the amount and type of bacteria in the intestine, levels of secretory IgA, pH levels, and a myriad of other pertinent parameters. The results of this test are very useful in determining which part of the digestive system needs treatment or support and which pathogens need to be removed. This test is strongly recommended as a diagnostic tool.

The Enzyme-Linked Immunosorbent Assay, ALCAT, and Food Challenge Tests are tests designed to determine which foods one is allergic to. The Enzyme-Linked Immunosorbent Assay and ALCAT are laboratory tests which require a blood draw. The blood is then exposed to different foods and the reaction noted. The Food Challenge Tests are non laboratory tests that may be conducted under the supervision of a doctor. The basic idea is to eat a very restricted diet of 4 or so known non-allergenic foods for two weeks. Then, once every 48 or 72 hours, introduce a new food noting any immediate or delayed reactions. In this manner, one may determine which foods pose an antigenic challenge to the body and may be eliminated. These tests are highly recommended to determine which foods are irritating the intestine and causing immune reactions, thus exacerbating the disease.

The Lactulose/Mannitol Absorption Test is an intestinal permeability test. The patient drinks a sugar solution and based on a urine analysis taken 6 hours later, intestinal permeability may be assessed (Great Smokies, 1999, p. G-32). This test is recommended as a diagnostic tool to track the effectiveness of the program and for gauging potential remission and relapses of the disease (Great Smokies Diagnostic Laboratory, online).

Beneficial Nutrients

Specific nutrients found to be particularly beneficial in ulcerative colitis include:

Fish oil

Fish oil appears to reduce intestinal inflammation. A study conducted over a four month period of time in which ulcerative colitis patients were either given 18 capsules of Max EPA fish oil daily (3.24 gm of eicosapentaenoic acid and 2.16 gm of docosahexaenoic acid) or a placebo consisting of vegetable oil found that the fish oil group had an average 65% drop in the level of inflammatory chemicals in the intestine, an 80% drop in the level of cellular abnormalities in the intestine, and a weight gain of 4 pounds after four months (Pizzorno, 1998, p 190). The fish oil group experienced in a mean prednisone dose decrease from 12.9 mg/dl to 6.1 mg/dl while the control group showed no significant improvements in inflammation or cell abnormalities, and the dose of prednisone rose on average from 10.4 mg/d to 12.9 mg/d (Stenson et al., 1992, abstract). Fish oil appears to be helpful in ulcerative colitis by reducing inflammation.

Probiotics

Probiotics (healthy or beneficial bacteria) may eliminate or displace causative organisms in ulcerative colitis. It was found that after killing the Bacteroides, one could add a harmless bacteria, (e.g. Lactobacillus), which would occupy the same niche and prevent the Bacteroides from coming back (Fackelmann, 1996, p.303). Thus, probiotics may displace and competitively compete with harmful bacteria.

Secondly, ulcerative colitis patients have been shown to have low levels of sIgA. Several studies show that the probiotic Lactobacillus GG (LGG) increases sIgA levels, as does Bifodobacterium (Lung, 1999, abstract; Schultz, 2000, p.S20).

These are some possible mechanisms of probiotics (Vanderhoof et al, 1998, p324):

• Competitive inhibition of bacterial adhesion
• Synthesis of compounds that inhibit or destroy pathogens
• Stimulation of immune response to pathogens
• Competitive consumption of nutrients required for growth of pathogens.

L-Glutamine

Dietary deficiency of glutamine is associated with atrophy and degenerative changes in the small intestine, resulting in intestinal permeability (Ackerson, IET syllabus p. 9-54). Glutamine supplementation has shown to prevent and repair damage to the intestinal mucosa (Ackerson, IET syllabus, p.9-54). L-Glutamine also appears to be required for the synthesis of secretory IgA (sIgA) (Ackerson, IET syllabus). L-glutamine is an important factor in rebuilding the intestinal lining.

N-Acetyl-Glucosamine

NAG is the key precursor in the biosynthesis of mucosal glycoprotiens, a major component of intestinal mucus (Ackerson, IET syllabus p. 9-54). Normally, L-glutamine is converted first to NAG, and then into mucosal glycoprotiens (Ackerson, IET syllabus p. 9-54). However, in IBD patients, there is a defect in the pathway between the conversion of L-Glutamine to NAG, therefore NAG must be taken for glycoprotien production (Ackerson, IET syllabus p. 9-54). Without the glycoprotiens, the intestinal wall lies unprotected and antigens adhere causing an immune response, intestinal inflammation, and damage. NAG is also a highly active growth promoter for Bifidobacterium bifidum (Ackerson, IET syllabus p. 9-54). Bifidobacterium bifidum competitively competes with harmful bacteria for binding sites at the intestinal wall (Vanderhoof et al, 1998, p.324)) and raises sIgA (Schultz et al. , 2000, p.S20).

Quercetin, Curcumin, and Bromelain

Quercetin is a potent antioxidant and has been shown to dramatically reduce the allergic/inflammatory response by inhibiting the release of inflammatory compounds (Murray, 1994, p. 96). Curcumin may be helpful as it is found to be as effective as cortisone in models of acute inflammation, however, it is only half as effective in chronic models (Pizzorno, 1998, p.183). Bromelain is also useful as it digests foreign proteins, thus reducing the antigenic load, while it also blocks the production of pro-inflammatory compounds (Murray, 1994, p.80). Together, quercetin, curcumin, and bromelain act synergestically to produce a strong anti-oxidant, anti-antigenic, and anti-inflammatory affect.

Nutritional Program for Ulcerative Colitis

Ulcerative colitis disease activity and intestinal permeability are directly correlated. Address the permeability problem and ulcerative colitis appears to go into remission. The following nutritional recommendations are geared toward making the intestinal tract less permeable, normalizing the abnormalities specific to ulcerative colitis patients and reducing the inflammatory response to minimize damage. The program will be a combination of diet, supplements, herbs, and lifestyle changes. All of these factors will be discussed in the framework of the "4R Program". "The 4R Program" is an efficient way to promote gastrointestinal healing and optimal food absorption. The four "R"s stand for remove, replace, re-inoculate, and rebuild/repair. It is important to implement and accomplish the remove phase first, before implementing the rest of the program. The replace, re-inoculate, and rebuild/repair stages may be implemented simultaneously, or in the order presented. The remove phase must be followed during the entire program.

Remove

Remove anything from the diet and system which may be causing or perpetuating the cycle of inflammation and leading to increased intestinal permeability. A comprehensive digestive stool analysis (CDSA) is highly recommended to determine which pathogens may be present and how best to remove them. Follow the remove stage of the program for at least two weeks before starting the other stages.

Remove:

• Microbial pathogens such as bacteria, parasites, yeast, etc. per CDSA results.
• Food allergens and foods to which the body is sensitized.
• Foods, herbs, and spices which cause inflammation or irritate the mucosal lining such as alcohol, caffeine, carageenan, chilies, curries, vinegar, pepper, mustard, cayenne.
• Refined carbohydrates such as sweets, chocolate, soft drinks, white bread, or any foods that may contain disaccharide sugars (See Appendix B for the Specific Carbohydrate diet which lists foods to eat and foods to avoid and is followed by a brief explanation as to the theory behind the diet).
• Stress
• Toxins including herbicides, pesticides, etc.
• NSAIDs and other medications (except as required).
• Land based proteins such as red meat and pork which are high in inflammatory fats.
• Processed foods and foods which are low in fiber.
• Commercially grown foods laden with pesticides and herbicides.

Include in the diet:

• Fiber to bind and eliminate intestinal toxins and to feed healthful bacteria. Soluble fiber is best since non-soluble fiber (such as wheat bran) may be irritating to the intestinal lining. Soluble fiber may be found in such foods as apples, pears, legumes, flax seeds, etc. Note: Lack of fiber may result in intense muscle spasms due to the lack of fecal bulk which acts as a physical buffer (Grimes, 1976, abstract).
• Water to continually flush the body of toxins. Drink at least 8 glasses of pure water a day.
• Chew food thoroughly to promote saliva. Saliva is high in secretory IgA (sIgA) which binds to the antigens or toxins and then escorts them out of the body, leaving them unable to irritate or be absorbed into the intestinal mucosa.
• Protein foods such as fish, very lean meats, and other protein sources which are low in inflammatory fats.
• Whole organic foods which are high in fiber and low in pesticides and other toxins.

Supplements:

Garlic	1/2 clove three times a day	Inhibits and eliminates toxic microorganisms
Fiber	30 gm a day of mostly soluble fiber	Binds intestinal toxins

Replace

Replace necessary digestive factors which may be deficient due to the gut's weakened state. This will allow the body to digest food properly, absorbing its nutrients and rendering it non-antigenic. Digestive factors include: secretory IgA, gastric acid, pancreatic enzymes, and bile secretions. Replace as needed based on the CDSA results.

To support digestive function:

• Chew food thoroughly! When food is chewed properly, 98% of the proteins eaten are absorbed as amino acids and small peptides (Murray, 1993, p.252). The food is much less allergenic.
• Eat in a relaxed state, this allows the body to put its energy into digesting the food and increases sIgA.
• Drink between meals, liquids dilute the stomach juices inhibiting digestion of meals.
• Eat bitter foods and herbs such as dandelion, artichoke, and turmeric to support bile secretion.

Supplements:

Hydrochloric acid (HCl)	Take 1 capsule (600 mg) before a meal, add a capsule each meal until a warm feeling is reached in the stomach, up to 7 capsules, then reduce dose by one.	Increases HCl in stomach for proper food digestion
Digestive Bitters	As directed on label	Stimulates the production of HCl in the stomach
Pancreatin	500 to 1,000 mg of 10X USP 3 times/day before meals	Improves digestion
Dandelion	1 to 3 capsules daily	Increases bile flow for digestion of fats
Bromelain*	400 mg three times a day between meals	Anti-inflammatory, aids in digestion of proteins
Inositol with	50 mg 3 times a day with meals	Emulsifies fats
Choline	50 mg 3 times a day with meals	Emulsifies fats
Lecithin	As directed on label	Emulsifies fats
Burdock, Turmeric, Ginger, and Black cohosh	As a tea, spice or supplement (take as directed on label) Note: Do not use Black cohosh if pregnant	Anti-inflammatory herbs

Re-inoculate

Re-inoculate or rebuild the gut with beneficial flora (probiotics) and nutrients (prebiotics) that support their colonization. Healthy bacteria (probiotics) inhibit the growth of toxic bacteria, viruses, fungi, yeast and parasites (Pizzorno, 1998, p.138). Healthy bacteria also aid in digestion, vitamin synthesis (folic acid and other B vitamins), and increases levels of sIgA. The primary strains of probiotics used to reseed the intestines are Lactobacillus acidophilus and Bifidobacteria. Bifidobacteria is extremely important as it has been shown to competitively compete with Bacteroides Vulgatus which is present in high levels in ulcerative colitis patients. The common prebiotics used are fructooligosaccharides (FOS) and inulin. Fermented foods such as sauerkraut contain probiotics. Onions, asparagus, and bananas are sources of prebiotics.

Supplements:

Lactobacillus acidophilus	3 to 10 billion organisms/day taken on an empty stomach	Re-inoculates the gut
Bifidobacteria	3 to 10 billion organisms/day taken on an empty stomach	Re-inoculates the gut
Inulin/FOS	3 gm once a day	Enhances population of healthy bacteria in the gut

Rebuild/Repair

Rebuild and repair the mucosal lining of the intestine. Rebuilding and repairing the mucosal lining will result in fewer antigens or toxins entering the body, increased nutrient absorption, and decreased inflammation. To rebuild and repair the intestinal lining, it is important to support the mucosa, the epithelial cells, and decrease inflammation.

• Eat a wide variety of fruits and vegetables which contain anti-oxidants including carotonoids and flavonoids. Anti-oxidants reduce free radicals which damage cells and cause inflammation. Anti-oxidants such as vitamins A, E, and C, zinc, selenium and an array of carotonoids and flavonoids may be found in wide variety of deeply colored fruits and vegetables. In general, the more pigments the fruit or vegetable has, the more anti-oxidant properties and nutrients it contains.
• Consume essential fatty acids such as those found in cold water fish, flax seeds, evening primrose oil, and borage seed oil. Essential fatty acids make the anti-inflammatory prostoglandins which reduce inflammation. Fish oil has been found to be particularly beneficial.
• Cabbage, okra, and onion are foods and herbs which are especially soothing and beneficial to the intestinal healing.

Supplements:

*Quercetin, bromelain, curcumin, and vitamin C act synergistically as a strong anti-inflammatory complex, and may be able to be purchased as a single supplement. Look for a dose of 400 mg of each substance, take a half hour before each meal.

Pre-packaged Program

Above is a lot of supplements to mix and match. Listed below is a pre-packaged alternative which may be taken instead of the individual supplements listed above. Note that the remove phase of the "4R" program must still be followed. Other companies have other pre-packaged programs, this is just one example.

Tyler Protocol (Take as directed on label)

Remove (2 to 4 weeks)

• Para-Gard - Suppresses intestinal pathogens (do not use if pregnant or nursing).
• Protease Concentrate - Plant enzymes for protein digestion.
• Fiber Formula - Soothing fiber formula, absorbs intestinal toxins (do not use if pregnant or nursing).

Replace and Repair/Rebuild (4 to 6 weeks)

• Similase - Plant enzymes.
• Permeability factors - Nutrients which repair and rebuild the intestinal lining.
• Oxyperm - Antioxidants.
• Fiber Formula - Soothing fiber formula, absorbs intestinal toxins (do not use if pregnant or nursing).
• Enterogenic Concentrate - Probiotics and prebiotics.

Maintenance

When the intestinal permeability has returned to normal, as per diagnostic tests or after symptoms have dissipated, continue to support and maintain proper gut functioning with the following maintenance program:

• Avoid allergenic foods.
• Eat "tolerated" foods infrequently and never two days in a row.
• Avoid processed foods and unnecessary toxins.
• Eat a diet of whole, organic, unprocessed foods high in fruits and vegetables.
• Drink at least 8 glasses of water a day.
• Take a good quality multivitamin and mineral supplement.
• Chew food thoroughly.
• Eat in a relaxed state.

CONCLUSION

Ulcerative colitis is an intestinal inflammatory disease of unknown etiology. Many people suffer from the disease which appears to be strongly correlated to intestinal permeability. Through discovering and removing the antigen or antigens that may be causing intestinal permeability and rebuilding the intestinal lining, one may be able to put the disease into remission. This paper has discussed ulcerative colitis, the diseases associated with it, where and how it occurs, theories as to its cause, tests to diagnose intestinal irritants and assess permeability, and has put forth a protocol to address the disease.

References

_____. "IBD and Intestinal Permeability" Great Smokies Diagnostic Laboratory. (online) www.gsdl.com. (visitied 4/20/01).

_____. "Ulcerative Colitis". NIH Publication No. 95-1597. National Digestive Diseases Information Clearinghouse, Bethesda, MD, April, 1992. (online) http://www.gastro.com/uc.htm. (visited 4/20/01).

Ackerson, Amber, N.D. "Nutritional Management of Intestinal Permeability Defects". Institute for Educational Therapy Syllabus. Cotati, California, 2001.

Anderson, Mark M.D., Robinson, Malcolm M.D. "Watching for - and managing - joint problems in inflammatory bowel diseas." The Journal of Musculoskeletal Medicine, 1996, Nov p.28-34.

Andresen. "Ulcerative Colitis: An Allergic Phenomenon," Am J Dig Dis, March, 1942;9(3):91-98.

Balch, James M.D., Balch, Phyllis A, C.N.C. Prescription for Nutritional Healing. Avery Publishing Group, Garden City Park, New York, 1997.

Bamba T, Matsuda H, Endo M, Fujiyama Y. "The pathogenic role of Bacteroides vulgatus in patients with ulcerative colitis." J Gastroenterol 1995 Nov;30 Suppl 8:45-7.

Brandt, Lawrence J., Steiner-Grossman, Penny. Treating IBD: a patient's guide to the medical and surgical management of inflammatory bowel disease. National Foundation for Ileitis and Colitis and Raven Press, New York, New York, 1989.

Carson-DeWitt, Rosalyn S. "Ulcerative Colitis". (online) Exerpt from Gale Encyclopedia of Medicine. Gale Research, Inc., 1999. p.2955. (Visited 04/20/01).

Carter MJ, di Giovine FS, Jones S, Mee J, Camp NJ, Lobo AJ, Duff GW. "Association of the interleukin 1 receptor antagonist gene with ulcerative colitis in Northern European Caucasians." Gut 2001, April;48(4):461-467).

Chapman MA, Grahn MF, Boyle MA, Hutton M, Rogers J, Williams NS. "Butyrate oxidation is impaired in the colonic mucosa of sufferers of quiescent ulcerative colitis." Gut 1994 Jan;35(1):73-6

Chapman MA, Grahn MF, Hutton M, Williams NS. "Butyrate metabolism in the terminal ileal mucosa of patients with ulcerative colitis." Br J Surg 1995 Jan;82(1):36-8.

Crohn's & Colitis Foundation of America, Inc. (CCFA) Crohn's & Colitis Foundation of America, Inc., New York, New York. (Online) http://www.ccfa.org (visited: 04/20/01)

D'Argenio G, Cosenza V, Delle Cave M, Iovino P, Delle Valle N, Lombardi G, Mazzacca G. "Butyrate enemas in experimental colitis and protection against large bowel cancer in a rat model." Gastroenterology 1996 Jun;110(6):1727-34.

Den Hond E, Hiele M, Evenepoel P, Peeters M, Ghoos Y, Rutgeerts P. "In vivo butyrate metabolism and colonic permeability in extensive ulcerative colitis." Gastroenterology 1998 Sep;115(3):584-90.

Duffy MM, Regan MC, Ravichandran P, O'Keane C, Harrington MG, Fitzpatrick JM, O'Connell PR. "Mucosal metabolism in ulcerative colitis and Crohn's disease." Dis Colon Rectum 1998 Nov;41(11):1399-405.

Duke, James A, Ph.D. The Green Pharmacy. Rodale Press Inc., New York, New York, 1998.

Fackelmann, Kathleen. "Gastrointestinal Blues: Research finds buge that inflame the human gut." Science News, 1996,Vol. 150, p. 302-303.

Feldman, Mark, M.D. Sleisenger, Marvin, H., M.D., Scharschmidt, Bruce F., M.D. Sleisenger and Fordtran's Gastrointestinal and Liver Disease: Pathophysiology/Diagnosis/Management. W.B. Saunders Company, Philadelphia, Pennsylvania, 1997.

Fetrow, Charles W. PharmD, Avila, Juan R. PharmD. The Complete Guide to Herbal Medicines. Springhouse Corporation, Springhouse, PA, 2000.

Finnie IA, Dwarakanath AD, Taylor BA, Rhodes JM. "Colonic mucin synthesis is increased by sodium butyrate." Gut 1995 Jan;36(1):93-9

Friedman, Scott L., MD, Grendell, James H., MD, McQuaid, Kenneth R. MD. Current Diagnosis & Treatment in Gastroenterology. Appleton and Lange, 1996, Stamford, Connecticut.

Giaffer MH, Holdsworth CD, Duerden BI "The Assessment of Faecal Flora in Patients With Inflammatory Bowel Disease by a Simplified Bacteriological Technique." J Med Microbiol, 1991;35:238-243.

Ghosh, Subrata, Shand, Alan, Ferguson, Anne. "Ulcerative Colitis". British Medical Journal, April 22, 2000 v320 i7242 p1119.

Great Smokies Diagnostic Laboratory. Functional Assessment Resource Manual. Great Smokies Diagnostic Laboratory, Asheville, NC, 1999.

Grimes, DS "Refined Carbohydrate, Smooth-Muscle Spasm and Disease of the Colon." Lancet, February 21, 1976;395-397.

Kanauchi O, Andoh A, Iwanaga T, Fujiyama Y, Mitsuyama K, Toyonaga A, Bamba T. "Germinated barley foodstuffs attenuate colonic mucosal damage and mucosal nuclear factor kappa B activity in a spontaneous colitis model." J Gastroenterol Hepatol 1999 Dec;14(12):1173-9.

Lipski, Elizabeth M.S., C.C.N. Digestive Wellness. Keats Publishing, Los Angeles, California, 2000.

Medscape DrugInfo. (online) http://promini.medscape.com/drugdb/drug_adverse_effects.asp? (visited: 05/02/01)

Murray, Michael T., N.D. Natural Alternatives To Over The Counter And Perscription Drugs. William Marrow and Company, Inc., New York, New York, 1994.

Murray, Michael T., N.D. The healing Power of Foods. Prima Publishing, Rockland, California, 1993.

Murray, Michael T., N.D., Pizzorno, Joseph, N.D. Encycopedia of Natural Medicine. Prima Publishing, Rocklin, California, 1998.

Pizzorno, Joseph E, N.D. Total Wellness. Prima Publishing, Rocklin, California, 1998.

Pizzorno, Joseph E, N.D., Murray, Michael T., N.D. The Textbook of Natural Medicine. Churchill Livingstone, London, England, 1999.

Roediger, WE. "The starved colon--diminished mucosal nutrition, diminished absorption, and colitis." Dis Colon Rectum 1990 Oct;33(10):858-62.

Schultz, Michael, M.D. and Sartor, Balfour, M.D. "Probiotics and Inflammatory Bowel Diseases". The American Journal of Gatroenterology, Vol. 95, No. 1, Suppl,. 2000 p. S19-S21.

Stein, Stanley H., M.D., Rood, Richard P., M.D., F.A.C.P. Inflammatory Bowel Disease: a guide for patients and their families. Lippincott-Raven Publishers, Philadelphia, PA, 1999.

Stenson WF, Cort D, Rodgers J, Burakoff R, DeSchryver-Kecskemeti K, Gramlich TL, Beeken W. "Dietary supplementation with fish oil in ulcerative colitis." Ann Intern Med 1992 Apr 15;116(8):609-14.

Swiatkowski M, Klopocka M, Suppan K. "Type I allergy and indices of immune response in patients with ulcerative colitis." Wiad Lek 1993;46(13-14):496-501.

Vanderhoof, Jon A, Young, Rosemary J. "Use of Probiotics in Childhood Gastrointestinal disorders". Journal of Pediatric Gastroenterology and Nutrition, Vol. 27, No. 3, p. 323-332, September1998.

Wolf, Douglas M.D. "Nutritional Deficiencies in IBD: Causes of Malnutrition." The Crohn's And Colitis Chronicle, Winter 1996 issue, published by CCFA's Georgia Chapter.

Yamada, Tadataka, Alpers, David H., Owyang, Chung, Powell, Don W., Silverstein, Fred E. Textbook of Gastroenerology. J.B. Lippincott Company, Philadelphia, Pennsylvania, 1995.

Biography

Laurel Garwin, NC, is a practicing nutrition consultant in the San Francisco Bay Area. She specializes in gastrointestinal disorders, food allergies, weight loss, diabetes, fibromyalgia, alcoholism, and depression. She may be reached for individual consultations at: lgarwin@gmail.com