36-47 owm0608 lambert · absorption of essential vitamins, minerals, ... ture search was conducted...

36 OstomyWound Management

FEATURE

Asurvey of the Fort Worth ostomy association

found the majority of the members are >65

years of age. Many have had their ostomies for

more than two decades.1 Thus, people who have had

significant bowel resections such as ileostomies,

ileoanal pull-throughs, continent diversions, and

colectomies are living long enough to have to deal

with some of the same degenerative diseases and con-

ditions commonly encountered by all older adults. Of

particular concern: Does living with an incomplete

intestine increase risk for age-related disabilities such

as osteoporosis?2

The intestine seems to adapt to surgery and resec-

tions. Generally, the physiology of vitamin and miner-

als (absorption from the resected intestine and subse-

quent use by the body) requires adequate nutritional

intake, including enzymes and specific hormones in

amounts sufficient to process the nutrients. Even with

as little as one third of the small intestine present, the

body continues to maintain adequate vitamin and

Does Intestinal Resection Affect theAbsorption of Essential Vitamins,Minerals, and Bile Salts? An Overview of the LiteratureGeraldine M. Lambert, RN, DBA, CWOCN

As the number of persons living long lives following ostomy and bowel resection surgery increases, so do their questions aboutthe effect of surgery on chronic conditions commonly associated with aging. The literature was reviewed to evaluate currentevidence about the effect of bowel resection on the absorption of vitamins and minerals and related health concerns such asosteoporosis, gallstones, and renal calculi. Present knowledge about the process of vitamin and mineral absorption in theintestine and clinical study results suggest that chronic inflammation and corticosteroid use may adversely affect absorption.In general, a history of bowel resection does not appear to increase the risk of developing osteoporosis, gallstones, or renalcalculi and the body can adjust to losing significant sections of intestine. Strategies to help prevent the majority of long-termcomplications should be encouraged, including monitoring hydration and transit time, consuming low-digestible carbohy-drates, and avoiding processed foods as well as agents with chelating properties.

KEYWORDS: ostomy, nutrient absorption, osteoporosis, gallstones

Ostomy Wound Management 2008;54(6):36–47

Ms. Lambert is an enterostomal therapy nurse, JPS Health Network, Fort Worth, Tex. Please address correspondence to: GeraldineM. Lambert, RN, DBA, CWOCN, 320 Fossil Rock, Azle, TX 76020; email: [email protected] or [email protected].

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June 2008 Vol. 54 Issue 6 37

mineral stores as long as the patient maintains a

healthy diet.3 However, loss of the distal ileum and

colon can affect bile salt production. Changes in

nutritional absorption have been found to cause

higher numbers of gallstones among patients who

have short bowel syndrome than among the normal

population.4 Calcium-related renal stones also are

more common among persons with significant

reductions in bowel length secondary to increased

transit time of effluent, which results in dehydration

and concentrated urine output.5

Clinicians, caregivers, and patients need to know

whether significant changes resulting from bowel

resection increase the risk of osteoporosis, gallstones,

and renal stones in persons with a stoma. Because

mineral absorption in people with ostomies was a

concern of the members of the Fort Worth Chapter

of the United Ostomy Association (UOA), a litera-

ture search was conducted to determine if intestinal

resection with loss of significant portions of the

intestine can affect absorption of vital nutritional

elements. The most productive searches resulted

from using the word calcium in combination with

Crohn’s or inflammatory bowel and yielded English-

language articles published between 1989 and 2007;

most involved retrospective research. The literature

search focused on the anatomy of the intestine, the

physiology that affects mineral and bile salt absorp-

tion, and whether intestinal resection can result in

latent deficiencies of essential vitamins and minerals.

The results of the literature search, first pre-

sented to the UOA Fort Worth chapter

members, are summarized to help clinicians

optimize care of all persons with a stoma.

Anatomy and FunctionThe intestinal tract comprises the stom-

ach, the small intestine, and the large intes-

tine or colon. Alcohol, some medications,

and simple carbohydrates are absorbed

directly from the stomach. Each section of

the intestine is responsible for the absorp-

tion of a particular nutritional element.

Small intestine. The small intestine in the

adult is approximately 22 feet long and con-

sists of the duodenum, the jejunum, and the

ileum. The small intestine wall is arranged in folds of

absorptive cells and villi. Most nutrient absorption

occurs in the small intestine,6 including minerals, vita-

mins, proteins, and fats. Iron, calcium, magnesium,

and zinc are absorbed almost immediately after leav-

ing the stomach — ie, in the 8 feet of the duodenum

and the jejunum. Sugars and vitamin C, as well as thi-

amin, riboflavin, pyridoxine, and folic acid, are

absorbed in the upper third of the small intestine.

Protein is absorbed approximately midway through

the ileum. Vitamins A, D, E, and K, fats, and choles-

terol are absorbed in the lower third of the ileum.

Vitamin B12 is absorbed just before the small intestine

joins the large intestine. Bile salts are reabsorbed in the

distal ileum and the ascending colon.3

Large intestine. The large intestine (colon) is

responsible for reabsorption of water, sodium, potas-

sium, and vitamin K. However, retrospective studies

have shown that the large intestine also is responsible

for absorption of small amounts of calcium and mag-

nesium. Ohta et al7,8 injected magnesium and calcium

directly into the large intestine of rats through a cecos-

tomy tube. Calcium, magnesium, and phosphorus lev-

els in the feces, urine, and femur were measured by

spectrophotometer; it was found that a small amount

of calcium and magnesium was absorbed by the large

intestine and absorption amounts increased slightly

when oral ingestion of the minerals was withheld.

Absorption. Immediately following removal of

portions of the small and large intestines, the body

KEY POINTS• In industrialized countries, population life expectancy as well as life

expectancy of persons with a history of bowel resections andstoma surgery has increased substantially.

• To help answer questions and prepare new patients for a long lifeafter stoma surgery, the authors reviewed the process of vitaminand mineral absorption and available information regarding threecommon long-term concerns among ostomy patients.

• In general, the body appears to adapt very well — especially ifpatients adopt simple dietary strategies to help prevent long-termcomplications.

Ostomy Wound Management 2008;54(6):36–47


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experiences problems with absorption. Disrupted

release of enzymatic secretions and an unusually rapid

increase in the gastric emptying account for the mul-

tiple loose stools that occur with new resections.9

Depending on the portion of intestine removed, the

patient may need at least 1 year for the bowel to return

to normal function. The bowel stabilizes because the

proximal portion of the ileum has a greater capacity

for absorption than the distal portion.

A person can lose up to one half of the distal ileum

and still maintain a normal diet; digestion and

absorption of nutrients occurs basically within the

first 100 cm of jejunum.3 A review of the literature3

has shown that once the patient with an ostomy is

consuming regular food, the small intestine expands

and lengthens slightly to increase absorption. After

approximately 1 year, most people with ostomies are

able to control the consistency of the effluent and

absorption of most of the needed nutrients returns

to normal. Total parenteral feedings do not produce

the increase in ileum circumference and do not pro-

mote increased reabsorption.

Minerals. Three major factors affect mineral

absorption: the solvency of the mineral, transit time,

and the intestine’s ability to absorb the nutrient. Other

factors that can affect the absorption of nutrients

include emotional stress,10 chronic diarrhea, oral

antibiotics, and corticosteroids.

The cilia that line the small intestine are responsi-

ble for nutrient absorption. The bacterial flora found

in the intestine breaks down nutrients.11 Emotional

stress is known to have a destructive effect on the cilia

and antibiotics can destroy the normal flora.

Destruction of the cilia and the flora results in copious

amounts of diarrhea. Diarrhea increases transit time

and reduces the absorption of nutrients. Diarrhea also

can be the result of loss of intestinal tissue, medica-

tions (eg, sorbitol-containing products), diet, and

chronic malabsorption of nutrients.11 Antidiarrheal

medications should be taken only on physician rec-

ommendation and are contraindicated in persons

with colitis and other infectious diarrheas.12 Klein and

Jeejeebhoy11 recommend loperamide to reduce transit

time related to mechanical diarrhea because it is

metabolized quickly by the liver, making it available

faster than codeine and diphenoxylate.

Physical impairments to absorption. The cecal

valve prevents backflow of stool into the small intes-

tine, slows transit time into the large intestine, and

prevents bacteria in the large intestine from contami-

nating the effluent in the ileum. Loss of the cecal valve

complicates the absorption process. Overgrowth of

bacteria from the large intestine increases the destruc-

tion of vitamin B12 and iron and hampers carbohy-

drate and protein metabolism. The lack of nutrient

absorption secondary to an incompetent cecal valve

results in abdominal pain and loose stools.11

Diarrhea secondary to increased transit time is

common immediately after surgery and, for ileostomy

patients, can be an on-going problem. Persons with

ileostomies are known to suffer from chronic poor

absorption of nutrients, putting them at increased risk

for dehydration. Depending on the amount of small

intestine surgically removed, loose watery stools and

increased transit time can reduce the absorption of

fats, proteins, and vitamins. Because vitamin B12 is

absorbed at the lowest portion of the small intestine,

persons with an ileostomy and urostomy also are at

greater risk for the development of pernicious anemia.

Ileostomy and urostomy patients should talk to their

physicians about periodic testing for vitamin B12 defi-

ciency.13 Starting oral food intake and maintaining a

well-balanced diet are extremely important in pre-

venting loss of minerals and other nutrients.

Medications. Corticosteroids have multiple effects

on the body’s metabolism. Long-term steroid use is

known to cause thinning of the bone and the skin.

Moreover, steroids decrease absorption of vitamin A

through the gut, which can be especially detrimental

to wound healing. There is some evidence in the liter-

ature,14 as well as clinician experience, to suggest that

patients with chronic non-healing wounds who are on

steroid therapy may benefit from a vitamin A com-

pound placed directly into the wound.14

Other medications that affect absorption (especial-

ly of vitamins A, D, E, K, and B12) include cholestyra-

mine and other bile acid-binding resins.4 Selected

diuretics increase calcium, magnesium, potassium,

and zinc excretion in urine. Prednisone decreases cal-

cium absorption. Sulfasalazine decreases folic acid

absorption.11 Deficiencies in folic acid can result in

mucosal changes in the intestinal lining.


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Calcium AbsorptionThe chemical absorption of calcium through the

gut and the use of calcium to produce bone minerals

are complicated processes. Calcium absorption is

dependent on magnesium levels, vitamin D levels,

proteins, and parathyroid levels. The parathyroid

hormone regulates the amount of calcium absorbed

from the intestine and the amount of calcium lost

from the bones.15 This hormone also affects vitamin

D levels, which actively stimulate the absorption of

calcium.16 Calcium absorbed through the intestine

binds with the protein calbindin. All of these ele-

ments have to be present in adequate amounts to

maintain bone strength.

Certain medications — particularly aluminum-

containing antacids — affect calcium absorption,

binding to the calcium; if used for prolonged periods,

they contribute to bone thinning.7 In terms of solven-

cy, calcium citrate is more easily absorbed that calci-

um carbonate.15

Abnormal acid-base balances also affect blood lev-

els of calcium and magnesium. Cloutier and Barr18

proposed a theory regarding acid-base balance — ie,

high protein diets increase the amount of calcium lost

through the kidneys. The researchers reviewed multi-

ple studies and suggested that changes in protein

ingestion (either increasing or decreasing the intake)

affected acid-base balance of the body, subsequently

affecting calcium absorption. A (Japanese) retrospec-

tive study7 involved fructooligosaccharides (simple

carbohydrates and sugars) that appear to enhance fer-

mentation in the intestine, lowering the pH in the

intestinal tract and stimulating increased passive and

active mineral transport of magnesium and calcium.

Influence of magnesium and parathyroid func-tion. Several studies indicate that 20% to 50% of chil-

dren with insulin-dependent diabetes (IDDM) have

significant bone loss. The defining factor appears to be

low magnesium levels. In a study by Saggese et al,19 23

children with IDDM were told to eat various concen-

trations of magnesium and calcium. Serum levels of

parathyroid hormone, magnesium, calcium, and vita-

min D were compared over a 60-day period.

Fructosamine levels also were measured and remained

stable. Magnesium was shown to be the catalyst that

controlled absorption levels, playing an essential role

in enzyme activity related to cellular metabolism.20 No

correlation was made between children and adults

with diabetes because the amount of calcium needed

varies by age.21

Determining the calcium balance. Calcium bal-

ance is the difference between the ingestion of dietary

calcium and dermal, fecal, and urinary losses of calci-

um. The simplest way to assess mineral levels involves

blood samples. However, normal lab values in the

plasma are not conclusive, given the body’s capacity to

maintain a normal equilibrium.19 The body will main-

tain normal plasma levels by pulling the minerals it

needs from any available source, including bone.

Therefore, plasma levels may be normal while bone

density is decreased.22 Adding the measurement of

fecal calcium increases the accuracy by determining

the loss of minerals secondary to malabsorption.2

Body mass indices, bone scans, bone density indices,

and dual-energy x-ray absorptiometry (DEXA; two-

view, low-dose radiation exposure x-rays of the lower

spine and hips) provide increasingly accurate bone

health information.2

Conditions Related to Malabsorption Osteoporosis. Osteoporosis is a disease charac-

terized by thinning of the bones. Fractures fre-

quently occur in the spine, pelvis, and long bones.

Osteoporosis has long been associated with

menopause because low estrogen levels result in

increased bone reabsorption.2 However, the current

theory is that bone strength is established during

young adulthood. If bone strength is not maximized

during these critical years, a higher likelihood exists

for fractures as a part of the natural aging process.23

Age-related osteoporosis is the result of both exces-

sive bone reabsorption and defective bone formation.

Magnesium and calcium, as well as zinc and copper,

absorption changes with age. Magnesium and calcium

intake by the elderly has been reported to be far below

recommended dietary levels. Low zinc levels can affect

protein absorption, which has an indirect effect on

calcium levels. Low copper levels also affect bone

strength through collagen depletion.21

Crohn’s Disease (an inflammatory bowel disease)

and bowel resection with or without stoma forma-

tion, have long been associated with osteoporosis


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and increased potential for fractures.24,25 However, the research on

the relationship and causes of osteoporosis in persons with these

conditions has been inconclusive. The prevalence of osteoporosis

depends on the population studied; in patients with inflammatory

bowel disease, it has been reported to range between 12% and 44%26;

according to 2007 US statistics from the National Osteoporosis

Association, 55% of persons 50 years of age and older are at risk. Van

Hogezand25 reviewed a number of studies relating to intestinal dis-

ease and osteoporosis. Results indicated that fewer than 50% of sub-

jects had decreased bone density, either in the form of osteoporosis

or osteopenia.

Although steroids are known to cause thinning of bone, patients

with inflammatory bowel disease have been known to show signs of

bone thinning even before beginning steroid treatment. In a study27

of 32 men, 22 to 32 years of age, newly diagnosed with inflammato-

ry bowel disease and evaluated before receiving corticosteroid ther-

apy, nine (28%) were found to have decreased bone mass. The study

concluded that patients with low body mass and inflammatory

bowel problems for more than 6 months are at greater risk for bone

mass loss.

Van Hogezand et al28 have conducted extensive research related to

Crohn’s disease. One retrospective study involved 146 patients (61

men, 85 women; mean age of 43 years) with Crohn’s disease (mean

duration 20 years) who were receiving a variety of therapies includ-

ing corticosteroids. Among participants, 66% had undergone ileum

resection. According to the authors, “ileum resection was the most

predictive factor for osteoporosis: RR3.84 (CI 1.24–9.77, P = 0.018),

followed by age: RR1.05 (CI 1.02-1.08, P <0.001).” However, follow-

ing a review of seven studies,2 a definite relationship between bowel

disease, bowel resection, chemical treatment, and loss of bone mass

could not be established. Nevertheless, frequent bone mass assess-

ments in patients with inflammatory bowel disease, Crohn’s disease,

and intestinal resection, as well as those undergoing steroid therapy,

are recommended.2 A healthy diet during the young adult years may

help prevent late life bone health complications.

In a review of the literature, Lee et al29 conclude that bone loss is

related to a combination of factors that include the disease itself and

associated inflammation, high-dose corticosteroid use, weight loss

and malabsorption, a lack of exercise and physical activity, and an

underlying genetic predisposition to bone loss.

Kung et al30 discuss the concept that osteoporosis is genetically

related. According to the authors, women in Hong Kong generally

have a low average calcium intake of <500 mg/d. A study evaluated

25 women with low bone density who had experienced vertebral

fractures, 25 age-matched post-menopausal women without frac-

tures, and 15 healthy pre-menopausal women. Over a 6-month



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period, four distinct phases of increased (600-mg

and 1,200-mg supplements) and decreased (300-mg

and 500-mg supplements) calcium ingestion were

monitored. Calcium levels were assessed through

blood and urine samples during each phase of the

study. Bone mineral density (BMD) was measured

by dual-energy X-ray. The study concluded that

intestinal calcium absorption was not significantly

different between pre- and post-menopausal

women. Although the researchers found lower plas-

ma vitamin D levels and higher urinary calcium lev-

els among the older female population, the final

conclusion of the research team was that osteoporo-

sis is genetically determined — that female mem-

bers of osteoporotic families have a significantly (P

<0.05) altered bone turnover response to acute

changes in calcium intake. Subsequently, the net

balance in bone turnover was significantly (P

<0.005) lower than that of the healthy control sub-

jects (P <0.05). An important part of the study con-

cluded that calcium absorption through the small

intestine is not affected by increasing the calcium

dosage or absorptive ability of calcium by the gut.

Gallstones. Production of bile acids for the

breakdown of nutrients is another complicated

chemical process, involving at least 12 enzymatic

steps to convert cholesterol to bile acids. The

process is controlled by multiple factors, including

nutritional status and the condition of the digestive

system. Bile production starts with the presence of

food in the stomach. As soon as the stomach emp-

ties, the gall bladder releases bile into the small

intestine. Bile salts combine with amino acids, cho-

lesterol, fat-soluble vitamins, lipids, and metal ions

(eg, iron and calcium) as they travel through the

small intestine and the ascending large intestine.31

At various times in the digestive process, bile salts

are conjugated (soluble) and unconjugated (insolu-

ble). The majority of bile salts are reabsorbed in the

distal end of the small intestine. A small amount of

the bile salts are absorbed in the ascending large

intestine. In normal intestinal tracts, only a mini-

mum of bile salts is lost through feces and the

process is so efficient that very little bile is lost from

the blood supply. The same bile salts are re-

processed by the liver and excreted back into the

gall bladder, on average, between three and 12 times

a day. Although considered very rare, short bowel

syndrome and hemicolectomy involving the ascend-

ing colon can affect the re-absorption of bile salts.17

One study documented a high prevalence of gall-

stones following colectomy in a sample of dogs.32

Ten dogs were subjected to proctocolectomy and

over a 12-week postsurgical period, bile and serum

were collected. Seven dogs developed gallstones.

The study concluded gall stone formation was the

result of increased unconjugated (water insoluble)

bilirubin in the gall bladder bile. When the distal

ileum and colon were removed and the bilirubin

could not be reabsorbed, the liver increased the pro-

duction of insoluble bilirubin from five- to 20-fold,

providing the basis for increased gallstone produc-

tion. The researchers also found increased acid lev-

els and increased ionized calcium in the bile of the

colectomized dogs.

Bile salts also affect the absorption of water and

the production of mucus to lubricate feces. Bile acid

diarrhea results from malabsorption of bile salts,

increased fluid loss, increased bacterial activity in

the large intestine, and increased lipid and choles-

terol loss through the intestine. Conversely, chronic

constipation can result from excessive absorption of

bile salts, fluid, and loss of mucus. Finally, reduced

bile salt production affects the absorption of fats

and fat soluble vitamins, leading to chronic malnu-

trition. Calcium salts also may precipitate out and

not be absorbed into the system. In mild cases, bile

acid secretion may be normal in the morning

because of replenished reserves during the night but

decreases as the day progresses.17

Renal stones. A 20-year retrospective study5

involving 1,941 patients with renal stones included

patients who had Crohn’s disease, ulcerative colitis,

ileal bypass, ileal resection, and total colectomy.

Study results indicated that patients with bowel

issues have less urine output secondary to increased

intestinal transit time. The increased concentration

of urine was a factor that contributed to stone for-

mation. Increased transit time also led to a mildly

acidic state that increased the excretion of magne-

sium and calcium into the urine. A review33 of four

cases involving three colectomies and one ileal



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resection describes the complex nature of chronic

inflammatory processes, low urine volume, and

increased acid balance as the source of increased

occurrence of renal stones. Thus, calcium supple-

ments should be taken with food to enhance proper

absorption and reduce the potential for calcium to

enter the kidneys and form kidney stones.7

Lifestyle StrategiesTransit time. Slowing transit time gives the

intestine more time to absorb fluids. Diet is a major

educational focus for persons with increased transit

time of fecal effluent. Healthy eating usually

becomes a way of life for people with Crohn’s

Disease, inflammatory bowel disease, diverticulitis,

or stomas. The need to prevent blockages and diar-

rhea is a major concern.25

Probiotics. Probiotics34 are live micro-organisms

that are beneficial for improving intestinal flora. Six

major types are found in the intestine; of the six, aci-

dophilus (Lacto-bacillus) is probably the best known

although not the most effective. Lacto-bacillus appears

to help prevent colitis. The authors suggest that Lacto-

bacillus might be beneficial in Crohn’s Disease, active

pouchitis, and some other inflammatory bowel dis-

eases. Yogurt, milk, and active yeast products also pro-

vide live anaerobic bacteria to the gut. Saccharomyces

boulardii has been shown to reduce antibiotic-induced

diarrhea.35 Persons with severely compromised immune

systems should consume probiotics with care because

an overgrowth of intestinal bacteria can occur.36

Low-digestible carbohydrates. Low-digestible car-

bohydrates (example: Nutriose FB™, Roquette,

Lestrem Cedex, France) have many beneficial effects,

especially on energy intake, digestive physiology, and

mineral absorption as well as an ability to reduce

intestinal transit time.37 The drawback of these low-

digestible carbohydrates is increased flatulence.

Vermorel et al37 studied 10 healthy men for 31 days to

determine the effects of adding low-digestible carbo-

hydrates to their diets. The researchers found that

adding 50 g DM/day of low-digestible carbohydrates

to the subjects’ diets reduced transit times without

causing gastric distress.

Sports drinks, on the other hand, contain high

concentrations of sugars that can increase transit

time. Chemically balanced liquids specifically

developed to replace electrolytes (eg, Pedialyte™,

Abbott Labs, Abbott Park, Ill) are the better choice

for rehydration.12 Other healthy foods include

wheat flour, rice bran, olive oil, anti-oxidants, and

raw fruits and vegetables. Green leafy vegetables are

a good source of magnesium. Sunshine is a good

source of vitamin D.12

DiscussionCurrent research suggests that living with an

incomplete intestine does not in and of itself

increase the likelihood of developing osteoporosis.

Calcium, magnesium, and vitamin D are absorbed

immediately after leaving the stomach. The amount

of calcium absorbed is determined by the parathy-

roid hormone and varies as people age. Bone

growth is at its peak in young adulthood. Exercise

and good nutrition are vital to enhancing bone

strength.4 However, because the parathyroid utilizes

only the amount of calcium it needs, taking mega-

doses of calcium and other minerals results in

excretion of excess calcium through the stool, not

absorption.22 The small intestine has a remarkable

ability to stretch and lengthen to provide greater

surface area for absorption. However, this only

occurs on an oral diet. Tube feedings and total par-

enteral nutrition do not accomplish the same goal.3

Acid balance, hormone levels, and proper diet all

work together to maintain normal mineral absorp-

tion. Avoiding processed foods and therapeutic

agents with chelating properties can prevent most

trace element deficiencies.12

Bone thinning appears to be more related to

lifestyle, chronic inflammatory processes, and

heredity than to intestinal issues. Intestinal resec-

tion in people with normal eating habits and nor-

mal effluent output should not be at any higher risk

for vitamin and mineral deficiencies than individu-

als with normal bowel function.31

Similarly, gall stone formation related to intestin-

al dysfunction is rare and generally only occurs as a

complication of short bowel syndrome.17 A survey

done by the Fort Worth chapter of the UOA1 found

that out of 125 members only three had both an

ileostomy and a history of gall bladder surgery.



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Renal stones related to intestinal malfunction are

a result of dehydration, usually secondary to

increased transit time of effluent. Adequate fluid

intake and slowing transit time reduces the risk of

developing renal stones.34

Conclusion Having an ostomy does not necessarily increase

risk for osteoporosis. Osteoporosis appears to be

related to heredity. People with a family history of

osteoporosis should be tested periodically for bone

mass. Nutrition, lifestyle, and exercise appear to be

the important factors relating to vitamin and min-

eral absorption and bone health for people with

stomas. Good nutrition during young adulthood

when bone growth is rapid provides bone mass in

later life. Persons with decreased intestinal capacity

should be able to maintain healthy body functions

by eating properly, exercising, and taking medica-

tions as prescribed. - OWM

References1. Membership files. Ostomy Support Association. Fort

Worth, Tex. Accessed February 2008.2. Engstrom P. Good to the bone. Cure.

2007:6(6):50–56.3. Westergaard H, Spady D. Short bowel syndrome. In:

Sleisenger M, Fordtran J, ed. Gastrointestinal DiseasePathophysiology/Diagnosis/Management, 5th ed.Philadelphia, Pa: W.B. Saunders Co;1993:1249–1257.

4. Hofmann AF. The enterohepatic circulation of bileacids in health and disease. In: Sleisenger M,Fordtran J, ed. Gastrointestinal DiseasePathophysiology/Diagnosis/Management, 5th ed.Philadelphia, Pa: W.B. Saunders Co;1993:127–150.

5. Trinchieri A, Lizzano R, Castelnuovo C, Zanetti G,Pisani E. Urinary patterns of patients with renalstones associated with chronic inflammatory boweldisease. Archivio Italiano di Urologia.2002;74(2):61–64.

6. Bryant R, Hampton B. Anatomy and physiology ofthe gastrointestinal tract. Ostomies and ContinentDiversions Nursing Management. St. Louis, Mo:Mosby Year Book; 1992:265–292.

7. Ohta A, Ohtuki M, Takizawa T, et al. Effects of fruc-tooligosaccharides on the absorption of magnesiumand calcium by cecectomized rats. Int J VitaminNutrition Res. 1994;64(4):316–323.

8. Ohta A, Baba S, Ohtsuki M, et al. In vivo absorptionof calcium carbonate and magnesium oxide from the

large intestine in rats. J Nutri Sci Vitaminology.1997;43(1):35–46.

9. Meyer JH. Chronic morbidity after ulcer surgery In:Scharschmidt BF, ed. Gastrointestinal DiseasePa t h o p h y s i o l o g y / D i a g n o s i s / M a n a g e m e n t .Philadelphia, Pa: W.B. Saunders Co;1993:731–758.

10. Kani T, Miki C, Tonouchi H, Akehi Y, Ono J. Urinaryexcretion of deoxypyridinoline increases after gas-trointestinal surgery. Nutrition. 2003;19(9):747–753.

11. Klein S, Jeejeebhoy K. Long-term nutritional man-agement of patients with maldigestion and malab-sorption. In: Scharschmidt BF, ed. GastrointestinalDisease Pathophysiology/Diagnosis/Management.Philadelphia, Pa: W.B. Saunders Co;1993:2048–2058.

12. Gorbach S. Infectious diarrhea and bacterial foodpoisoning. In: Scharschmidt BF, ed. GastrointestinalDisease Pathophysiology/Diagnosis/Management.Philadelphia, Pa: W.B. Saunders Co;1993:1128–1173.

13. Athanasiadis S. Restorative protocolectomy with anileal pouch. Functional and biochemical results.Langenbecks Archiv fur Chirurgie.1993;360(3):207–220.

14. Falanga V, Eaglstein W. Away from the ulcer area. In:Leg and Foot Ulcers. St. Louis, Mo: Mosby;1995:9.

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