Page 41 – Practical Gastro

It is recommended that adult patients with portal hypertension (PH) undergo screening for varices, especially in order to prevent the complication of variceal hemorrhage. There is variably in PH management in children, often due to complicating factors such as a child’s smaller size. Capsule endoscopy, specifically the esophageal capsule (EC) that captures images on both ends of the capsule at a rapid frequency, has been used to assess for esophageal varices in adults. Although EC has no therapeutic ability, it can screen for variceal formation in patients without the requirement of anesthesia. Minimal data on EC use in children with portal hypertension is available, and the authors performed a single-center, retrospective study to assess the capability of EC for variceal screening in a specific pediatric population with PH.

A 12-year chart review occurred to identify children with a diagnosis of PH who had underwent screening using EC. Patients had to be able to swallow an EC, and children with prior abdominal surgery or pacemaker placement were excluded. Three models of EC capsules (PillCam ESO, PillCam ESO2, and PillCam UGI Capsule made by Given Imaging Ltd, Yoqneam, Israel/Medtronic) were utilized. After a patient swallowed the EC by standard protocol, esophageal varices were described in regards to esophageal location (proximal, mid, or distal esophagus) and size (small, medium, or large). The electronic medical record was reviewed on each included patient to determine various aspects including testing indications for PH as well as medication use. The clinical status for each patient was defined as compensated cirrhosis, decompensated cirrhosis (cirrhosis with complications such as ascites, encephalopathy, variceal hemorrhage, or hepatopulmonary syndrome), noncirrhotic portal hypertension, cardiac cirrhosis (such as from congenital heart failure), and suspected PH.

A total of 98 patients were included in the study (57.1% male), and 146 completed EC studies were performed. The average age at the time of EC was 16 years with a median interquartile range of 13.7 – 18.5 years. Compensated cirrhosis was present in 57% of patients; noncirrhotic portal hypertension was present in 19.5% of patients. EC was used as a screening modality in 66.5% of studies and for surveillance for known varices in 33.5% of patients. No portal hypertension changes were seen in 74 EC studies, and 64 EC studies demonstrated variceal formation (59 esophageal, 17 gastric, 6 duodenal). Other findings included blood flecks (23% of studies), erosions (22.5%), portal gastropathy (18.1%), esophagitis (14.5%), heterotopic tissue (9.4%), scarring from prior ligation (12.3%), and ulcer formation (3.6%). Most identified varices were in the esophagus (59 studies), specifically in the distal esophagus (56 studies), and most varices were described as small (40 studies). The authors noted that 12 of the EC studies led to new medication use while 11 esophagogastroduodenoscopies were performed as a result of EC studies (mostly esophageal variceal band placement). Finally, a total of 4 patients had an episode of GI bleeding within 1 year of their EC study; however, none of these patients had a bleeding event due to missed findings on EC.

This study demonstrated that EC is an effective screening and surveillance tool for varices in children with portal hypertension. The safety of EC use makes it a potential quick tool for determining variceal formation, and it has the potential to be used for screening / surveillance in children who cannot tolerate anesthesia.

^{Pai A, Jonas M, Fox V. Esophageal capsule endoscopy in children and young adults with portal hypertension. Journal of Pediatric Gastroenterology and Nutrition. 2019; 69: 641-647}

^{John Pohl, M.D., Book Editor, is on the Editorial Board of Practical Gastroenterology}

NUTRITION ISSUES IN GASTROENTEROLOGY, SERIES #196

ORS: The Solutions to Optimize Hydration in Short Bowel Syndrome

Elizabeth Wall

Short bowel syndrome is a rare disorder characterized by malabsorption and dehydration. The degree of fluid and electrolyte losses will depend on the condition, length, and sites of remaining intestine. Recognition of the need for hydration in this population is imperative to prevent long term consequences of kidney injury. Home IV hydration therapy is possible, though expensive and laborious, and can result in undue burden to patients. Oral rehydration therapy is a non-invasive and relatively inexpensive alternative to maintain hydration in some patients. The question remains, who will benefit from oral rehydration (ORS)? This article will focus on assessment of hydration status in patients with short bowel syndrome, identification of patients who may benefit from ORS, and it will provide guidelines for the use of ORS.

INTRODUCTION

Short bowel syndrome (SBS) is a rare disorder characterized by malabsorption and dehydration after extensive surgical resection of the small bowel (SB); the resection may also include part or all of the colon.¹ The degree of malabsorption and fluid loss will depend on length, location, and condition of the remaining SB, and the presence or absence of not only the ileocecal valve, but more importantly, the colon as well. Small bowel length < 200 cm and/or ostomy effluent > 1.5L/d will result in malabsorption of nutrients, fluid, and electrolytes, and therefore defines SBS ^(2-4), although Medicare defines SBS as < 150 cm.⁵

Under normal conditions the intestinal tract secretes 6-7 L of fluid daily, reabsorbing virtually all, in addition to the 1-2 L of ingested fluid.⁶ After SB resection, patients have net losses of fluid and electrolytes; those without a colon will have an even greater net loss. Negative fluid balance can develop soon after surgery and progress rapidly to dehydration and acute kidney injury necessitating medical attention and fluid resuscitation.⁷ Some patients will “survive” in a state of chronic dehydration, without overt signs of kidney injury, but over time negative fluid balance can lead to nephrolithiasis and chronic kidney injury.^8,9 Long term parenteral support (PS) can replace electrolyte losses and prevent dehydration, but it is associated with serious risks such as infection and injury to central blood vessels, not to mention the impact on lifestyle and healthcare expenses.10 The long term goal for hydration management is to optimize enteral intake and reduce need for PS. Oral rehydration solutions (ORS) can help achieve this goal for many.

Intestinal resections disrupt neuroendocrine hormone signaling to the gastrointestinal tract and related organs.² The dysregulation of postprandial hormone responses affects motility and absorption. It is not uncommon for SBS patients to have rapid gastric emptying (dumping) of hypo- or hypertonic chyme into the SB. The proximal SB reacts to this by secreting sodium or water to adjust the luminal fluid concentration to isotonicity, thus increasing the total volume of fluid needing to be absorbed.² Water absorption across the SB epithelium is dependent on a sodium-glucose cotransport system; sodium and glucose molecules are transported together across the SB epithelium, dragging along water molecules.6,11 The ileum is more efficient than jejunum in reabsorbing water, but many with SBS have little or no ileum. Table 1 lists the expected daily volume of ostomy/stool output.^3,11

Oral rehydration solutions were developed to utilize the sodium-glucose co-transport system and are found to be effective in many patients with SBS.¹² The ideal solution contains 20-40 g (5-10 teaspoons) of sugar and 90-120 mEq sodium/L (1 teaspoon of salt = 104mEq of Na).¹³ The concentration of sodium makes these solutions unpalatable; therefore commercially available ORS products contain slightly less sodium to improve taste without loss of effectiveness. Pediatric ORS contain lower concentrations of both glucose and sodium. Table 2 lists ORS products commercially available in the United States.^14,15

Assessing Hydration Status in SBS

Accurate assessment of hydration status is imperative when considering ORS therapy, however the typical indicators of dehydration may not be accurate in SBS. The kidneys work to preserve blood volume despite total body water depletion from excessive gastrointestinal losses of sodium and water; serum sodium and blood urea nitrogen to creatinine ratio can remain normal until the patient is severely dehydrated.^12,16 Common signs of dehydration can be factitious in SBS including: deep yellow urine from multivitamin ingestion, muscle cramps from hypomagnesemia, and dry mouth from narcotic-based anti-motility or other medications. Physical exam with attention to clinical signs of dehydration (dry mucus membranes, skin tenting, dry or peeling skin) in conjunction with a downward spiral of serial weights, 24 hour volume of urine and ostomy/stool outputs, and spot urine sodium concentration are all helpful to assess true hydration status in this population.¹⁷ Table 3 lists physical signs of dehydration commonly experienced by SBS patients. Adequate hydration is indicated by urine volume > 1200mL/day and spot urine sodium > 20 mEq/L.¹⁷

Patient Selection

Many patients with SB ostomy, or those with only a small portion of colon in continuity, may benefit from ORS therapy; those with most of their colon usually do not need ORS to maintain hydration. Ideal candidates have insatiable thirst and drink large volumes of water (hypotonic fluids) without relief, have low urine volume and escalating ostomy/stool output. Patients who can accurately measure and track their weight, PS/enteral/oral intake, and output (urine and ostomy/stool) to determine efficacy of ORS are more likely to be successful with the therapy. If the patient has an ostomy, measurement of the pouch volume will help ease data collection by simply counting the number of times it is emptied in 24 hours; however actual measurement of the volume with a canister with ounces or mL marked on the outside is better, at least initially.

Using Oral Rehydration Solutions

In combination with anti-motility medications and strict adherence to recommended meal patterns, ORS can facilitate fluid absorption, but it will not necessarily decrease ostomy/stool output.17 Patients should start by sipping a low volume of ORS, 500-750mL/d, to gain acceptance to the taste, learn how to sip between meals throughout the day, all the while ensuring consumption of ORS does not worsen their hydration status (by driving their stool/ostomy volume too high to keep up). If ORS therapy leads to increased urine volume, irrespective of ostomy/stool output, then it can be considered effective. Patients can then gradually increase their consumption to 1-3 L/d while continuing to monitor their hydration. However, if stool/ostomy output increases without an increase in urine output, then ORS therapy is not effective and it should be discontinued, and the patient may require PS to maintain hydration and protect kidney function. Table 4 identifies keys factors for ORS success.

Some patients will try to consume ORS by gulping the daily volume, “just to get it down.” Rapid ingestion of ORS can cause dumping into the SB, exceeding its absorptive capacity, resulting in increased unabsorbed effluent into the ostomy appliance or colon. It is important to train patients to slowly sip ORS throughout the day for maximum absorption. In patients with enteral feeding access, slow infusion of ORS overnight via a pump has proven to be effective in maintaining hydration and weaning from PS.¹⁸

Long term adherence to ORS regimens is often poor due to unpalatable flavors and the expense of commercially prepared products.¹⁹ To overcome these barriers patients can mix their own solutions and reserve use of commercial ORS for times when self-preparation is not feasible (traveling). Recipes for homemade ORS are listed in Table 5.^14,15 It must be emphasized that these recipes are designed with specific balance between sugars and sodium for optimal absorption. Inaccurate measurement of ingredients or enhancing ORS with additional water, ice, juice or sugar-containing flavorings will alter the sodium to carbohydrate ratio making the beverage less effective. Non-nutritive flavorings and sweeteners (e.g., Crystal Light®, Zero Sugar Sunkist®, Kool-Aid Liquid Drops®, or Water Drops™) can be added without altering the sodiumcarbohydrate ratio; use of these products will help to prevent taste fatigue and maintain intake. Compliance improves when clinicians encourage creativity with ORS consistency and temperature such as freezing in ice cube trays, mixing with plain gelatin, and using a thermos to maintain warm or cool temperatures throughout the day.

Success of ORS therapy can be dependent on a patient’s access to proper tools for mixing of ORS ingredients and equipment to monitor their hydration status (Table 6). When trialing or adjusting daily volume of ORS the patient should record daily weight and 24 hour intake (including ORS) and output measurements (see Table 7). These data will help the patient and clinician ascertain whether or not ORS is an effective therapy for that patient.

Other Fluids

What about fluids other than ORS? Sugary or hypertonic fluids (soda, sweet tea, juice, fruit drinks, flavored coffees) will rapidly pass into the jejunum where water will be secreted into the SB lumen to dilute the chyme to isotonicity. Likewise, consumption of hypotonic fluids (plain water, diet soda, plain tea or coffee, dilute juices) leads to jejunal secretion of sodium (and water) to adjust the chyme to isotonicity. Both scenarios increase ostomy/stool output and result in net fluid and sodium losses. In the case of patients who are unable to tolerate, or refuse to drink ORS, the next “best” fluid options are hypotonic fluids that contain lower amounts of carbohydrate and sodium compared to ORS (e.g., G2 Gatorade® or Powerade® [not the “zero calorie” variety]). Electrolyte powders and waters such as Trioral Oral Rehydration Salts® and Propel Electrolyte Water® are sugar free and can be sipped while snacking on small portions of saltystarchy snack foods like pretzels, soda crackers, potato or corn chips. Small volumes (4-8 oz.) of these fluids or plain water are generally tolerated with meals. Caffeine and alcohol act as diuretics and can exacerbate dehydration in SBS. As discussed above, sports and electrolyte drinks contain the wrong proportions of carbohydrate and sodium and therefore are not considered ORS. Oral nutrition supplements (e.g., Boost® or Ensure® and store bought equivalents) are high in sugar and low in sodium, leading to water and sodium losses with increased stool/ostomy output. These supplements should not be offered to those with SBS or high volume ostomy output.

CONCLUSION

Maintaining hydration is a chronic issue for SBS patients. Although PS is available for most patients, it is associated with high costs, health risks and lifestyle burden. Oral rehydration therapy can be a viable option to reduce or eliminate the need for PS for many with SBS. To maximize benefits from ORS, it is essential that patients receive education and ongoing support from a knowledgeable provider. Patients must have proper tools to prepare the ORS and ability to self-monitor their response to sipping ORS throughout the day. Creativity and experimentation with flavors and consistency can improve acceptance and adherence to the therapy. Although ORS is not effective for all patients, in those with benefit, transition from PS to ORS will reduce risks of iatrogenic complications and overall healthcare expense, while permitting a more normal lifestyle

References

^{1. Jeppesen PB. Short bowel syndrome: Definition, classification, etiology, epidemiology, survival, and costs. In: DiBaise JK, Parrish CR, Thompson JS. Eds. Short Bowel Syndrome: Practical Approach to Management. CRC Press, Boca Raton, FL 2016;1-13.
2. Nightingale J. Short bowel syndrome: Anatomical and physiological considerations. In: DiBaise JK, Parrish CR, Thompson JS. Eds. Short Bowel Syndrome: Practical Approach to Management. CRC Press, Boca Raton, FL 2016;29-40.
3. Nightingale J, Woodward JM. Guidelines for management of patients with short bowel. Gut. 2006;55(suppl 4):iv1-iv12.
4. Buchman AL, Scolapio J, Fryer J, et al. AGA technical review on short bowel syndrome and intestinal transplantation. Gastroenterol. 2003;124(4):1111-1134.
5. Allen P. Medicare Coverage for Home Parenteral Nutrition – An Oxymoron? Part I. Prac Gastroenterol. 2016;Dec(12):34-50.
6. Barrett KE. Water and electrolyte absorption and secretion. In: Barrett KE. ed. Gastrointestinal Physiology, 2e New York, NY: McGraw-Hill; 2014. http://accessmedicine.mhmedical.com/content.aspx?bookid=691& sectionid=45431395. Accessed January 16, 2020.
7. Banerjee A, Warwicker P. Acute renal failure and metabolic disturbances in the short bowel syndrome. Q J Med. 2002;95:37-40.
8. Lauverjat M, Aissa AH, Vanhems P, et. al. Chronic dehydration may impair renal function in patients with chronic intestinal failure on long-term parenteral nutrition. Clin Nutr. 2006;25:75-81.
9. Bridges M, Nassar R, Parrish CR. High Output Ileostomies: The Stakes are Higher than the Output. Prac Gastroenterol. 2019;Sept (9):20-33.
10. Winkler MF, Hagan E, Wetle T, et al. An exploration of quality of life and experiences of living with home parenteral nutrition. JPEN J Parenter Enteral Nutr. 2010;34(10):395-407.
11. Parrish CR, DiBaise J. Part 3: Hydrating the adult patient with short bowel syndrome. Prac Gastroenterol. 2015;Feb(2):10-18.
12. Beaugerie L, Cosnes J, Verwaerde F, et al. Isotonic high-sodium oral rehydration solution for increasing sodium absorption in patients with short-bowel syndrome. Am J Clin Nutr. 1991;53:769-772.
13. Nightingale JMO, Lennard-Jones JE, Walker ER, et al. Jejunal efflux in short bowel syndrome. Lancet 1990;336:765-768.
14. Parrish CR, Ross V. Hydration and SBS in Adults Patient Handout. https://www.nmpgdpg.org/members/ page/digid-resources. Accessed January 19, 2020.
15. Parrish, CR. A Patient’s Guide to Managing a Short Bowel, 4th Edition. Intouch Solutions, Overland Park, KS; June 2016:1-66. Available at: no cost at: www.shortbowelsyndrome.com/sign-up
16. Blalock BE, Parrish CR. Maintaining hydration in the short bowel patient. In: DiBaise JK, Parrish CR, Thompson JS. Eds. Short Bowel Syndrome: Practical Approach to Management. CRC Press, Boca Raton, FL 2016:145-153.
17. O’Neil M, Teitelbaum DH, Harris MB. Total body sodium depletion and poor weight gain in children and young adults with an ileostomy: A case series. Nutr Clin Pract. 2014;29(3):397-401.
18. Nauth J, Chang CW, Mobarhan S, et. al. A therapeutic approach to wean total parenteral nutrition in the management of short bowel syndrome: Three cases using nocturnal enteral rehydration. Nutr Reviews. 2004;62(5):221-231.
19. Hurt RT, Vallusmsetta N, Varayil JE, et al. Piolet study comparing 2 oral rehydration solutions in patients with short bowel syndrome receiving home parenteral nutrition: A prospective double-blind randomized controlled trial. Nutr Clin Pract. 2017;32(6):814-819.}

FROM THE PEDIATRIC LITERATURE

Transnasal Endoscopy for Children with Eosinophilic Esophagitis

Currently, the best way to perform disease monitoring in eosinophilic esophagitis (EoE) is through direct visualization of the esophageal mucosa with biopsy via esophagogastroduodenoscopy (EGD). Repeat EGDs requiring sedation can be a potential risk in children, and the authors of this study evaluated the alternative use of transnasal endoscopy (TNE) to monitor disease in children with EoE. The authors of this study looked at a protocol of monitoring EoE in children in which the patients were given a web-based video to watch prior to the procedure. The patients did not eat or drink 2 hours before the procedure. During TNE the patients wore either movie goggles or virtual reality movie goggles. Topical lidocaine or aerosolized benzocaine was applied orally and intranasally. A small bronchoscope or endoscope (size range 2.8 mm to 4.9 mm outer diameter) was placed transnasally based on the patient’s nasal passage size, and esophageal biopsies were obtained via forceps placed through a 1.2 mm or 2 mm operating channel depending on the size of the bronchoscope or endoscope used. Patient demographics, procedure number, completion rate, type of endoscopy, and adverse events were recorded.

There were 300 TNE attempts recorded over a 3-year period, and 294 TNEs were performed successfully (98%). The study population consisted of 190 patients (age range 3 to 22 years). Both operating channel sizes were used throughout the age range. Throughout the 3-year study, the average number of TNE procedures increased every year (48 in 2015; 131 in 2017), and time from procedure check-in to discharge decreased by a small amount as well (maximum time 79 minutes which decreased to 71 minutes by the end of the study period). The total percentage of endoscopies for EoE that were performed via TNE increased as well (15.7% in 2015 to 31.8% in 2017). In 2018, the average cost for TNE with biopsy for EoE was $4393 while the average cost for EGD with biopsy for EoE was $9444.33 (a 53.4% reduction in cost using the transnasal approach). All biopsies obtained by TNE were adequate for examination by a pathologist. Adverse events were rare and only consisted of interventions that included telephone management, reassurance, and supportive care.

This study demonstrates that TNE with video goggles is a safe and effective diagnostic technique to perform in children with EoE. The ability to obtained esophageal tissue with no sedation and with an associated reduction in healthcare costs provides the possibility to expand the use of this procedure throughout pediatric healthcare systems.

^{Nguyen N, Lavery W, Capocelli K, Smith C, Deboer E, Deterding R, Prager J, Leinwand K, Kobak G, Kramer R, Menard-Katcher C, Furuta G, Atkins D, Fleischer D, Greenhawt M, Friedlander J. Transnasal endoscopy in unsedated children with eosinophilic esophagitis using virtual reality video goggles. Clinical Gastroenterology and Hepatology. 2019; 17: 2455-2462.}

^{John Pohl, M.D., Book Editor, is on the Editorial Board of Practical Gastroenterology}

A CASE REPORT

Colonic Adenocarcinoma Masquerading as a Pork Bone

Megan Willard

We present a patient with acute onset of abdominal pain and colonic obstruction occurring soon after eating a pork sandwich. Imaging was suggestive of a colonic obstruction related to a foreign body, likely a bone fragment. Ultimately, the patient was found to have a calcified colonic adenocarcinoma masquerading as a foreign body. Case reports have been written about foreign bodies masquerading as colonic tumors, but here we present a case of a colonic tumor masquerading as a foreign body.

INTRODUCTION

Intra-abdominal calcifications seen on imaging are usually benign, and do not portend significant pathology. Gastrointestinal tumors rarely have calcifications within the primary tumor, and occasionally calcification can be seen in a gastrointestinal tumor metastases. Calcifications within tumors of the gastrointestinal tract, when seen, are usually in association with a mucoid or mesenchymal tumor, but not in adenocarcinoma, as in this case. Herein, we report a case of a primary colonic adenocarcinoma with calcifications that resembled a bone fragment in a patient with an acute bowel obstruction.

Case Report

A 62-year-old male presented to the emergency department (ED) with diffuse abdominal pain, worst in the left lower quadrant, and constipation for the past 48 hours. The pain waxed and waned and was worsened by eating. He noted that his symptoms started soon after eating a BBQ pork sandwich. He was discharged from the ED with a diagnosis of constipation and a prescription for laxatives, but within 24 hours his pain worsened and he returned. At this time, he also complained of nausea and inability to tolerate oral intake. He noted that at baseline his stools were always normal in caliber and consistency, and that he had no new medications or dietary changes. On physical examination, his blood pressure was 167/101 mmHg, heart rate 88, and he was afebrile with normal oxygen saturation. He appeared uncomfortable but non-toxic. Abdominal exam revealed a distended and diffusely tender abdomen, with guarding but no rebound tenderness. On auscultation there were high-pitched, tinkling bowel sounds. Rectal exam revealed scant brown stool. Laboratory studies revealed a slightly elevated white blood cell count at 10.5 K/mcL, an otherwise normal complete blood count, and normal basic metabolic and liver enzyme panels. Computed tomography (CT) of the abdomen and pelvis with oral and intravenous contrast demonstrated focal colonic narrowing at the junction of the descending and sigmoid colon, with associated thickening and pericolonic stranding. A curvilinear 4 cm density presumed to be a foreign body, possibly a pork bone, was located at the proximal aspect of this narrowed segment (Arrow, Image 1). Surgery was performed. At laparotomy the proximal colon was severely dilated with no evidence of necrosis or perforation. No foreign body was noted; however, a sigmoid mass was palpated and a resection was performed. Pathology revealed a calcified invasive well-differentiated T3N1a colonic adenocarcinoma with tumor deposits in the mesenteric fat.

Discussion

Many case reports have been written about foreign bodies masquerading as colonic tumors, but here we present a case of a colonic tumor masquerading as a foreign body. This patient’s history of the acute onset of symptoms, so close in proximity to a meal which potentially contained a bone, and the CT scan which revealed a curvilinear density, which very much appeared to be a bone of some type, made foreign body ingestion and subsequent obstruction high on the differential. Ultimately, it was determined that the curvilinear density seen on CT scan represented calcification within the tumor. Intra-abdominal calcifications seen on imaging are usually benign.^1,2 Calcifications within tumors of the gastrointestinal tract are infrequent,^2,3 and when seen are usually in association with a mucoid or mesenchymal tumor, but not in adenocarcinomas, as in this case.^2,4 Calcifications associated with colonic adenocarcinomas are more frequently observed in the metastases of the colonic primary, especially in the liver, which occurs in 12-27% of cases.⁴ More frequently, calcifications are seen in more slow growing tumors. The pathophysiology of this process is unknown but is thought to be attributed, in part, to devitalized tissue or mucin within the tumor creating a more alkaline environment which allows for precipitation of phosphate and carbonate salts.^1,4 A few case reports exist in the literature of calcifications within colonic tumors, with the first case being reported in 1954.² These calcifications were described as small and punctate, or arranged in stippled fashion, and overwhelmingly, the histopathology revealed mucoid carcinoma, not adenocarcinoma.³ Our patient’s calcification more closely resembled a curvilinear foreign body. In summary, we present an unusual case of acute colonic obstruction with imaging suggestive of a foreign body, perhaps a bone, which ultimately was diagnosed as calcified colonic adenocarcinoma.

^{References
1. Chen YG, Kao WY, Tsai SH. Nonspecific but Significant. Am J Med. 2012 May;125(5):461-4.
2. Fletcher B, Morreels J, Christian W, Brogdon B. Calcified Adenocarcinoma of the Colon. Am J Roentgenol. 1967 Oct;101(2):301-5.
3. Engel S, Dockerty M. J Calcifications and Ossification in Rectal Malignant Processes. JAMA. 1962; 179(5): 347-350.
4. Chang SL, Lin CP, Lee RC. Calcification of Liver Metastases in a Colon Cancer Patient Following Chemotherapy with 5-fluorouracil: A Case Report. Chin J Radiol 2002; 27:73-77.}

FRONTIERS IN ENDOSCOPY, SERIES #60

Clinical Update on the Role of EUS in Pelvic Abscess

Gandhi Lanke,

Douglas G. Adler

The role of Endoscopic ultrasound (EUS) as a tool for drainage of pelvic abscess is emerging. With the advent of stenting and drainage catheters, EUS-guided drainage of pelvic abscess has become more feasible. The understanding of pelvic anatomy is key in the technical success of EUS-guided pelvic abscess drainage. Surgical drainage of pelvic abscess should be the last option when computer tomography (CT), ultrasound (US) or EUS fail to achieve the drainage of abscess. This review article focuses on the role of EUS in pelvic abscess drainage.

INTRODUCTION

EUS-guided drainage of pelvic abscess is evolving as an alternative to percutaneous or surgical methods of drainage. Pelvic abscess can occur as a result of diverticulitis, ischemic colitis, inflammatory bowel disease, perforated appendicitis, pelvic inflammatory disease, or secondary to post-surgical complications from low anterior rectal resection or total abdominal hysterectomy (among other surgeries).^1-4 Pelvic abscess drainage poses challenge as they are surrounded by the bony pelvis, neurovascular structures, as well as the bladder, bowel, uterus, vagina, prostate and rectum. EUS guided drainage can be an alternative option when percutaneous methods of drainage are not amenable because of lack of adequate and safe window for access to the abscess.

Etiology and Pathogenesis

Pelvic abscesses are usually polymicrobial in etiology and contain a mixture of aerobic, anerobic and facultative microorganisms. The most common microorganisms isolated from pelvic abscess include aerobic gram-positive cocci (group B streptococci, enterococci, and staphylococcal species), aerobic gram-negative bacilli (Escherechia coli, pseudomonas, klebsiella pneumonia and proteus species), anaerobic grampositive cocci (peptococci and peptostreptococci species), anaerobic gram-negative bacilli (Bacteroides and Prevotella species) and grampositive facultative anaerobe (actinomyces species).^5-7

The development of postoperative pelvic abscess is dependent on complex interaction between host defense mechanisms and the bacterial inoculum. In females, the ascending route of normal bacterial flora from the vagina and cervix plays an important role in the development of pelvic abscess.⁵ Microbial contamination of the surgical field also plays a key role in the post-operative development of pelvic abscess.⁶

Clinical Presentation and Diagnosis

The common symptoms include lower abdominal pain, with or without fever and chills, nausea and vomiting.⁶ Patients can also present with septic shock, altered mental status along with hypotension, tachycardia and tachypnea.⁶ On physical exam, the abdomen/pelvis is often tender and rigidity or guarding may be present when there is peritonitis.⁸ A fluctuant mass may be palpable.8 Laboratory findings include leukocytosis with left shift, elevated erythrocyte sedimentation rate (ESR) and C-reactive protein (CRP).⁹ Routine blood cultures should be obtained before the administration of antibiotics. All patients should undergo a dedicated computed tomography (CT) or magnetic resonance imaging (MRI) of pelvis to determine the size, extent, proximity to Gastrointestinal (GI) lumen and to assess if it is uniloculated or multiloculated abscess before the endoscopic ultrasound (EUS).^8,10 Transvaginal ultrasound may be useful in female patients with suspected tubo-ovarian abscess and history of pelvic inflammatory disease (PID).¹¹

Management

Most authors agree that pelvic collections greater than 3 cm with suspected infection should be drained.⁸ Antibiotics in combination with drainage of pelvic abscess have led to decreased rates of surgical intervention, especially in patients with large pelvic abscess greater than 5cm.¹² Pelvic abscess can be drained by various techniques like ultrasound (US), CT-guided percutaneous, surgical and EUS-guided drainage. The choice of drainage technique depends on the size, type of collection, location of the abscess, services available, and experience of the operator.⁸ US-guided technique is easy to perform, inexpensive and no radiation. US-guided drainage of the pelvic abscess is possible only when the abscess is within the reach of ultrasound probe.¹³ However, sometimes with US it becomes difficult to visualize deep collections in pelvis due to body habitus and the air acoustic barrier created by interposed small or large bowel.8 CTguided percutaneous drainage has better spatial resolution, better access to pelvic collections and better detection of adjacent structures.8 However, CT-guided drainage of pelvic abscesses can be challenging in deep pelvic collections because of surrounding anatomy and vascular structures.¹³ Also, CT-guided pelvic drainage can be more painful with transvaginal or trans gluteal route as the drainage catheters will be left in place.¹³ Unlike EUS-guided pelvic abscess drainage, there is no scope for transmural stent placement with CT-guided drainage, necessitating the placement of uncomfortable and potentially painful drainage catheter for long duration.^13,14 EUS has several advantages when compared to other techniques which include drainage of pelvic abscess under real time sonographic guidance, intervening blood vessels and nerves can be avoided, provides access to abscess cavities which do not cause luminal compression and aids in establishing an alternative diagnosis in a small subset of patients.¹⁵

Procedure

Proper selection of the patient is very important as there is a high chance of therapeutic failure and risk of perforation whenever there is multiloculated pelvic abscess with size less than 4cm, located at the level of dentate line, immature wall without a rim, rectocele, J pouch, perianal abscess and location of the abscess 2 cm away from the EUS transducer.^1,15Prophylactic antibiotics should be administered if the patient is not already on antibiotics. To avoid the risk of bleeding during the procedure, laboratory abnormalities including coagulopathy and thrombocytopenia should be checked and corrected if abnormal before the procedure. The bladder should be empty, or foley catheter should be inserted before the procedure as there is a risk of bladder puncture and often missing the small pelvic fluid collections with distended bladder.¹⁶ Bowel preparation prior to the procedure can minimize contamination of the abscess with stool and aids in better visualization of the abscess.¹⁶ The procedure can be performed under conscious sedation or general anesthesia.^1,13

Technique

A curved linear echoendoscope is used to locate the abscess and color doppler helps to identify and thus avoid any intervening vasculature. The linear echoendoscope has the advantage of visualization of the needle while performing the procedure. However, with the radial echoendoscope (which may be used to identify the target abscess), therapeutic intervention is not possible.¹⁷ The linear echoendoscopes available in USA include the FG 38UX (Pentax Precision Instruments Corp., Orangeburg, NY, USA), the EG 38UT (Pentax Precision Instruments Corp., Orangeburg, NY, USA), and the GF-UCT140/180 (Olympus Medical System Corporation, Center Valley, PA, USA). Both the EG 38UT and the GF-UCT 140 allow placement of a 10 F stent and they have working channels of 3.8 and 3.7 mm, respectively.¹⁵ With the FG 38X, it only permits placement of an 8.5 F stent and has a working channel of 3.2 mm.15 Once the abscess is located, a 19-guage fine needle aspiration (FNA) needle (Wilson-Cook, Winston-Salem, NC, USA) can be used to puncture the abscess cavity.1The abscess is then aspirated and, if desired, fluid can be sent to microbiology for culture and sensitivity to optimize the antibiotic treatment.¹⁷ Some practitioners skip this step as the fluid is usually polymicrobial in nature. Normal saline with 10-20 milliliter (ml) can be used to irrigate the FNA needle, if needed,as it can be clogged from mucosa or debris and to evacuate as much pus as possible.15 A 0.035” guide wire is then passed in to the abscess cavity under EUS and/or fluoroscopic guidance. Once the guide wire is in place, the transmural tract is sequentially dilated over the guide wire using a 5 F endoscopic retrograde cholangiopancreatography (ERCP) canula and a 6-15 mm over the guide wire biliary balloon dilator can also be used to further dilate the tract.^15,17 Alternatively, a needle knife can also be used to puncture the abscess cavity after the FNA needle is withdrawn, followed by leaving a Teflon catheter in the abscess cavity after the metal part of the needle knife is withdrawn from the abscess cavity.¹⁷ Giovannini introduced a one-step drainage of pelvic abscess after the needle is withdrawn using the NWOA system (Cook Endoscopy® WinstonSalem, NC, USA). NWOA system consists of a 0.035-inch needle-wire suitable for cutting current, a 5.5F dilator and an 8.5 or 10 F stent preassembled on the same catheter.¹⁷

After the tract is dilated, straight or double pigtail stents are deployed in the abscess cavity under fluoroscopic guidance, usually 2 or more stents if plastic stents are used.15 After the deployment of first stent, an ERCP cannula preloaded with the guide wire is passed adjacent to the first stent into the abscess cavity under fluoroscopic guidance to deploy second stent. A 10 F transrectal catheter can be deployed adjacent to the stent especially when the pelvic abscess size is large to aid in better evacuation of the abscess.1 The transrectal catheter exits the anus and it can be secured to the gluteal region with the tape. The transrectal catheter can be irrigated with normal saline periodically until the aspirate is clear.¹

Alternatively, fully covered self-expanding lumen-apposing metal stents (LAMS) can be used as tools for access and drainage of pelvic abscesses.18 LAMS (AXIOS and AXIOS- EC; Boston scientific, Marlborough, MA) are available in 3 sizes (lumen diameter x length; 10×10 mm, 10×15 mm, and 10×20 mm).19 The stent is available in electrocautery enhanced (hot) and nonelectrocautery enhanced (cold) versions. Under EUS guidance, the constrained stent is delivered in to the abscess cavity and the distal flange is deployed.20 The proximal flange is deployed under endoscopic ultrasound, or fluoroscopic guidance. Using a through-the scope balloon dilator, the stent lumen can be immediately dilated to the LAMS diameter if so desired.18 Dilation aids in immediate apposition of the tissues, maximizes initial drainage, and if required allows direct access for debridement.18 The enhanced-electrocautery LAMS can also be used to deliver the catheter in to the abscess cavity without prior dilation of the tract as it has the capability of application of electrocautery at the distal tip of the device introducer by means of cautery ring.21 Advantages include easy deployment system, a saddle-shaped design that decreases migration risk and decreases the risk of stent clogging with fecal matter. Also, a larger inner stent diameter allows better drainage of pelvic abscess without the need for drainage catheter and if needed allows direct endoscopic debridement by passage of standard gastroscope through the stent lumen.^18,22,23 A representative EUS-guided pelvic abscess drainage is illustrated in Figure 1.

DISCUSSION

Results of studies that have evaluated outcomes of EUS-guided pelvic abscess drainage are shown in Table 1. Giovannini et al. evaluated the efficacy of EUS-guided transrectal aspiration and drainage of deep pelvic abscesses by using plastic stents (8.5-Fr, 10-Fr).²⁴ In this study, 12 patients with perirectal or pelvic abscess were evaluated using EUS. Three patients had aspiration only and two of these developed recurrences requiring surgery. Nine patients underwent transrectal stent placement and one patient with an abscess>8cm experienced incomplete drainage requiring surgery. No major complications occurred in this study. Poincloux et al. evaluated the long-term outcome of 37 patients who underwent EUS-guided drainage of perirectal and perisigmoid abscesses via plastic stents or LAMS.13 Four patients underwent needle aspiration, plastic stent placement in 29 and LAMS placement in 4 patients. Technical success (ability to drain the pelvic abscess under EUS guidance) was 100%, clinical success (complete resolution of the abscess with symptom relief on follow up CT in 4 weeks) was 91.9% and longterm success (abscess resolution without the need for surgery and recurrence after 12 months) was 86.5% respectively. Five patients required reintervention via EUS within 14 days, 1 patient required surgery and 1 patient received supportive care because of persistent abscess. Stents were removed after complete resolution of the abscess. LAMS were removed within 6 weeks and plastic stents were removed 3-6 months after placement. Complications included perforation (1 patient) and stent migration (1 patient).

Puri et al. evaluated the efficacy of EUS-guided pelvic abscess drainage without fluoroscopy in 30 (4 prostatic, 7 perisigmoid and 19 perirectal abscesses) patients.25 Five patients underwent only aspiration (3 perisigmoid and 2 prostatic abscesses), aspiration with dilation in 6 (2 perirectal, 2 perisigmoid and 2 prostatic abscesses) and dilation with stent placement in 19 (17 perirectal and 2 perisigmoid abscesses) patients. Technical success (ability to drain the abscess under EUS guidance) was 100%, treatment success (symptom relief with complete resolution of the abscess on follow up EUS or CT in 1-2 weeks) was 93.3% with no recurrence (need for repeat EUS-guided drainage within 90 days after the stent removal) of abscess during 6-60 months follow up. Five (2 with perirectal abscess had migration of stent requiring repeat stent placement, 1 with prostatic abscess required re-aspiration and 2 underwent only aspiration with perisigmoid abscess required surgery) patients required re-intervention. Ramesh et al. evaluated the outcomes of EUSguided transrectal (TR-27) and trans colonic (TC11) drainage of abdomino-pelvic abscesses in 38 patients.26 Technical success (successful placement of stents or drainage catheters in the abscess cavity) was 100%, treatment success (resolution of abscess on follow up CT at 2 weeks with symptom improvement) was 70% (trans colonic) and 96.3% (transrectal) respectively. There were no procedural complications. Repeat EUS drainage was performed in 4 (TC cohort-1 diverticular

phlegmon, TR cohort- 3 diverticular phlegmon) patients because of worsening symptoms. Four patients (TC cohort-3, TR cohort-1) required surgery after failed EUS-guided drainage. Patients with diverticular abscess had poor outcomes (25 % vs 97%) compared to other (post-surgical, ischemic colitis, perforated appendix, endocarditis, trauma and IBD) causes. There was no recurrence of abscess in patients with treatment success after a median follow up of 3.36 years. Meylemans et al. evaluated the efficacy and safety of EUS-guided (23) and surgical transrectal drainage (23) of pelvic abscesses in 46 patients.27 The success rate (no need for additional treatment or intervention with surgical/EUS or radiological) of EUS-guided vs surgical transrectal drainage was 83% and 48% respectively. Anastomotic leak occurred in 3 cases of EUS-guided and 9 cases of surgical transrectal drainage of pelvic abscesses. The mean duration of drainage in EUS-guided vs surgical transrectal drainage was 42 and 13 days respectively. The total length of stay for EUSguided vs surgical transrectal drainage was 24 and 20 days respectively. The total duration of follow up for EUS-guided vs surgical transrectal drainage was 261 and 301 days respectively. Varadarajulu et al. evaluated the rate of recurrence, complications, technical and treatment success of EUS-guided pelvic abscess drainage in 25 patients.1 All patients with abscess size less than 8cm underwent placement of one or two 7F transrectal stents and for abscess size 8cm or more, a 10F drainage catheter is placed in addition to transrectal stents. The drainage catheter is removed if the abscess size decreased by more than 50% on follow up CT after 36 hours and the decision to discharge the patient from the hospital is made. All stents were retrieved by sigmoidoscopy after a follow up CT at 2 weeks showed complete resolution of abscess. Technical success (ability to drain the abscess under EUS guidance) and treatment success (symptom relief with complete resolution of the abscess on follow up CT at 2 weeks) was 100% and 96% respectively. One patient with perforated diverticulitis had persistent abscess requiring surgery. The mean duration of hospital stay was 3.2 days and after a mean follow up of 189 days there was no recurrence of abscess in all 24 patients.

Zator et al. evaluated the efficacy of single step EUS-guided lavage and instillation of gentamicin antibiotic for drainage of pelvic abscesses in 6 patients.28

All patients underwent EUS-guided aspiration, equal volume sterile saline lavage and gentamicin instillation (40mg/ml). Four patients had complete resolution of the abscess on follow up CT. One patient with diverticular abscess had recurrent diverticulitis without abscess requiring surgery, 1 patient with diverticular abscess had decreased size (7.3 to 3.4 cm) permitting planned surgery and 1 patient with crohn’s disease had decreased supra-levator abscess size (6.5 x 3.5 cm to 2.5 x 0.5 cm) required surgery for persistent sinus tracts with anal narrowing.

CONCLUSION

EUS-guided pelvic abscess drainage is safe and effective in experienced hands. Multidisciplinary care by different physicians including surgery, gynecology, radiology, oncology and interventional gastroenterology is key in the effective management of pelvic abscesses. Aspiration with stent placement and drainage catheter is more efficacious than aspiration with stent alone, especially in larger pelvic abscesses. Diverticular abscesses are more prone to recurrence and timely management can prevent complications. Use of LAMS should be individualized based on the indications. These devices have advantages including decreased migration risk, less risk of stent clogging with fecal matter and a larger inner stent diameter allows better drainage of pelvic abscess without the need for drainage catheter. Close follow up with repeat imaging after the procedure is essential to recognize early complications. Prompt recognition and early referral to interventional gastroenterology when indicated can prevent invasive surgery.

^{References
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2. Bang JY, Varadarajulu S. Endoscopic ultrasound-guided transrectal drainage of a pelvic abscess following total abdominal hysterectomy. Eur J Obstet Gynecol Reprod Biol. 2012;164(1):113-114.
3. Puri R, Eloubeidi MA, Sud R, Kumar M, Jain P. Endoscopic ultrasound-guided drainage of pelvic abscess without fluoroscopy guidance. Journal of gastroenterology and hepatology. 2010;25(8):1416-1419.
4. Granberg S, Gjelland K, Ekerhovd E. The management of pelvic abscess. Best Pract Res Clin Obstet Gynaecol. 2009;23(5):667-678.
5. Soper DE. Bacterial vaginosis and postoperative infections. Am J Obstet Gynecol. 1993;169(2 Pt 2):467-469.
6. Jaiyeoba O. Postoperative infections in obstetrics and gynecology. Clin Obstet Gynecol. 2012;55(4):904-913.
7. Hadithi M, Bruno MJ. Endoscopic ultrasound-guided drainage of pelvic abscess: A case series of 8 patients. World J Gastrointest Endosc. 2014;6(8):373-378.
8. Robert B, Yzet T, Regimbeau JM. Radiologic drainage of post-operative collections and abscesses. J Visc Surg. 2013;150(3 Suppl):S11-18.
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10. Nguyen TL, Soyer P, Barbe C, et al. Diagnostic value of diffusion-weighted magnetic resonance imaging in pelvic abscesses. J Comput Assist Tomogr. 2013;37(6):971-979.
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12. To J, Aldape D, Frost A, Goldberg GL, Levie M, Chudnoff S. Image-guided drainage versus antibiotic-only treatment of pelvic abscesses: short-term and long-term outcomes. Fertil Steril. 2014;102(4):1155-1159.
13. Poincloux L, Caillol F, Allimant C, et al. Long-term outcome of endoscopic ultrasound-guided pelvic abscess drainage: a two-center series. Endoscopy. 2017;49(5):484490.
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16. Holt B, Varadarajulu S. Endoscopic ultrasound-guided pelvic abscess drainage (with video). Journal of hepatobiliary-pancreatic sciences. 2015;22(1):12-15.
17. Fernandez-Urien I, Vila JJ, Jimenez FJ. Endoscopic ultrasound-guided drainage of pelvic collections and abscesses. World J Gastrointest Endosc. 2010;2(6):223-227.
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19. Shah RJ, Shah JN, Waxman I, et al. Safety and efficacy of endoscopic ultrasound-guided drainage of pancreatic fluid collections with lumen-apposing covered self-expanding metal stents. Clinical gastroenterology and hepatology: the official clinical practice journal of the American Gastroenterological Association. 2015;13(4):747-752.
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A SPECIAL ARTICLE

Quality of Online Information About Irritable Bowel Syndrome

Ann Ouyang

Currently there are no studies evaluating web-based resources providing patient information about irritable bowel syndrome (IBS), a common condition with complex pathophysiology.

Aims: to assess the reliance of patients on the internet for medical issues and the quality of commonly viewed websites about IBS.

Methods: 198 patients were surveyed about using the internet for medical information and the most popular websites identified by their web searches for “irritable bowel syndrome” were evaluated for validity, readability, and content.

Results: although a large portion of respondents rely on the internet for medical information, the majority of online resources for IBS are not easily readable. Four of 14 are written at an eighth grade reading level or below. Of these, only two have a Content Score of over 60 out of 93. This analysis supports clinicians in taking an active role to assist patients in finding online resources to improve their understanding.

Introduction

Irritable bowel syndrome (IBS) is a common functional gastrointestinal disorder with an overall prevalence of up to 20% in the United States. Most patients with IBS are managed by primary care providers. However, the syndrome remains a challenge to diagnose due to both the
heterogeneity of clinical presentations and a lack of definitive diagnostic testing. The complex pathophysiology of IBS and the limited time that health care providers have to spend with patients in a single clinic encounter make it difficult to fully educate all patients in the outpatient primary care setting. These factors may result in many patients not fully understanding the condition, making them more likely to turn to alternate sources, including the internet.

With increased awareness of IBS by the public, patients are also more commonly self-diagnosing IBS based on their own symptoms.² In today’s technological age, more patients access and rely on the internet as a major resource when seeking medical information about themselves or others.3 Some studies also suggest that females use the internet more frequently than men for the purpose of obtaining health information.^4-7 IBS is much more commonly diagnosed in women8, making it especially important for online information about IBS to be of high quality.

While recent studies have evaluated internetbased resources for other common medical conditions,^9-12 there are no current studies that assess the quality of online information pertaining to IBS specifically. The purpose of our study was to identify the most commonly viewed online websites providing information about IBS and to assess their validity, readability, and relevance of content. We hypothesize that there are many online patient education resources on the topic of IBS and that these are of variable quality. With a thorough evaluation of current online information on IBS, providers taking care of patients with this syndrome can both be aware of and recommend the highest quality patient education materials to all patients using the internet as a major resource for improving their understanding of IBS.

METHODS

Patients visiting an outpatient gastroenterology clinic at an academic medical center were provided instructions to search “irritable bowel syndrome” on their smartphones or tablets and to voluntarily complete a survey to report their search results and answer a set of questions pertaining to demographics and internet use for medical information. Patients were asked to search using their own devices because online search engines customize search results based on an individual’s location and previous browsing history. All adult patients visiting the clinic were eligible for participation in the study. Specific exclusion criteria included age less than 18, lack of an Apple or Android device, or inability to properly complete the survey. The survey was cross-sectional in design and patients were recruited over a two-week period. Informed consent was obtained from each participant prior to beginning the survey. Study data were collected and managed using REDCap electronic data capture tools hosted at Penn State Health Milton S. Hershey Medical Center and Penn State College of Medicine.13 REDCap (Research Electronic Data Capture) is a secure, web-based application designed to support data capture for research studies, providing an intuitive interface for validated data entry, audit trails for tracking data manipulation and export procedures, automated export procedures for seamless data downloads to common statistical packages, and procedures for importing data from external sources. The study was approved by the researchers’ institutional review board.

Survey Instrument

The survey included five questions: age (organized by generation category; i.e. Millennial/Gen Y, Gen X, Baby Boomer, Mature), gender, highest level of education, and two questions about the use of and reliance on the internet for obtaining medical information. Finally, participants were asked to paste the link to their individual online search results for IBS. The complete survey instrument can be viewed in Figure 1. Results from the survey were tabulated and analyzed for trends.

Validity, Readability, and Content of Web-based Resources

Websites appearing on the first page of patient search results were noted. The 14 most frequently appearing websites from patient search results were individually scored by three researchers (L.L., N.A., L.G.) for validity, readability, and relevance of content. Results from each evaluator were averaged. Validity, as defined as the ability to trust an online resource’s information, was measured with the DISCERN (maximum score: 5) and Health on the Net (HON) tools. DISCERN is an online instrument supported by the National Health Services Executive Research and Development Programme that measures the reliability of medical information, including treatment options for conditions.¹⁴ It has three sections with 16 questions total. Though originally designed for print materials, DISCERN is viewed as an effective tool to measure the reliability of online medical information.¹⁵ The HON resource, a non-profit organization affiliated with the World Health Organization, is a measure of the quality, confidentiality, and transparency of websites.¹⁶ Online patient education websites can request certification by HON and, if specific criteria are met, this status can be indicated by an emblem displayed at the bottom of the website. A standardized tool was used to measure the readability of each online resource. The Flesch Reading Ease Score scale was originated by Rudolf Flesch and estimates the difficulty of reading passages in English.¹⁷ The Flesch-Kincaid Grade Level scale was adapted from Flesch’s original tool, initially used by the United States Navy.¹⁸ These scales measure readability based on word length, number of syllables, and sentence length. Flesch Reading Ease Scores typically span from 0 to 100, with lower scores indicating a greater degree of difficulty in reading by persons with a basic reading level. The Flesch-Kincaid Grade Level estimates the average school grade level matched to the Flesch Reading Ease Score. These tools are conveniently found in Microsoft Word; however, the calculable formulas for each of these scores is shown: Flesch Reading Ease Score = 206.835 – 1.015 x (words/sentences) – 84.6 x (syllables/words) Flesch-Kincaid Grade Level = 0.39 x (words/ sentences) + 11.8 x (syllables/words) – 15.59 Relevance of content was measured using a rubric developed by three of the researchers who specialize in the care of patients with functional gastrointestinal disorders (E.T., S.R., A.O.). The content scoring rubric was developed with reference to the Rome IV criteria.¹⁹ It contains a list of terms and phrases that are believed to be important for patients to know about IBS. The rubric includes pertinent IBS symptoms, disease mechanisms, differential diagnoses, components of the work-up, and management options. Items that were considered important received a score of 3, those that were felt to be useful but not critical information received a score of 2, and those that were factual but probably not important to patient understanding of the condition received a score of 1. The maximum score was 93. Each page’s patient education content about IBS was scored using this rubric. A sample of the Content Score rubric with point breakdown can be viewed in Figure 2

RESULTS

Trends in Internet Usage Among Survey Respondents 200 patients successfully completed the survey. Two were excluded due to age less than 18. Results of the survey, including demographic information, are displayed in Table 1 (N=198). 65% of the patients completing the survey were female. Nearly 40% of respondents did not have any educational degree beyond high school. When patients have questions regarding medical problems, 83% reported that they “always”, “often”, or “sometimes” use the internet, and 43% said that they use the internet as their main resource for obtaining medical information. A univariate logistic regression was performed (Table 2). This analysis reveals that there was a statistically significant (p <0.05) difference in the frequency of internet usage for medical information based on both age and gender. Compared to the 18-40 age group (Millennial/Gen Y), the age >70 group (Mature) relies on the internet for medical information significantly less frequently. Compared to males, females in the survey rely on the internet for medical information more frequently. Based on the regression results, there was no consistent statistically significant difference in frequency of internet use based on level of education.

Evaluation of Internet Resources

The 14 most commonly viewed websites on a search for IBS are shown in Table 3, along with their scores for validity, readability, and content for each website, sorted by the Content Score. Despite their presence on many patient search results, MedlinePlus and The Atlantic were excluded from evaluation because they were not formatted appropriately for analysis using the validated tools.

Results of Validity

7 of the 14 websites (50%) were certified by the Health on the Net (HON) foundation, as indicated by a visible emblem at the bottom of the page. Using the DISCERN rubric for validity, average scores for the websites ranged from 1.7 to 3.7 (out of 5). No website scored a 5 out of 5 using this rubric, primarily due to lack of detail about the exact sources of their information.

Results of Readability

No source evaluated was categorized as having “Easy” (>80) or “Fairly Easy” (70-79) readability according to the Flesch Reading Ease Score. Gastro. org, WebMD, the National Institute of Diabetes and Digestive and Kidney Diseases (NIDDK), and Womenshealth.gov scored highest with >60 on the Flesch Reading Ease Score (“Standard”). All other sites were “Fairly difficult” (50-59), “Difficult” (30-49), or “Very confusing” (<29). Table 3 also shows the Flesch-Kincaid Grade Level for each website, which is the average educational grade level required to comprehend the information contained on the webpage.

Results of Content

Only 2 sources scored an average of >70 out of 93 for the content score (Wikipedia, Medicinenet). 6 sources scored between 60-69 (NIDDK, Emedicinehealth, Patient.info, MayoClinic, Medicalnewstoday, and GI.org). A comparison of Flesch Reading Ease Score and Content Score for the websites is shown in Figure 3, organized into groups based on the established Flesch Reading Ease Score categories. The Pearson’s correlation coefficient (r) between Flesch Reading Ease Score and Content Score was -0.5 (95% CI: -0.80 to 0.06), suggesting a moderate negative association between the two variables. Given the sample size of 14 websites, this result was not statistically significant at the p < 0.05 level (p = 0.0691). In general, the higher the Content Score of the resource, the more difficult it was to read (lower Flesch Reading Ease Score).

DISCUSSION

The results of this study reveal that almost 50% of patients frequently use the internet as their main educational resource for obtaining medical information, consistent with results from prior studies.20 The results support the published data that women rely on the internet as a resource for medical information more often than men.4-7 Further, trends from this study show that older generations (those aged >70) rely less on the internet as a resource for medical information than other age groups. This older age group reported that they use their health care provider most often when seeking medical information. Our study suggests that the internet is a more valuable tool for younger generations who grew up with access to the internet, highlighting the need to provide the highest quality online resources for this growing subset of patients. High quality medical information requires accuracy and depth of content, and the information should be understandable to the patient. When evaluating individual websites from an online search on IBS, the validity, readability, and relevance of content on the website could be measured. Most online IBS resources scored similarly on measurements of validity using the DISCERN scale. Half of the websites were certified by HON. Of those websites not certified by HON, some may in fact meet HON criteria due to their association with major medical associations (e.g., the National Institute of Diabetes and Digestive and Kidney Diseases, the American Gastroenterological Association, and the American Society of Colon and Rectal Surgeons). As shown in Table 3, the highest scoring resources for readability include Gastro. org, WebMD, NIDDK, and Womenshealth. gov. The highest scoring resources for relevance of content include Wikipedia, Medicinenet, NIDDK, and Emedicinehealth. Figure 3 also shows a moderate negative association between Flesch Reading Ease Score and Content Score, indicating that, in general, as websites add more pertinent content about IBS to their education materials, the readability for the average patient declines. Though the correlation was not statistically significant at the level of p < 0.05 because of the sample size of 14 websites, investigating this relationship further with additional websites about IBS may be an avenue for additional research. Creators of online patient education materials should be cognizant of this balance and design websites that are easily readable by the public but still contain the most important content.

This evaluation of popular websites reveals that most online resources providing information about IBS have poor readability, particularly Wikipedia. Given that only 4 out of 14 websites are written at the grade level recommended by the American Medical Association for patient education resources (6th-8th grade),21 there is likely poor patient comprehension of most online resources about IBS. For example, despite having the highest Content Score, Wikipedia would not be recommended as an educational source for patients due to the very advanced grade level (“16th grade”, i.e. a graduate-level degree) required to comprehend the information. Most websites did not indicate if content was directed towards health care professionals or patients. Recognizing that patients frequently use the internet for medical questions unanswered in a clinic visit, health care providers can take a proactive role in directing patients to online resources that are valid, readable, and relevant. Figure 3 serves as a tool that providers can use when managing patients with IBS, by referring patients to higher quality and appropriate online patient education material. Ideally, this would be a resource at the very topright of Figure 3 (high readability, high content). In practice, designing such a website would be difficult. However, because each patient has a different level of education and reliance on the internet for seeking medical information, providers can use Figure 3 to tailor their recommendations for online resources about IBS based on the patient’s unique needs and background. For example, a highly educated patient may appreciate a site that is slightly less readable with more detailed content. Further research is needed to determine if tailoring internet resources for patients has a beneficial impact on patients’ understanding of their disease. This study is the only thorough evaluation of online information about IBS, an exceedingly common diagnosis in the United States. The study confirms what other studies have discovered about trends in internet usage for medical information. There are limitations to the study, including the Hawthorne effect: most patients completed the brief survey in the presence of a researcher, which may have influenced the way they responded to the questions about internet usage. Additionally, the DISCERN score and Content Scores were determined by three of the study’s researchers. However, these tools were designed to be objective to limit bias. The data presented indicate that most current online information about IBS is of variable quality. Primary care physicians managing IBS patients should use these results to take an active role in directing patients to credible online resources that have key disease information written in an easily readable format. Doing so may be able to increase patient understanding of disease, improve the doctor-patient relationship and, ultimately, improve health outcomes for patients.

Acknowledgements

The research team would like to acknowledge Vernon M. Chinchilli and Sandeep Pradhan for their contribution to the statistical analysis of the data. The project described was supported by the National Center for Advancing Translational Sciences, National Institutes of Health, through Grant UL1 TR002014 and Grant UL1 TR00045. The content is solely the responsibility of the authors and does not necessarily represent the official views of the NIH.

References

^{1. Canavan C, West J, Card T. The epidemiology of irritable bowel syndrome. Clin Epidemiol. 2014;6:71.}

^{2. Van den Houte K, Carbone F, Pannemans J, et al. Prevalence and impact of self-reported irritable bowel symptoms in the general population. United European Gastroenterol J. 2019;7.2:307-15.}

^{3. Stevenson FA, Kerr C, Murray E, Nazareth I. Information from the Internet and the doctor-patient relationship: the patient perspective–a qualitative study. BMC Fam Pract. 2007;8.1:47.}

^{4. Basch CH, MacLean SA, Romero RA, Ethan D. Health Information Seeking Behavior Among College Students. J Community Health. 2018;43.6:1094-9.}

^{5. Bidmon S, Terlutter R. Gender differences in searching for health information on the internet and the virtual patient-physician relationship in Germany: exploratory results on how men and women differ and why. J Med Internet Res. 2015;17.6:e156.}

^{6. Fox S. The social life of health information 2011. Washington, DC: Pew Internet & American Life Project; 2011.}

^{7. Rice RE. Influences, usage, and outcomes of Internet health information searching: multivariate results from the Pew surveys. Int J Med Inform. 2006;75.1:8-28.}

^{8. Lovell RM, Ford AC. Effect of gender on prevalence of irritable bowel syndrome in the community: systematic review and meta-analysis. Am J Gastroenterol. 2012;107.7:991.}

^{9. van der Marel S, Duijvestein M, Hardwick J, et al. Quality of web-based information on inflammatory bowel diseases. Inflamm Bowel Dis. 2009;15.12:18916.}

^{10. Zhang D, Schumacher C, Harris MB, Bono CM. The quality and readability of information available on the internet regarding lumbar fusion. Global Spine J. 2016;29.02:133-e8.}

^{11. Saeed F, Anderson I. Evaluating the quality and readability of Internet information on meningiomas. World Neurosurg. 2017;97:312-6.}

^{12. Lovett J, Gordon C, Patton S, Chen CX. Online Information on Dysmenorrhea: An Evaluation of Readability, Credibility, Quality, and Usability. J Clin Nurs. 2019.}

^{13. Paul A. Harris, Robert Taylor, Robert Thielke, Jonathon Payne, Nathaniel Gonzalez, Jose G. Conde, “Research electronic data capture (REDCap) – A metadata-driven methodology and workflow process for providing translational research informatics support,” J Biomed Inform. 2009 Apr;42(2):377-81.}

^{14. Charnock D, Shepperd S, Needham G, Gann R. DISCERN: an instrument for judging the quality of written consumer health information on treatment choices. J Epidemiol Community Health. 1999;53.2:105-11.}

^{15. Charnock D, Shepperd S. Learning to DISCERN online: applying an appraisal tool to health websites in a workshop setting. Health Educ Res. 2004;19.4:440-46.}

^{16. Health on the Net Foundation. [http://www.hon.ch]. Last accessed July 11, 2019.}

^{17. Flesch R. How to write plain English: A book for lawyers and consumers. New York, NY: Harper & Row; 1979.}

^{18. Kincaid JP, Fishburne Jr RP, Rogers RL, Chissom BS. Derivation of new readability formulas (automated readability index, fog count and flesch reading ease formula) for navy enlisted personnel. Institute for Simulation and Training 1975:56. [https://stars.library.ucf.edu/istlibrary/56]}

^{19. Drossman DA, Hasler WL. Rome IV—functional GI disorders: disorders of gut-brain interaction. Gastroenterology. 2016;150.6:1257-61.}

^{20. Diaz JA, Griffith RA, Ng JJ, Reinert SE, Friedmann PD, Moulton AW. Patients’ use of the Internet for medical information. J Gen Intern Med. 2002;17.3:180-5. 21. Weiss B. Health literacy. American Medical Association (2003).}

BOOK REVIEWS

Diagnosis and Management Guide for Anorectal Disease: A Clinical Reference

Justin C. Wheeler

Editor: Waqar Qureshi, MD

Publisher: SLACK Incorporated Publication

Year: 2020

ISBN-13: 978-1-63091-492-9 (paperback)

List Price: $119.95

Diagnosis and Management Guide for Anorectal Disease: A Clinical Reference, edited by Dr. Waqar Qureshi, was written to help address comprehensive training deficiencies in management of anorectal disorders in gastroenterology fellowship programs. Dr. Qureshi is Professor in the section of Gastroenterology and Hepatology at Baylor College of Medicine in Houston, TX, where he established an anorectal clinic and served as Chief of Endoscopy. The book was written by 28 contributing authors, most of which are gastroenterologists or surgeons working in the United States. Management of a broad spectrum of nonsurgical anorectal disease is covered, as well as underlying disease processes and management strategies of surgical topics for non-surgeons. This book was written for gastroenterology fellows and practicing gastroenterologists. Pediatric-specific topics are not addressed.

The succinct and easy to navigate 213page book is divided into four sections, with 17 total chapters. The sections are:
1) Anatomy and Examination
2) Benign Anorectal Conditions
3) Benign Soft Tissue, Perianal, Perineal, and Complicated Conditions, and
4) Neoplasms. Chapter topics include anatomy and physiology of the pelvic floor, hemorrhoids, anal fissures, anal pruritus, pilonidal disease, anorectal IBD management, defecations disorders, and anal carcinoma, among others.

Each chapter begins with bulleted key-points, and are broken into easy-to-read subsections such as pathophysiology, symptoms, diagnosis, and evidence-based treatment strategies. Chapters end with a comprehensive list of references. The book is written concisely and includes numerous tables, diagrams, color pictures, and treatment algorithms. Clinical management strategies for both common and rare conditions are covered, including frequently used medications and procedures. A particularly welcome inclusion are ideas on how to address real-world challenges facing clinicians, ranging from costly medications to minimizing side-effects of interventions. As the first comprehensive volume covering both conservative treatment and surgical strategies for anorectal diseases, this book would serve well as a desk reference for any trainee or practicing gastroenterology clinician. Inclusion of pediatricspecific topics may broaden the applicability of this well-written book.

Justin C. Wheeler, MD, FAAP

Assistant Professor of Pediatrics,

Division of Pediatric Gastroenterology

University of Utah

Primary Children’s Hospital

Salt Lake City, Utah

A CASE REPORT

Gastric Varices from Metastatic Ovarian Cancer with Splenic Involvement

Allyce Caines,Ghassan Allo,Yousuf Siddiqui

Left-sided portal hypertension (LSPH), also known as splenoportal hypertension, is a rare but life-threatening cause of upper gastrointestinal bleeding. LSPH often occurs in non-cirrhotic patients as a consequence of splenic vein obstruction. We present a case of isolated gastric varices due to mass effect on the splenic vein and likely tumor thrombus due to metastatic ovarian cancer.

INTRODUCTION

Portal hypertension refers to increased pressures in the hepatic portal system. This in turn leads to complications such as variceal hemorrhage from gastric or esophageal varices, ascites and hepatic encephalopathy. Upper gastrointestinal bleeding secondary to portal hypertension in the form of variceal hemorrhage is a recognized lifethreatening cause of gastrointestinal bleeding. In patients with gastrointestinal bleeding due to portal hypertension, bleeding from gastric varices is the cause in 5%-10% of patients.1 Increased resistance to portal flow due to a stiff, cirrhotic liver is often the cause of portal hypertension. However, portal hypertension can also be caused by isolated obstruction of the splenic vein, which is often referred to left sided portal hypertension (LSPH). LSPH accounts for less than 5% of all patient with portal hypertension1. Most of the reported cases of splenic vein obstruction have been the result of malignancy involving the spleen. Pancreatic disorders, including pancreatic carcinoma, acute and chronic pancreatitis, cysts, and pseudocysts which may block the splenic vein via thrombus formation or mass effect, are the most common causes of LSPH. These patients often have no known prior liver disease and have no evidence of cirrhosis on presentation. Bleeding can be catastrophic due to high portal pressures. In these cases, it is important to consider causes of left sided portal hypertension and the available treatment options.

Case Report

A 59 year-old female with a past medical history of metastatic ovarian cancer and obstructive uropathy, secondary to extrinsic compression, presented to her primary gynecologic oncologist with complaints of fatigue, lightheadedness and melena for one week. On laboratory evaluation, she was found to have a hemoglobin of 5.7 g/dL prompting emergency evaluation. Four years prior she was diagnosed with stage IIIC serous carcinoma of the ovary, at which time she underwent total abdominal hysterectomy, omentectomy, pelvic lymphadenectomy, tumor debulking and subtotal colectomy with diverting ileostomy followed by chemotherapy. She remained disease free for approximately nine months when imaging showed disease recurrence. She developed significant disease progression involving the splenic hilum, retroperitoneal lymph nodes and pelvis in addition to bilateral hydronephrosis. On presentation to the emergency department she was hemodynamically stable with unremarkable physical exam. An episode of hematemesis consisting of 500cc of bright red blood occurred in the emergency department with repeat hemoglobin of 4.5 g/dL. Endoscopy revealed type 1 isolated gastric varices (IGV1). She received a total of 6 units of packed red blood cells. The patient was then transferred for consideration of balloon retrograde transvenous obliteration (BRTO). Repeat endoscopy confirmed the findings of type 1 isolated gastric varices with red wale signs (Figure 2). BRTO, splenectomy, gastric vessel ligation and cyanoacrylate injection were discussed as potential therapeutic options. The patient had no further episodes of bleeding and her hemoglobin remained stable. Magnetic resonance imaging (MRI) revealed a hypovascular mass in the splenic hilum with minimal central enhancement concerning for metastatic disease. Areas of hypovascular nodularity around the lesion extending into part of the splenic vein at the hilum and branches were suggestive of tumor thrombus. Liver lesions concerning for metastatic disease were also present. On MRI the hepatic vein, celiac artery, hepatic artery, portal vein and superior mesenteric vein were patent. The splenic artery appeared tortuous and the splenic vein was engorged. The patient was not a candidate for BRTO due to the lack of portosystemic collaterals. She underwent splenic artery embolization to decrease inflow to the spleen and splenectomy the following day. Pathology revealed a 4.4 x 3.7 x 3.1 cm ill-defined mass located within the splenic hilum (Figure 1A), which consisted of poorly differentiated adenocarcinoma (Figure 1B1C). Immunohistochemically, the adenocarcinoma was positive for cytokeratin AE1/AE3, CK7, PAX-8 and estrogen receptor (Figure 1D). The adenocarcinoma was negative for CK20. The morphology and immunohistochemistry were consistent with metastatic adenocarcinoma of müllerian origin, from the patient’s known ovarian adenocarcinoma.

Discussion

LSPH, also known as splenoportal or sinistral hypertension is a rare, but life-threatening cause of upper gastrointestinal bleeding.2 LSPH often occurs in non-cirrhotic patients as a consequence of splenic vein obstruction. Pancreatic disorders, including pancreatic carcinoma, acute and chronic pancreatitis, cysts, and pseudocysts which may block the splenic vein via thrombus formation or mass effect, are the most common causes of LSPH.3 To our knowledge there is only one other case of LSPH with bleeding gastric varices secondary to metastatic ovarian cancer published by Wallace et al in 2004.4 In our case, mass effect on the splenic vein as well as likely tumor thrombus caused splenic venous outflow obstruction. Obstruction of the splenic vein results in venous hypertension in collateral pathways that carry splenic arterial blood via the short gastric, coronary, and gastroepiploic veins to the superior mesenteric and portal veins. In the gastric wall veins of the fundus, blood flow and pressure increase, and submucosal structures consequently dilate, producing gastric varices.4,3 Risk factors for gastric variceal hemorrhage include the size of fundal varices (as there is a linear relationship between size of varices and risk of variceal hemorrhage), endoscopic presence of variceal red spots, and Child-Pugh class in patients with cirrhosis.5 Gastric varices are less frequent than esophageal varices and are present in 5%33% of patients with portal hypertension. The reported incidence of bleeding from gastric varices is approximately 25% in two years, with a higher bleeding incidence for fundal varices.6 Compared to esophageal varices, gastric varices are larger, more extensive, and lie deeper in the submucosa. As a result, standard endoscopic treatments for esophageal varices, including band ligation and sclerotherapy are largely ineffective for gastric varices.7 Management of gastric varices is dependent on the etiology, presence of collaterals and the available treatment modalities. LSPH, for example, has distinct therapeutic management options that are not appropriate for the management of generalized portal hypertension. Currently the gold standard for treatment of fundal (IGV1) varices as a result of splenic vein thrombosis is splenectomy. Surgical removal of the spleen decreases venous outflow through collateral circulations and decompresses IGV to prevent future bleeding.8 Additional therapies have been used to control gastric variceal bleeding and prevent re-bleeding from occurring. These include band ligation and endoscopic sclerotherapy (frequently by cyanoacrylate glue injection). The American Association for the Study of Liver Diseases (AASLD) Society guidelines recommend endoscopic variceal sclerotherapy in patients who bleed from gastric fundal varices otherwise when available, endoscopic variceal ligation is an option. AASLD also recommends that transjugular intrahepatic portosystemic shunt (TIPS) should be considered in patients in whom hemorrhage from fundal varices cannot be controlled or in whom bleeding recurs despite combined pharmacological and endoscopic therapy.5 Left-sided portal hypertension should be considered in the presence of gastrointestinal bleeding with normal liver function and unexplained splenomegaly.1 Isolated gastric varices type 1 should immediately raise the clinician’s suspicion for splenic vein obstruction. Although a rare cause, in patients with prior malignancy or without evidence of pancreatic pathology, malignancy should remain on the differential as a cause of splenic vein obstruction.

INTRODUCTION: DISPATCHES FROM THE GUILD CONFERENCE

Dispatches from the GUILD Conference 2020

Uma Mahadevan

Welcome to the Fourth annual Dispatches from GUILD series! The Gastrointestinal Updates-Inflammatory Bowel DiseaseLiver Disease (GUILD) Conference is an annual CME conference held in Maui, Hawaii every February (GUILD 2020: February 16-19). This meeting offers a cutting edge update in gastroenterology by world class speakers in a setting conducive to learning and interaction with peers. Our topics this year include 2 days of IBD updates, a day of hepatology and a day of obesity related topics. GUILD also recognizes the role played by nurse practitioners and physician assistants in the care of IBD patients and introduced an IBD boot camp in 2019. Scholarships are awarded to 10 NP/PA’s and 10 Gastroenterology fellows to attend the meeting and receive daily mentoring and networking.
To share our learning with the gastroenterology community at large, we are happy to continue our series beginning with the following article, “Prevention in Inflammatory Bowel Disease: An Updated Review”. We look forward to providing informative and educational articles covering IBD, Hepatology and special topics in GI in Practical Gastroenterology over the following months

DISPATCHES FROM THE GUILD CONFERENCE, SERIES #27

Prevention in Inflammatory Bowel Disease: An Updated Review

Millie D. Long

Patients with inflammatory bowel disease (IBD) are subject to complications from the disease itself and also from the immunosuppressive therapies used for treatment. To optimize the care of patients with IBD, providers need to consider primary, secondary and tertiary prevention. Primary prevention is employed to prevent a disease or complication from developing, such as immunizations. Secondary prevention detects a disease early to prevent disability, such as through screening programs. Tertiary prevention employs measures to reduce the impact of long-term disease and disability. This review highlights methods of prevention that can be utilized in patients with IBD via partnership between the primary care and gastroenterology provider.

INTRODUCTION

Inflammatory bowel disease (IBD), including both Crohn’s disease (CD) and ulcerative colitis (UC), causes inflammation and ulceration in the gastrointestinal tract. This inflammation results in considerable morbidity for patients, including symptoms such as diarrhea, abdominal pain, rectal bleeding, and weight loss. The prevalence of IBD is increasing in the United States (US) and worldwide. It is estimated that 2.2 million Americans will be living with IBD by 2025.^1,2 With this growing population, there is an increasing need for effective and safe therapies for management of inflammation. Currently, there are a large number of classes of agents available for treatment of IBD, with varying relationships between safety and efficacy. Immunosuppressive agents used in the treatment of IBD include corticosteroids, biologic agents [anti-tumor necrosis factor alpha (anti-TNF), antiintegrin therapies, anti IL-12/23 inhibitors, janus kinase (JAK) inhibitors, and immunomodulators such as thiopurines or methotrexate]. As we target goals of mucosal healing in our IBD population using immunosuppressive agents, we must also use a patient-centered approach to prevent downstream complications, either of IBD itself, or of the therapies used for treatment of IBD. To do so, a partnership must exist between gastroenterology and primary care providers to target primary, secondary and tertiary prevention for our patients. This article will discuss current guidelines and recommendations for prevention specific to patients with IBD

Primary Prevention

Primary prevention is defined as prevention of disease development. Examples of primary preventive efforts include immunizations against infectious diseases or educational interventions on regular exercise. Primary preventive efforts can occur at an individual level or at a population level. One example of a population level primary preventive effort is fluoridation of the water supply to prevent dental caries. As compared to the agematched general population, patients with IBD are at increased risk for vaccine-preventable illnesses, such as influenza,⁵ pneumococcal pneumonia,⁶ and shingles.⁷ Inactivated vaccines are safe to administer in patients with IBD, regardless of immunosuppression status. Therefore, adherence to vaccination guidelines of inactivated vaccines can reduce these infectious complications. Annual influenza vaccination is indicated in all patients with IBD, pneumococcal vaccination series is indicated in all immunosuppressed patients with IBD and herpes zoster vaccination is indicated in all patients with IBD ≥ 50 years of age. Due to increased risk of shingles in younger IBD populations,⁷ consideration can be given for earlier vaccination while on certain high risk therapies. In particular, tofacitinib is associated with an increased risk of shingles, particularly at higher doses.⁸ However, more data are needed on safety, efficacy and durability in younger populations prior to a definitive recommendation. The human papillomavirus (HPV) vaccine has been shown to protect against specific serotypes of HPV linked to cervical dysplasia and genital warts. This vaccine has been studied specifically in IBD populations. The HPV vaccine has demonstrated both efficacy and safety.⁹ Another method of primary prevention in IBD patients is sunscreen use to prevent skin cancer. Patients with IBD have increased risks of both non-melanoma (NMSC) and melanoma skin cancer.^{10, 11} Evidence has demonstrated that thiopurines specifically increase the risk of NMSC and that the mechanism of action is associated with photosensitivity to ultraviolet-A light.¹² Therefore, this is a potentially preventable complication of therapy through broad-spectrum sunscreen use. Finally, weight bearing exercise and calcium/ vitamin D supplementation, when appropriate, can prevent downstream osteoporotic fracture in these patients who may require recurrent courses of corticosteroids during their lifetimes with IBD. Table 1 shows a summary of primary preventive measures recommended in IBD patients.

Secondary Prevention

Secondary prevention is defined as detecting a disease early to prevent disability; such as through screening programs. Therefore, there are a number of important opportunities for secondary prevention in IBD patients. For example, patients with IBD are known to have an increased risk of melanoma, regardless of immunosuppressive therapy. Individuals on anti tumor necrosis factor alpha (anti-TNF) agents have nearly a two-fold further increased risk of developing melanoma.10 Therefore, a dermatology skin screening program is recommended in all patients with IBD.3 Prior studies have suggested an increased risk of abnormal Pap smear and/or cervical dysplasia in patients with IBD on immunosuppression.13 Therefore, annual cervical cancer screening is recommended in patients with IBD on immunosuppression.3 Patients with IBD who have longstanding colonic inflammation (> 10 years of duration) have an increased risk of developing colorectal dysplasia and cancer. Therefore, patients with longstanding colonic inflammation should undergo routine colonoscopy starting at 8-10 years of colonic disease duration, with subsequent colonoscopy intervals based on the results (often every 1-3 years). From a bone health perspective, all individuals (regardless of gender) with ≥ 3 months duration of corticosteroid use are at risk for osteopenia or osteoporosis. Therefore, screening with DEXA scan for these individuals and in women age ≥ 65 years is recommended. Subsequent DEXA screening can be determined based on the initial results. Finally, depression and anxiety are common in IBD patients.14 Earlier recognition and treatment of depression and anxiety can improve quality of life in patients with IBD. Screening for depression and anxiety is recommended in all patients with IBD.3 Table 2 describes currently recommended secondary preventive efforts in IBD patients.

Tertiary Prevention

Tertiary prevention refers to utilization of measures to reduce the impact of long-term disease and disability. In CD, ongoing inflammation can lead to development of strictures, which may cause obstruction and require bowel resection surgery. Additionally, inflammation can progress to fistulizing disease, including abnormal connections between the bowel and other organs. These fistulas can result in abscesses and other complications ultimately often requiring surgery. In UC, ongoing inflammation can increase the risk of colon cancer and dysplasia. Additionally, disease can extend from only left-sided involvement to pan-colonic involvement over time. Therefore, by intervening early and treating inflammation, with a goal of mucosal healing, we can potentially prevent these morbid and potentially life-threatening, complications of IBD. The paradigm in IBD management has shifted to one of a “treat to target” approach¹⁵. After initiation of medical therapy for the treatment of IBD, guidelines recommend subsequent reassessment to ensure that both symptoms and mucosal inflammation are improved.^16,17 This dual method of reassessment is important, as symptoms do not always correlate with ongoing inflammation. This standard of reassessing a current therapy is also important in post-operative CD, where early evaluation with colonoscopy in the first 6-12 months after a resection, with alteration of medical therapies based on this, has been shown to improve long-term endoscopic outcomes.¹⁸ Therefore, by optimizing therapies to improve mucosal healing, we may be able to impact the long-term disability associated with irreversible bowel damage in IBD.

CONCLUSION

Management of patients with IBD can be difficult. IBD itself can be associated with a number of complications for patients, including ongoing chronic bowel symptoms and structural bowel damage, as well as extra-intestinal manifestations of IBD. These extra-intestinal manifestations
can include significant joint symptoms, skin manifestations, anemia, and kidney stones. While there are a number of effective therapeutic agents for the treatment of IBD and these extraintestinal complications, many of these therapies are themselves immunosuppressive. Therefore, the drugs themselves can result in therapy-related complications. These may include infectious, malignant, or idiopathic complications. As the patient may present to the primary care provider or the gastroenterologist for evaluation of symptoms or complications, it becomes very important for the entire care team to collaborate on diagnostic and management plans for individual patients with IBD. Importantly, prior studies have demonstrated that primary care physicians may not be comfortable addressing preventive care in IBD patients on immunosuppression.³ However, the gastroenterologist may assume that all preventive activities are occurring in primary care. The gastroenterologist may also not be comfortable addressing all of an IBD patient’s preventive health needs. In fact, many patients with IBD consider their gastroenterologist to be their primary care provider. Therefore, a collaboration between primary care and gastroenterology is needed to ensure appropriate adherence to preventive health recommendations in patients with IBD. Each IBD patient should have regular evaluation with both a primary care and gastroenterology provider. Through this partnership, an individualized plan for preventive medicine can be developed for each patient with IBD. This proactive approach of addressing primary, secondary and tertiary prevention in IBD patients can ultimately help to reduce infectious, malignant and long-term disease-related complications. There is an old African proverb stating, “It takes a village to raise a child.” This reflects the emphasis that African cultures place on family and community. In fact, this community of support is also needed for each patient with IBD. By sharing the burden of the complete care of the IBD patient, a care team can deliver evidencebased, patient-centered care. Figure 1 shows the integral components of a care team for a patient with IBD. Through collaboration, a care plan can be implemented for each IBD patient addressing his or her individual needs and goals. By focusing on implementing the three forms of prevention: primary, secondary, and tertiary, we can improve the lives of our patients with IBD.