The American Journal of Surgery (2011) 202, 487– 491
Society of Black Academic Surgeons
Profiling adult intussusception patients: comparing colonic versus enteric intussusception Richard Alexander, M.D.*, Purnell Traverso, M.D., Oluwaseyi B. Bolorunduro, M.D., M.P.H., Gezzer Ortega, M.D., David Chang, Ph.D., M.P.H., Edward E. Cornwell III, M.D., Terrence M. Fullum, M.D. Department of Surgery, Howard University Hospital, 2041 Georgia Ave., Suite 4100B, Washington, DC 20060, USA KEYWORDS: Adult intussusception; Surgical; Malignant; Comorbidity; Neoplasm
Abstract BACKGROUND: Adult intussusception is a rare entity representing 1% of all adult bowel obstruction, hospital admissions secondary to intussusception historically has ranged between .003% and .02%. There is limited knowledge regarding enteric and colonic surgical intussusception patients and their associated conditions. METHODS: A retrospective study was conducted using data from the National Inpatient Sample from 1998 to 2006. The inclusion criteria were surgical patients with intussusception. RESULTS: A total of 1,178 cases of intussusception requiring surgery were isolated from the database. The mean patient age was 49.57 years, about 58% were females, 99.43% of this population was insured, and the overall mortality rate was 1.70%. Colonic resection was associated with greater mortality compared with the enteric resection group (P ⫽ .018). CONCLUSIONS: This was a large study on surgical adult intussusception patients conducted in the United States. We show differences in demography, comorbidities, and potential causes between colonic and enteric intussusception. Published by Elsevier Inc.
Adult intussusception is a rare entity representing 1% of all adult bowel obstruction, and 5% of all intussusceptions including the pediatric population.1 Hospital admissions secondary to intussusception historically have ranged between .003% and .02%.2 The etiology in the adult population usually is evident in 70% to 90% of cases, with a malignant focus making up approximately 50% to 60% of Terrence Fullum is a consultant for Ethicon (Cincinnati, OH) Richard Alexander’s current affiliation is Athens Medical Group, 1630 Lafayette Rd, Suite 300, Crawfordsville, IN 47933. * Corresponding author: Tel.: ⫹1-765-361-1234; fax: ⫹1-765-3612267. E-mail address:
[email protected] Manuscript received July 1, 2010; revised manuscript February 15, 2011
0002-9610/$ - see front matter Published by Elsevier Inc. doi:10.1016/j.amjsurg.2011.02.006
surgical specimens. It is this preponderance for malignancy in adults that prompted the classification of adult intussusception as a surgical disease. This entity can be classified into 4 distinct categories: (1) enteric, in which the intussusception is confined to the small bowel; (2) ileocolic, in which the ileum invaginates through a fixed ileocecal valve; (3) ileocecal, in which the ileocecal valve itself is the lead point for the intussusception; and (4) colocolic, in which the lead point is restricted to the colon.3 The majority of information that has been collected regarding intussusception has been gathered via small case studies or institutional reviews. Little is known regarding comorbidities or previous ailments that may predispose patients to develop intussusception, nor is there information discerning colonic versus enteric patients. The aim of this study was to evaluate the
488 Table 1
The American Journal of Surgery, Vol 202, No 4, October 2011 ICD-9 codes used for diagnosis
AI Large-bowel resection Small-bowel resection Malignant GI neoplasm Benign GI neoplasm Benign other neoplasm Diabetes Nutrition deficiency Anemia Drug abuse Hypertension Appendicitis Abdominal hernia Intestinal obstruction Peritoneal adhesions
560.0 457.2, 457.3, 457.4, 457.5, 457.6, 457.9, 459.3, 459.4, 486.3, 456.0 453.3, 456.2, 459.1 153.1, 153.2, 153.3, 153.4, 153.5, 153.6, 153.7,153.8, 153.9 211.1, 211.2, 211.3, 211.9 212.7, 214.1, 214.2, 214.3, 214.8, 214.9, 215.3, 215.5, 216.6, 216.7, 218.0, 218.1, 218.2, 218.9, 219.9, 220.0, 221.0, 225.0, 225.2, 227.0, 227.3, 228.0, 228.01, 228.04, 228.09, 228.01, 229.0, 229.8 250.0 269.8, 269.9 280.9 305.9 403.9 540.0, 540.1, 540.9, 541, 542 553, 553.1, 553.2 560.9 560.81
conditions and outcomes of colonic and enteric surgical intussusception patients.
and LOS, respectively. Age, sex, insurance status, undergoing laparoscopy, and undergoing large-bowel resection were covariates controlled for in our model.
Methods A retrospective study was conducted using data from the Healthcare Cost and Utilization Project-National Inpatient Sample (NIS) from 1998 to 2006. The NIS is the largest all-payer inpatient care database in the United States. It contains data from approximately 8 million hospital stays each year. Information during this time period contained data from up to 38 states and it is approximately a 20%-stratified sample of all US community hospitals. The inclusion criterion was patients with intussusception as defined by International Classification of Diseases, 9th revision (ICD-9) diagnosis code 560.0 who had any surgical procedure. Excluded were all patients younger than 18 years of age and patients with rectal prolapse (ICD 9 diagnosis code 569.1), previous esophagogastroduodenoscopy with or without biopsy, colonoscopy, and flexible sigmoidoscopy (ICD 9 procedure codes 451.6, 451.3, 452.3, and 452.4, respectively). Also excluded were patients who had neither small- nor largebowel resection. Extrapolation of data observed in the NIS database to estimate the total number of patients in the US population was performed by weighing the identified records using the sampling weights associated with each hospital in the NIS database. The outcome variables were mortality and total length of hospital stay (LOS). A comparison was made between patients with large-bowel resection versus small-bowel resection (Table 1). Comorbidity profiles were defined as specified in Table 1. A bivariate analysis was conducted using the Pearson chi-square analysis. Multivariate analyses involved the use of multiple logistic regression and multiple linear regressions for mortality
Results A total of 1,178 surgical intussusception patients were identified, including 634 (53.82%) with colonic resections and 544 (46.18%) with small-bowel resections (Table 2). The mean age for those with colonic resections was 47.2 years whereas those with small-bowel resections had a mean age of 51.5 years. Most patients were female in both groups, 59.81% and 55.82%, respectively. In terms of race those individuals who went on to have surgery were mostly Caucasian, with 329 (71.83%) undergoing a colonic resection and 291 (74.23%) with a small-bowel resection. Most cases were performed without laparoscopy: 96.37% and 95.77%, respectively. LOS was almost equivalent between
Table 2 Demographic and outcome data of surgical intussusception patients using the NIS Large bowel, n (%) Small bowel, n (%) N 634 Mean age, y (SD) 47.24 Female 378 Male 254 Race (n ⫽ 850) White 329 Black 67 Hispanic 28 Asian 16 Laparoscopic approach 23 Open approach 611 Insured 556 Mean LOS, d Mortality 16
(53.82) (18.03) (59.81) (40.19
544 51.5 302 239
(71.83) (14.63) (6.11) (3.49) (3.63) (96.37) (99.29) 7.9 (2.52)
291 60 28 6 23 521 484
(46.18) (18.87) (55.82) (44.18)
(74.23) (15.31 (7.14) (1.53) (4.23) (95.77) (99.59) 7.8 4 (.74)
R. Alexander et al. Table 3 patients
Intussusception patients
489
Comorbidities among all surgical intussusception
Categories Malignant GI neoplasm Malignant other Benign GI neoplasm Benign other neoplasm Diabetes Nutrition deficiency Anemia Drug abuse Hypertension Appendicitis Abdominal hernia Intestinal obstruction Peritoneal adhesions
Large bowel, n (%)
Small bowel, n (%)
P value
35 (5.52)
10 (1.84)
.001
16 (2.52) 92 (14.51) 89 (14.04)
32 (5.88) 73 (13.42) 55 (10.11)
.004 .59 .04
Multivariate analysis: malignant GI neoplasms
Categories
Odds ratio
P value
Large bowel (reference: small bowel) Age, 45–65 y Age, ⬎65 y Female (reference: male) Black (reference: white) Hispanic (reference: white) Asian (reference: white)
2.15 13.5 16.2 .9 2.4 1.6 4
.07 .012* .008* .966 .048* .496 .085
*Parameters that were statistically significant.
40 25 86 70 171 39 28 129 39
(6.31) (3.94) (13.56) (11.04) (26.97) (6.15) (4.42) (20.35) (6.15)
45 22 95 65 131 10 38 152 36
(8.27) (4.04) (17.46) (11.95) (24.08) (1.84) (6.99) (27.94) (6.62)
.194 .93 .064 .626 .257 ⬍.001 .056 .002 .744
the 2 groups at 7.9 and 7.8 days, respectively. In terms of mortality between the populations there were 16 and 4 deaths, but after multivariate analysis there was no statistical significance. Upon the evaluation for the presence of comorbid conditions we found that primary malignant gastrointestinal (GI) neoplasms (primary adenocarcinoma) were more common among those with colonic resections 35 (5.52%) (Table 3). Although the malignant other category (metastatic lesions) was seen more often in those patients who had an enteric resection (32; 5.88%). Most benign lesions (be them primarily GI or other) were seen in the colonic and enteric groups at 92 (14.51%) and 89 (14.04%) patients, respectively. After analyzing many other comorbid conditions, the only 2 that were statistically significant were intestinal obstruction and appendicitis. Those patients with enteric resections were most likely to present initially with intestinal obstruction (152; 27.94%), whereas colonic patients had initial symptoms of appendicitis (39; 6.15%). Two variables were isolated for multivariate analysis: LOS and malignant GI neoplasm (Tables 4 and 5). When
Table 4 LOS
Table 5
Multivariate analysis: adjusted difference in mean
Categories
Odds ratio
P value
Large bowel (vs small bowel) Age Female (reference: male) Black (reference: white) Hispanic (reference: white) Asian (reference: white) Insured (reference: uninsured) Laparoscopy (reference: open)
⫺.180 .087 .198 1.584 ⫺1.176 .637 .999 .154
.686 ⬍.001* .659 .015* .177 .668 .815 .154
*Parameters that were statistically significant.
attempting to isolate factors that would influence the overall LOS, the only parameters that were significant were age (age ⬎ 45 y) and black race. When analyzing malignancy rates in primary GI tumors it was found that 2 factors increased the likelihood of malignancy: age younger than 65 years, and black race/ethnicity.
Comments Intussusception is the telescoping of 1 proximal portion of the intestine into the other with the exact mechanism unknown. It is postulated to involve some irritant within the lumen of the intestine that affects normal peristaltic activity, causing invagination of the proximal bowel into the distal lumen. The classic presentation of intussusception in the pediatric population, which includes a mass, abdominal pain, and blood per rectum, is rarely found in the adult population.4 Adult intussusception (AI) is an uncommon clinical entity. It presents with acute, subacute, or chronic nonspecific symptoms and as such is difficult to diagnose, with accuracy rates ranging between 30% and 90% in some earlier reports.2,5–7 In this study, in cases of AI the location was only in the small bowel, or was enteric intussusception (EI) (46%) or colonic intussusception (CI) (54%). The NIS database has no ICD-9 codes for combined enteric and colonic disease. This is unlike earlier reports of a higher incidence of surgically correctible EIs in previously published data.8 Goh et al9 published 60 cases of AI and showed EI to have a 26.7% incidence, with CI being the least common type. There was a predominance of females who underwent surgical management of both EI and CI. The NIS database identified intestinal obstruction as the presenting diagnosis in intussusception in 20.35% of CI and 27.94% of EI (P ⫽ .002), whereas appendicitis was the presenting etiology in 6% of CI and 2% of EI (P ⱕ .001). Azar and Berger described intestinal obstruction in 50% of patients.2 As medicine has evolved, immediate surgical intervention for intestinal obstruction has been diluted with expectant management in certain situations. Black patients were shown to have an increased LOS by 1.6 days compared with their Caucasian counterparts (P ⫽ .015).
490 This may have been owing to management of comorbid conditions caused by poor primary care. The NIS database does not have information on socioeconomic status and this variable cannot be commented on intelligently. We found no difference in LOS between enteric or colonic surgical management. Age also was shown to be statistically significant on multivariate analysis, with an increased LOS of .087 days (P ⱕ .001). Age between 45-65 years was shown to have a 13.5 times increased risk of malignancy (P ⫽ .012) as etiology of intussusception. This high risk associated with the older age group can be accounted for by the higher incidence of colon cancer found in patients older than age 50. Screening for adenocarcinoma of the colon begins at age 50 for this very same reason. More complications of mitotic-related complications should be expected in this higher-risk group. Black patients were found to have a 2.5 times increased risk of presenting with malignant intussusception (P ⫽ .048). Insurance status as well as access to primary care physicians remains a socioeconomic challenge. Poor primary care or referral for colonoscopy is key in the early identification of malignant colonic lesions. Late diagnosis of this condition in black patients allows a higher incidence of patients presenting with complications of the disease, one of which is intussusception. Contrary to published data known to us, this article illustrates a low incidence of malignant causes of both EI (1.84%) and CI (5.52%) (P ⫽ .001). Benign causes of intussusception were 10.11% (EI) and 14.51% (CI). Historically, the management of CI in adults was accepted to be surgical with few unusual exceptions. This stemmed from high incidences in published data (30%–70%) of malignancy associated with CI. Published data describe a malignant etiology as the cause for EI in up to 30% of cases and as the cause for CI in up to 66% of cases. AI has been described as a surgical disease and there is much controversy regarding its optimal management. Most of the controversy focuses on initial reduction followed by a more limited resection versus primary en bloc resection.2,4,6,10 Many theories have been postulated including intraluminal seeding and venous dissemination of malignant cells, and possible perforation during manipulation.8 Historically, the management of CI in adults was accepted to be surgical with few unusual exceptions. Advocates for primary resection quote high incidences of underlying malignancy, especially with CI. Azar and Berger reported, in a 30-year review of 58 cases of surgically proven intussusception, a malignancy rate of 46% in colonic lesions.2 Older data by Briggs et al showed a 20% to 66% malignant etiology.11–13 Wang et al concluded that there is a role for selective resection for CI. Our multivariate analysis encompasses all US centers surgically managing intussusception and as such found a much lower incidence of malignancy. On multivariate analysis of 1,178 surgical intussusception patients, the largest published data set at this time showed a malignant etiology in only 5.52% of CI and 1.84% (P ⫽ .001) of EI
The American Journal of Surgery, Vol 202, No 4, October 2011 patients. This requires further discussion as to the need for surgical intervention for all cases of adult intussusception. These low percentages warrant the revisiting of the core teaching of mandatory surgical resection for AI and are markedly lower than any previously reported. It is possible that because previously published data originate from large, individual referral centers, they treat a specific patient population that may be at higher risk of malignancy. This may reflect a selection bias. One of the limitations of our study that we need to consider is the possibility of incomplete documentation in the NIS database. This data resource does not allow us to identify the exact etiology of intussusception. We can retrieve comorbidities (malignant lesions or benign lesions) but are limited to relying on accurate documentation of the pathology of the causes of intussusception. We believe that a nonsurgical approach of reduction either intraoperatively or preoperatively can be considered in low-risk groups. Computed tomography scan is the mainstay method of diagnosing intussusception in this age of technology. As stated earlier, most AIs present as intestinal obstruction. We suggest using computed tomography to determine the likelihood of a definitive mass as the etiology of the intussusception. Patients with a low likelihood of an obstructing lesion may benefit from a barium enema or colonoscopy during that admission to determine the presence of malignancy. For EI, a small-bowel follow-through versus video endoscopy may be of value. Patients who are taken to the operating room can be managed by manual palpation and surgeon assessment, which possibly may determine the need for a biopsy with frozen section if necessary. This may prevent the complications associated with formal intestinal resection and anastomosis.
Conclusions This was a large study on surgical AI patients conducted in the United States. We show differences in demography, comorbidities, and potential causes between CI and EI. The malignancy rates between CI and EI patients were lower than previously reported percentages. It is still unclear as to the etiology of such low rates. However, this study suggests that there is justification for nonsurgical management and a role for selective surgical resection as treatment for AI.
References 1. Nagomey DM, Sarr MG, Mcllrath DC, Surgical management of intussusception in the adult. Ann Surg. 1981;193:230 – 6. 2. Azar T, Berger D. Adult intussusception. Ann Surg 1997;226:134 – 8. 3. Eisen LK, Cunningham JD, Aufses AH. Intussusception in adults: an institutional review. J Am Coll Surg 1999;188:390 –5.
R. Alexander et al.
Intussusception patients
4. Begos DG, Sandor A, Modlin IM. The diagnosis and management of adult intussusception. Am J Surg 1997;173;88 –94. 5. Chun-Chao C, Yang-Yuan C, Yung-Fa C, et al. Adult intussusception in Asians: clinical presentations, diagnosis, and treatment. J Gastroenterol Hepatol 2007;22:1767–71. 6. Barussaud M, Regenet N, Briennon X, et al. Clinical spectrum and surgical approach of adult intussusceptions: a multicentric study. Int J Colorectal Dis 2006;21;834 –9. 7. Erkan N, Haciyanli M, Yildirim M, et al. Intussusception in adults: an unusual and challenging condition for surgeons. Int J Colorectal Dis 2005;20;452– 6.
491 8. Zubaidi A, Al-Saif F, Silverman R. Adult intussusception: a retrospective review. Dis Colon Rectum 2006;49:1546 –51. 9. Goh BK, Quah HM, Chow PK, et al. Predictive factors of malignancy in adults with intussusception. World J Surg 2006;30:1300 – 4. 10. Yalamarthi S, Smith RC. Adult intussusception: case reports and review of literature. Postgrad Med J 2005;81:174 –7. 11. Briggs DF, Carpathios J, Zollinger RW. Intussusception in adults. Am J Surg 1961;101:109 –13. 12. Harlaftis N, Skandalakis JE, Droulias C. The pattern of intussusception in adults. J Med Assoc Ga 1977;66:534 –9. 13. Roper A. Intussusception in adults. Surg Gynecol Obstet 1956;103:267–78.