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The clinical outcome of elderly patients with acute pancreatitis is not different in spite of the different etiologies and severity
Archives of Gerontology and Geriatrics 54 (2012) 256–260
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The clinical outcome of elderly patients with acute pancreatitis is not different in spite of the different etiologies and severity Jang Eon Kim a,b, Jin-Hyeok Hwang b, Sang Hyub Lee b,*, Byung Hyo Cha b, Young Soo Park b, Jin-Wook Kim b, Sook-Hyang Jeong b, Nayoung Kim b, Dong Ho Lee b a
Division of Gastroenterology, Department of Internal Medicine, Seoul Medical Center, 171-1 Samsung-dong, Gangnam-gu, Seoul 135-090, South Korea Department of Internal Medicine, Seoul National University College of Medicine, Seoul National University Bundang Hospital, 300 Gumi-dong, Bundang-gu, Seongnam-si, Gyeonggido 463-707, South Korea b
A R T I C L E I N F O
A B S T R A C T
Article history: Received 15 October 2010 Received in revised form 13 January 2011 Accepted 14 January 2011 Available online 17 February 2011
The aim of this study was to investigate the overall clinical characteristics of elderly patients with acute pancreatitis. We retrospectively evaluated 227 consecutively enrolled patients who were admitted with acute pancreatitis. The clinical features, the radiological and laboratory data and the clinical outcome were analyzed according to the age groups (65 years vs. <65 years). Among the 227 enrolled patients with acute pancreatitis, there were 85 elderly patients and 142 non-elderly. The mean age of the elderly patients was 72.3 5.5 years and that of the non-elderly was 44.7 11.7 (p < 0.001). For the elderly patients, biliary pancreatitis was the most common cause (56.5%), but alcoholic pancreatitis was most common in the non-elderly patients (45.8%). Although the computed tomography (CT) severity index was significantly higher for the non-elderly patients (p < 0.001), the acute physiology and chronic health evaluation (APACHE II) score was significantly higher for the elderly than that for the non-elderly (p < 0.001). However, the duration of the hospital stay (10.3 9.6 days vs. 11.9 10.1 days, p = 0.619) and mortality (3.5% vs. 0.7%, p = 0.148) were not different between the age-groups. In our study, chronological age had no significant influence on the clinical outcome in spite of the different etiologies and severity of acute pancreatitis. ß 2011 Elsevier Ireland Ltd. All rights reserved.
Keywords: Acute pancreatitis in elderly Etiology of acute pancreatitis Severity of acute pancreatitis Outcome of pancreatitis
1. Introduction Acute pancreatitis is an acute inflammatory disease of the pancreas that frequently involves the peripancreatic tissues and/ or remote organ systems (Banks, 1997). Acute pancreatitis has consistently increased in Western countries over the past decades (Eland et al., 2000; Floyd et al., 2002; Tinto et al., 2002; Goldacre and Roberts, 2004; Yadav and Lowenfels, 2006; Singla et al., 2009). In Korea, the annual incidence of acute pancreatitis per 100,000 people has likewise increased from 15.6 in 1995 to 19.4 in 2000 (Kim, 2003). With the increased life span, elderly patients now comprise a large proportion of the population. As a result, physicians are more often being faced with acute pancreatitis in elderly patients (Gullo et al., 1994; Kang et al., 1998). Acute pancreatitis is a potentially fatal disease with an overall mortality of 2.1–7.8% (Eland et al., 2000; Floyd et al., 2002; Tinto et al., 2002; Kim, 2003; Goldacre and Roberts, 2004; Yadav and Lowenfels, 2006; Singla et al., 2009). However, more
* Corresponding author. Tel.: +82 31 787 7042; fax: +82 31 787 7051. E-mail address: [email protected] (S.H. Lee). 0167-4943/$ – see front matter ß 2011 Elsevier Ireland Ltd. All rights reserved. doi:10.1016/j.archger.2011.01.004
than 80% of these patients have mild acute pancreatitis and it resolves itself without serious complications (Wang et al., 2009). The association of the severity of acute pancreatitis with age is still controversial. One study showed that the overall mortality rate of elderly patients with acute pancreatitis increased from 2% for those under 55 years of age to 11% for older patients (De Beaux et al., 1995). Another study reported that the mortality rate of patients with acute pancreatitis and who were aged 70 years was three-fold more increased as compared to that for the patients who were under 60 years (McKay et al., 1999). However, some studies reported that the mortality rate of acute pancreatitis was not significantly different between the elderly patients and younger patients (Fan et al., 1988; Lankisch et al., 1996). The association of age with the severity of acute pancreatitis has been focused on by several studies. However, while the management of acute pancreatitis has recently improved and the most of the patients have mild acute pancreatitis, not many studies have evaluated the comprehensive clinical characteristics of elderly patients with acute pancreatitis in the recent years. The aim of this study was to investigate the comprehensive clinical characteristics of elderly patients with acute pancreatitis.
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2. Patients and methods 2.1. Patients We retrospectively evaluated the demographic features and the laboratory and radiology data of 227 consecutively enrolled patients with acute pancreatitis. These patients were admitted to Seoul National University Bundang Hospital from April, 2003 to March, 2009. However, if the patients with acute pancreatitis were diagnosed with chronic pancreatitis with acute execration, post endoscopic retrograde cholagiopancreatography (ERCP) pancreatitis or a tumorous condition, including pancreatic cancer, intraductal papillary mucinous neoplasm (IPMN) and mucinous cystic neoplasm (MCN), then they were excluded. The study protocol was approved by the Institutional Review Board of our hospital. 2.2. Definition of events Acute pancreatitis was defined as typical abdominal pain associated with elevated levels of serum amylase to more than 3 times the upper normal limit (normal range: 30–100 IU/). All the patients showed radiologic imaging (ultrasonography, abdomen contrast-enhanced CT and magnetic resonance imaging) that was compatible with acute pancreatitis. Co-morbidity was defined a preexisting disease or condition in addition to the acute pancreatitis. Clinical severity evaluations were carried out using the APACHE II (Knaus et al., 1985) and CT severity index scoring systems within 48 h after admission (Balthazar et al., 1990). The diagnostic criteria for severe acute pancreatitis were an APACHE II score of more than 8 within 48 h after admission. Necrotizing pancreatitis was defined as the appearance of pancreatic or extra-pancreatic necrosis on the contrast-enhanced CT and a serum C-reactive protein (CRP) value of more than 150 mg/l (Sakorafas et al., 1999; Buchler et al., 2000; Forsmark and Baillie, 2007). Serial abdominal contrast-enhanced CT was performed for all patients on admission and the findings were graded according to the Balthazar classification (Balthazar et al., 1990). The etiology was considered to be of an alcoholic origin when the patient had consumed more than 40 g ethanol in the form of ‘‘soju’’ (Korean vodka) per day (20 g in female) for at least 5 years or the patient had consumed excessive alcohol shortly before the onset of the disease (Lin et al., 2001; Chen et al., 2006; Bai et al., 2007a,b). A serum triglyceride level more than 1000 mg/dl and exclusion of other etiologies were accepted as the hyperlipidemic etiology (Kyriakidis et al., 2005). Biliary pancreatitis was defined as gall stones and sludge were found on subsequent ultrasonography, contrast-enhanced CT, or ERCP after other etiologic factors (such as alcohol and hyperlipidemia) have been excluded. The miscellaneous etiologic factors included trauma and autoimmune disease. All the patients with no identifiable etiology were classified as having idiopathic pancreatitis. On admission, all the patients were treated medically according to generally accepted principles, which consisted of stopping the oral intake, providing pain relief, restoring fluids and electrolytes intravenously and administering prophylactic antibiotics. An endoscopic sphincterotomy was done if stones and sludge were present in the common bile duct and some patients with this condition were treated with endoscopic nasobiliary drainage. Necrectomy was performed for the patients with clinical deterioration and for those with infected necrosis, which was diagnosed by fine needle aspiration under CT guidance. 2.3. Data analysis The demographic data (age, gender, smoking, body mass index (BMI)), the data on co-morbidities and etiologies and the
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laboratory data, including the white blood cell count, the hematocrit and the blood urea nitrogen (BUN), creatinine, bicarbonate, sodium, potassium, serum alkaline phosphatase (SAP), amylase, lipase, aspartate aminotransferase (AST), alanine transaminase (ALT) and CRP levels, were analyzed according to the age groups (<65 years vs. 65 years) to clarify the clinical characteristics of the elderly with acute pancreatitis. The disease severity (the APACHE II score and CT severity index) and the clinical outcome (the number of hospital days and mortality) were also investigated. 2.4. Statistical analysis The data is presented as mean S.D. for continuous variables. Comparison of the nominal data between groups was performed using the x2-test and Fisher’s exact test. Continuous variables between groups were compared with the Student’s t-test. All statistical analyses were carried out using SPSS 15.0 software (SPSS, Chicago, IL, USA). The p < 0.05 was considered statistically significant. 3. Results 3.1. The clinical and laboratory data of the patients according to the age groups The patients’ clinical and laboratory findings are summarized in Table 1. There were 227 patients in our study, including 85 elderly patients and 142 non-elderly patients. The mean age of the elderly patients was 72.3 5.5 years and that of the non-elderly patient was 44.7 11.7 years. Of the 85 elderly patients, 45 were men and 40 were women. For the non-elderly patients, 94 were men and 48 were women. Current smokers and heavy drinkers were significantly predominant among the non-elderly patients (p < 0.001). Comorbidities such as hypertension and previous stroke were significantly more common among the elderly patients. However, diabetes
Table 1 The clinical features and laboratory data of the patients with acute pancreatitis according to the age groups, n, mean S.D., n(%). Elderly
Non-elderly
p<
Number Age (years) Male/female Current smoker Heavy drinker BMI (kg/m2) Obesity Diabetes mellitus Hypertension COPD Coronary heart disease Previous stroke Liver cirrhosis Malignant disease White blood cell
85 72.3 5.5 45/40 12(14.1) 15(17.6) 23.3 3.4 26(30.6) 21(24.7) 34(40.0) 6(7.1) 6(7.1) 7(8.2) 1(1.2) 3(3.5) 11.5 5.0
142 44.7 11.7 94/48 66(46.5) 65(45.8) 23.9 3.7 52(36.6) 23(16.2) 35(24.6) 12(8.5) 3(2.1) 3(2.1) 6(4.2) 2(1.4) 12.0 4.4
0.001 0.047 0.001 0.001 0.237 0.354 0.117 0.015 0.707 0.065 0.030 0.198 0.292 0.514
count (103/dl) Hematocrit (%) BUN (mg/dl) Creatinine (mg/dl) Bicarbonate (mmol/l) Sodium (mmol/) Potassium (mmol/l) SAP (IU/l) Amylase (U/l) Lipase (U/l) AST (IU/l) ALT (IU/l) CRP (mg/dl)
40.2 5.1 19.1 9.9 1.08 0.55 23.6 3.2 138.4 4.7 3.9 5 0.51 161.4 120.6 892.7 827.0 11065.1 14185.4 309.8 529.1 208.9 275.5 6.02 7.90
42.8 5.9 15.2 12.5 1.08 1.28 22.4 4.2 137.1 4.6 3.96 0.45 122.6 78.0 663.6 1136.6 7634.4 11225.7 160.2 278.0 149.2 240.4 6.85 9.00
0.001 0.014 0.966 0.057 0.041 0.866 0.004 0.085 0.066 0.006 0.100 0.499
Notes: Obesity was defined as a BMI 25.
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Table 2 The etiology of the patients with acute pancreatitis, n(%).
Number Alcoholic acute pancreatitis Biliary acute pancreatitis Idiopathic acute pancreatitis Miscellaneous acute pancreatitis
Elderly
Non-elderly
p<
85 15(17.6) 48(56.5) 22(25.9) 0(0)
142 65(45.8) 42(29.6) 34(23.9) 1(0.7)
0.001 0.001 0.743 0.438
Table 3 The severity of the patients with acute pancreatitis, mean S.D.
Number CT severity index APACHE II APACHE II-age
Elderly
Non-elderly
p<
85 1.7 1.5 9.3 2.5 4.0 2.7
142 2.2 1.3 4.9 2.9 3.6 2.6
0.015 0.001 0.326
Note: APACHE II-age was defined as an APACHE II score except the age factor.
mellitus, chronic obstructive pulmonary disease (COPD), coronary heart disease, liver cirrhosis and malignant disease were not different between both groups. For the laboratory findings, the BUN, bicarbonate, sodium, SAP and AST levels were significantly higher in the elderly patients. The hematocrit was lower in the elderly patients.
Table 5 The etiology and severity of the patients who had necrotizing pancreatitis according to the age group, n, n(%), or mean S.D.
Number Alcoholic acute pancreatitis Biliary acute pancreatitis Idiopathic acute pancreatitis CT severity index APACHE II APACHE II-age
Elderly
Non-elderly
p<
3 1(33) 0(0) 2(67) 5.6 2.1 11 0.0 5.3 0.6
9 7(78) 1(11) 1(11) 4.6 1.3 6.0 2.7 5.1 2.8
0.151 1.000 0.127 0.459 0.023 0.454
Table 6 The clinical outcomes of the patients with acute pancreatitis, n, mean S.D. or n(%).
Hospital stay (days) Overall acute pancreatitis (n = 227) Alcoholic acute pancreatitis (n = 80) Biliary acute pancreatitis (n = 90) Idiopathic acute pancreatitis (n = 56) Miscellaneous acute pancreatitis (n = 1) Mortality
Elderly
Non-elderly
p<
10.3 9.6 9.6 4.9 8.8 7.7 14.0 14.3 NA 3(3.5)
11.0 10.1 13.0 13.5 9.4 5.1 9.2 6.0 5 1(0.7)
0.619 0.115 0.663 0.153 NA 0.117
Note: NA = not applicable.
3.3. The severity evaluation of the patients according to the age group 3.2. The etiology of patients according to the age group The etiology of the elderly patients was significantly different from that of the non-elderly patients. For the elderly patients, biliary pancreatitis was the most common cause (56.5% vs. 29.6%, respectively, p < 0.001), but alcoholic pancreatitis (45.8% vs. 17.6%, respectively, p < 0.001) (Table 2) was the most common cause for the non-elderly patients. Idiopathic pancreatitis was the second most common etiology for the elderly patients (25.9%). For the non-elderly patients, the second most common cause was biliary pancreatitis (29.6%). There was I case of autoimmune pancreatitis in the non-elderly group.
Table 4 The clinical features and laboratory data of the patients having necrotizing pancreatitis according to the age group, n, mean S.D., n(%).
Number Age (years) Male/female Current smoker Heavy drinker BMI Obesity Diabetes mellitus Hypertension COPD Previous stroke Coronary heart disease Liver cirrhosis Malignant disease White blood cell count (103/dl) Hematocrit (%) BUN (mg/dl) Creatinine (mg/dl) Bicarbonate (mmol/l) Sodium (mmol/l) Potassium (mmol/l) SAP (IU/l) Amylase (U/l) Lipase (U/l) AST (IU/l) ALT (IU/l) CRP (mg/dl)
Elderly
Non-elderly
p<
85 72.3 1.5 1/2 0(0) 1(33) 22.8 3.4 0(0) 1(33.3) 1(33.3) 0(0) 0(0) 0 (0) 0 (0) 1(33.3) 16.5 2.8 41.1 3.1 17.3 4.5 0.70 0.44 22.7 1.5 136.4 4.0 3.97 0.65 95.7 7.5 1000.7 1117.7 8245.7 10483.3 51.3 26.0.1 48.7 38.1 12.5 6.3
142 40.6 13.7 7/2 4(44) 7(78) 22.8 3.4 0(0) 1(11.1) 2(22.2) 0(0) 1(11.1) 0 (0) 0 (0) 0 (0) 12.6 5.5 43.9 5.6 19.4 19.3 1.36 1.79 21.1 4.0 142.7 3.5 3.82 0.50 106.1 40.9 1701.6 3921.9 4547.6 4600.6 122.1 117.9 56.3 33.4 8.7 11.2
0.001 0.151 0.157 0.151 0.433 1.000 0.455 1.000 1.000 0.546 1.000 1.000 0.250 0.137 0.642 0.307 0.457 0.710 0.064 0.750 0.679 0.644 0.782 0.518 0.644 0.433
In our study, three severity scores (the APACHE II score, the CT severity index score and the APACHE II-age score (the APACHE II except the age score)) were determined and collected (Table 3). The mean CT severity index score was 1.7 1.5 for the elderly patients and 2.2 1.3 for the non-elderly patients, respectively. The CT severity index score was significantly higher for the non-elderly patients (p = 0.015). But the APACHE II score was 9.4 2.4 for the elderly patients and 4.9 2.9 for the non-elderly patients, respectively. The APACHE II score was significantly higher for the elderly patients (p < 0.001). Interestingly, the APACHE II-age score was not significantly different between both groups (p = 0.326). We further compared the clinical characteristics of necrotizing pancreatitis in both groups (Tables 4 and 5). We found no difference in the demographic features and laboratory findings between both subgroups (Table 4). The etiology, CT severity index and APACHE II-age score were not different between both subgroups. Only the APACHE II score was significantly higher for the elderly patients with necrotizing pancreatitis (Table 5). The hospital stay was not significantly different between both subgroups (the elderly group: 16.3 10.4 days vs. the non-elderly group: 11.6 6.9 days, p = 0.519). The mortality rate was not significantly different either between both subgroups (0% vs. 0%, respectively). 3.4. Evaluation of the clinical outcome of the patients according to the age group The hospital stay was not significantly different between the elderly group and the non-elderly group (10.3 9.6 days vs. 11.0 10.1 days, respectively, p = 0.641) (Table 6). The hospital stay according to the etiology was not significantly different between both groups. The morality rate was not significantly different between both groups (3.5% vs. 0.7%, respectively, p = 0.148) (Table 6). 4. Discussion Due to the steadily increasing lifespan, the elderly patients with acute pancreatitis comprise an increasingly large portion of population. However, there have been relatively few reports in the recent years about acute pancreatitis in the elderly, as well as
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the limited available clinical data about elderly patients with acute pancreatitis. In this retrospective study, we compared the clinical characteristics between the elderly patients (65 years old) and the non-elderly patients (<65 years old). We paid special attention to the age-related clinical differences of patients with acute pancreatitis and to the question of whether age is an independent risk factor. We showed that chronological age itself had no significant influence on the clinical outcome in spite of the different etiologies and severity among the two age groups. In our study, biliary pancreatitis was the most common cause for acute pancreatitis in the elderly group. However, alcohol was the most common etiology in the non-elderly group. In most studies, two etiological factors, biliary disease and alcohol abuse, together accounted for more than 80% of the acute pancreatitis patients (Gloor et al., 2001; Flint et al., 2004). Breakdown of the incidence by etiology and gender gave a consistent picture across these previous studies: biliary acute pancreatitis was more common in the female subjects; alcoholic acute pancreatitis was more common in the middle-age male subjects (Eland et al., 2000; Floyd et al., 2002; Yadav and Lowenfels, 2006). The incidence of biliary acute pancreatitis increased in both genders (and especially in the female subjects) with age, and especially after 65 years of age (Yadav and Lowenfels, 2006). Our results are in accordance to this incidence trend. Concerning the incidence of idiopathic pancreatitis, the frequencies of idiopathic pancreatitis in the elderly (22.5%) and non-elderly (23.9%) in our study were similar to those reported from other previously published studies (Lee et al., 1992; Steinberg and Tenner, 1994; Ballinger et al., 1996; Bai et al., 2007a,b). Although most patients with acute pancreatitis have a mild and self-limited clinical course, it is generally known that elderly patients with acute pancreatitis have a severe and life threatening disease (De Beaux et al., 1995; McKay et al., 1999). There are many methods that can be used to assess the severity of acute pancreatitis. In study by Kaya et al. (2007), it has recently been demonstrated that the APACHE II score is the best predictor of mortality among the Ranson, Imrie and APACHE II scores (Ranson, 1982; Blamey et al., 1984). We found that the APACHE II score was significantly higher for the elderly patients. Unexpectedly, the CT severity index of the elderly patients was lower than that for the non-elderly patients. It seems that the average local pathological conditions in the elderly were less serious than those in the young patients. One study suggested that the likelihood of prolonged pancreatitis or serious complication is negligible when the CT severity index is 1 or 2 (Balthazar, 2002). In our current study, the mean CT severity index score was 1.7 1.5 for the elderly patients and 2.2 1.3 for the non-elderly patients, respectively. Most of the patients in both groups had mild acute pancreatitis. However, even if contrast-enhanced CT is considered the gold standard for diagnosing pancreatic necrosis, early scanning for predicting the severity is limited because the full extent of pancreatic necrosis may not develop within the first 48 h of presentation (Ryu, 2009). As described above, the CT index score could be underestimated. But our data showed that the non-elderly group with alcoholic pancreatitis has a tendency of showing a severe CT grading score. These findings are in agreement with those of some previous studies, which showed that patients with idiopathic pancreatitis and those with alcoholic pancreatitis had a higher risk of developing severe pancreatitis than did the patients with biliary pancreatitis or other disease etiologies (Singh and Simsek, 1990; Chen et al., 2006). In our study, chronological age had no significant influence on mortality and the length of the hospital stay. As we did not consider the elderly patients’ physiologic age, it seems that the APACHE II score system overestimated the severity of acute pancreatitis for the elderly patients, as compared to their clinical outcome. There was no clear trend toward higher mortality and a
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longer duration of the hospital stay for the elderly patient. Age alone was not an independent risk factor. Regarding age and the mortality rates, no obvious association was found between these 2 factors, and we have not firmly reached a consensus about this. This is dissimilar to the report by Frey et al. (2006) which, to the best of our knowledge, is the largest sample size clinical study of acute pancreatitis, and it indicated that an advanced age was significantly related to morality and that age was an independent factor for mortality. However, their study’s limitations were the striking differences in the observed racial and age distributions among the subgroups; there were predominant differences of the incidence rates of the etiologies among the different racial/ethnic groups. Because of these limitations, it was impossible to directly compare Frey et al. (2006)’s study with our study. Our clinical outcome results are in line with the study by Lankisch et al. (1996), who revealed that the increase in the mortality rate with age was only weakly significant, which is also similar with results of Fan et al. (1988), who reported that the mortality rate of acute pancreatitis was not significantly different between the elderly patients and the young patients (Bai et al., 2007a,b). When only considering those who died of acute pancreatitis in Fan et al.’s study, there was no difference between the age groups: 5.9% of the patients <50 years died and 10.6% of the patients >75 years died (Fan et al., 1988). In the study by Lankisch et al. (1996), there was no linear correlation between the age groups, nor was the duration of the hospital stay significantly different among the age groups. One potential weakness of the APACHE II is that the patients older than 65 years have very high scores and there is a possibility of a false-positive score in that age group (Kaya et al., 2007). It was reasonable to presume that age alone cannot affect the outcome of acute pancreatitis due to other confounding factors such as gender, etiology and comorbidities, which can determine the outcome (Bai et al., 2007a,b). The limitations of our study were its retrospective design and a single center experience. However, our subjects were a consecutively enrolled cohort without arbitrary selection, and our review of the medical and radiological data was meticulously performed. The etiology, severity and clinical outcome of acute pancreatitis were evaluated by strict criteria, and complete data was obtained based on the evaluation and management protocol of our institute. All the subjects were ethnic Koreans. In conclusion, chronological age had no significant influence on the clinical outcome in spite of the different etiologies and severity of disease. The influence of age on the clinical outcomes of patients with acute pancreatitis is as yet uncertain. Conflict of interest statement None. Acknowledgements Jang Eon Kim and Jin-Hyeok Hwang contributed equally to this work as first author. This study was supported by grant no 112010-002, the Seoul National University Bundang Hospital Research Fund. References Bai, Y., Jia, L., Wang, B., Yang, B., Wang, L., Shi, X., Zhang, W., Liu, Y., Zou, D., Li, Z., 2007. Acute pancreatitis in the Guangdong Province, China. Digestion 75, 74– 79. Bai, Y., Liu, Y., Jia, L., Jiang, H., Ji, M., Lv, N., Huang, K., Zou, X., Li, Y., Tang, C., Guo, X., Peng, X., Fang, D., Wang, B., Yang, B., Wang, L., Li, Z., 2007. Severe acute pancreatitis in China: etiology and mortality in 1976 patients. Pancreas 35, 232–237.
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The clinical outcome of elderly patients with acute pancreatitis is not different in spite of the different etiologies and severity Jang Eon Kim a,b, Jin-Hyeok Hwang b, Sang Hyub Lee b,*, Byung Hyo Cha b, Young Soo Park b, Jin-Wook Kim b, Sook-Hyang Jeong b, Nayoung Kim b, Dong Ho Lee b a
Division of Gastroenterology, Department of Internal Medicine, Seoul Medical Center, 171-1 Samsung-dong, Gangnam-gu, Seoul 135-090, South Korea Department of Internal Medicine, Seoul National University College of Medicine, Seoul National University Bundang Hospital, 300 Gumi-dong, Bundang-gu, Seongnam-si, Gyeonggido 463-707, South Korea b
A R T I C L E I N F O
A B S T R A C T
Article history: Received 15 October 2010 Received in revised form 13 January 2011 Accepted 14 January 2011 Available online 17 February 2011
The aim of this study was to investigate the overall clinical characteristics of elderly patients with acute pancreatitis. We retrospectively evaluated 227 consecutively enrolled patients who were admitted with acute pancreatitis. The clinical features, the radiological and laboratory data and the clinical outcome were analyzed according to the age groups (65 years vs. <65 years). Among the 227 enrolled patients with acute pancreatitis, there were 85 elderly patients and 142 non-elderly. The mean age of the elderly patients was 72.3 5.5 years and that of the non-elderly was 44.7 11.7 (p < 0.001). For the elderly patients, biliary pancreatitis was the most common cause (56.5%), but alcoholic pancreatitis was most common in the non-elderly patients (45.8%). Although the computed tomography (CT) severity index was significantly higher for the non-elderly patients (p < 0.001), the acute physiology and chronic health evaluation (APACHE II) score was significantly higher for the elderly than that for the non-elderly (p < 0.001). However, the duration of the hospital stay (10.3 9.6 days vs. 11.9 10.1 days, p = 0.619) and mortality (3.5% vs. 0.7%, p = 0.148) were not different between the age-groups. In our study, chronological age had no significant influence on the clinical outcome in spite of the different etiologies and severity of acute pancreatitis. ß 2011 Elsevier Ireland Ltd. All rights reserved.
Keywords: Acute pancreatitis in elderly Etiology of acute pancreatitis Severity of acute pancreatitis Outcome of pancreatitis
1. Introduction Acute pancreatitis is an acute inflammatory disease of the pancreas that frequently involves the peripancreatic tissues and/ or remote organ systems (Banks, 1997). Acute pancreatitis has consistently increased in Western countries over the past decades (Eland et al., 2000; Floyd et al., 2002; Tinto et al., 2002; Goldacre and Roberts, 2004; Yadav and Lowenfels, 2006; Singla et al., 2009). In Korea, the annual incidence of acute pancreatitis per 100,000 people has likewise increased from 15.6 in 1995 to 19.4 in 2000 (Kim, 2003). With the increased life span, elderly patients now comprise a large proportion of the population. As a result, physicians are more often being faced with acute pancreatitis in elderly patients (Gullo et al., 1994; Kang et al., 1998). Acute pancreatitis is a potentially fatal disease with an overall mortality of 2.1–7.8% (Eland et al., 2000; Floyd et al., 2002; Tinto et al., 2002; Kim, 2003; Goldacre and Roberts, 2004; Yadav and Lowenfels, 2006; Singla et al., 2009). However, more
* Corresponding author. Tel.: +82 31 787 7042; fax: +82 31 787 7051. E-mail address: [email protected] (S.H. Lee). 0167-4943/$ – see front matter ß 2011 Elsevier Ireland Ltd. All rights reserved. doi:10.1016/j.archger.2011.01.004
than 80% of these patients have mild acute pancreatitis and it resolves itself without serious complications (Wang et al., 2009). The association of the severity of acute pancreatitis with age is still controversial. One study showed that the overall mortality rate of elderly patients with acute pancreatitis increased from 2% for those under 55 years of age to 11% for older patients (De Beaux et al., 1995). Another study reported that the mortality rate of patients with acute pancreatitis and who were aged 70 years was three-fold more increased as compared to that for the patients who were under 60 years (McKay et al., 1999). However, some studies reported that the mortality rate of acute pancreatitis was not significantly different between the elderly patients and younger patients (Fan et al., 1988; Lankisch et al., 1996). The association of age with the severity of acute pancreatitis has been focused on by several studies. However, while the management of acute pancreatitis has recently improved and the most of the patients have mild acute pancreatitis, not many studies have evaluated the comprehensive clinical characteristics of elderly patients with acute pancreatitis in the recent years. The aim of this study was to investigate the comprehensive clinical characteristics of elderly patients with acute pancreatitis.
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2. Patients and methods 2.1. Patients We retrospectively evaluated the demographic features and the laboratory and radiology data of 227 consecutively enrolled patients with acute pancreatitis. These patients were admitted to Seoul National University Bundang Hospital from April, 2003 to March, 2009. However, if the patients with acute pancreatitis were diagnosed with chronic pancreatitis with acute execration, post endoscopic retrograde cholagiopancreatography (ERCP) pancreatitis or a tumorous condition, including pancreatic cancer, intraductal papillary mucinous neoplasm (IPMN) and mucinous cystic neoplasm (MCN), then they were excluded. The study protocol was approved by the Institutional Review Board of our hospital. 2.2. Definition of events Acute pancreatitis was defined as typical abdominal pain associated with elevated levels of serum amylase to more than 3 times the upper normal limit (normal range: 30–100 IU/). All the patients showed radiologic imaging (ultrasonography, abdomen contrast-enhanced CT and magnetic resonance imaging) that was compatible with acute pancreatitis. Co-morbidity was defined a preexisting disease or condition in addition to the acute pancreatitis. Clinical severity evaluations were carried out using the APACHE II (Knaus et al., 1985) and CT severity index scoring systems within 48 h after admission (Balthazar et al., 1990). The diagnostic criteria for severe acute pancreatitis were an APACHE II score of more than 8 within 48 h after admission. Necrotizing pancreatitis was defined as the appearance of pancreatic or extra-pancreatic necrosis on the contrast-enhanced CT and a serum C-reactive protein (CRP) value of more than 150 mg/l (Sakorafas et al., 1999; Buchler et al., 2000; Forsmark and Baillie, 2007). Serial abdominal contrast-enhanced CT was performed for all patients on admission and the findings were graded according to the Balthazar classification (Balthazar et al., 1990). The etiology was considered to be of an alcoholic origin when the patient had consumed more than 40 g ethanol in the form of ‘‘soju’’ (Korean vodka) per day (20 g in female) for at least 5 years or the patient had consumed excessive alcohol shortly before the onset of the disease (Lin et al., 2001; Chen et al., 2006; Bai et al., 2007a,b). A serum triglyceride level more than 1000 mg/dl and exclusion of other etiologies were accepted as the hyperlipidemic etiology (Kyriakidis et al., 2005). Biliary pancreatitis was defined as gall stones and sludge were found on subsequent ultrasonography, contrast-enhanced CT, or ERCP after other etiologic factors (such as alcohol and hyperlipidemia) have been excluded. The miscellaneous etiologic factors included trauma and autoimmune disease. All the patients with no identifiable etiology were classified as having idiopathic pancreatitis. On admission, all the patients were treated medically according to generally accepted principles, which consisted of stopping the oral intake, providing pain relief, restoring fluids and electrolytes intravenously and administering prophylactic antibiotics. An endoscopic sphincterotomy was done if stones and sludge were present in the common bile duct and some patients with this condition were treated with endoscopic nasobiliary drainage. Necrectomy was performed for the patients with clinical deterioration and for those with infected necrosis, which was diagnosed by fine needle aspiration under CT guidance. 2.3. Data analysis The demographic data (age, gender, smoking, body mass index (BMI)), the data on co-morbidities and etiologies and the
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laboratory data, including the white blood cell count, the hematocrit and the blood urea nitrogen (BUN), creatinine, bicarbonate, sodium, potassium, serum alkaline phosphatase (SAP), amylase, lipase, aspartate aminotransferase (AST), alanine transaminase (ALT) and CRP levels, were analyzed according to the age groups (<65 years vs. 65 years) to clarify the clinical characteristics of the elderly with acute pancreatitis. The disease severity (the APACHE II score and CT severity index) and the clinical outcome (the number of hospital days and mortality) were also investigated. 2.4. Statistical analysis The data is presented as mean S.D. for continuous variables. Comparison of the nominal data between groups was performed using the x2-test and Fisher’s exact test. Continuous variables between groups were compared with the Student’s t-test. All statistical analyses were carried out using SPSS 15.0 software (SPSS, Chicago, IL, USA). The p < 0.05 was considered statistically significant. 3. Results 3.1. The clinical and laboratory data of the patients according to the age groups The patients’ clinical and laboratory findings are summarized in Table 1. There were 227 patients in our study, including 85 elderly patients and 142 non-elderly patients. The mean age of the elderly patients was 72.3 5.5 years and that of the non-elderly patient was 44.7 11.7 years. Of the 85 elderly patients, 45 were men and 40 were women. For the non-elderly patients, 94 were men and 48 were women. Current smokers and heavy drinkers were significantly predominant among the non-elderly patients (p < 0.001). Comorbidities such as hypertension and previous stroke were significantly more common among the elderly patients. However, diabetes
Table 1 The clinical features and laboratory data of the patients with acute pancreatitis according to the age groups, n, mean S.D., n(%). Elderly
Non-elderly
p<
Number Age (years) Male/female Current smoker Heavy drinker BMI (kg/m2) Obesity Diabetes mellitus Hypertension COPD Coronary heart disease Previous stroke Liver cirrhosis Malignant disease White blood cell
85 72.3 5.5 45/40 12(14.1) 15(17.6) 23.3 3.4 26(30.6) 21(24.7) 34(40.0) 6(7.1) 6(7.1) 7(8.2) 1(1.2) 3(3.5) 11.5 5.0
142 44.7 11.7 94/48 66(46.5) 65(45.8) 23.9 3.7 52(36.6) 23(16.2) 35(24.6) 12(8.5) 3(2.1) 3(2.1) 6(4.2) 2(1.4) 12.0 4.4
0.001 0.047 0.001 0.001 0.237 0.354 0.117 0.015 0.707 0.065 0.030 0.198 0.292 0.514
count (103/dl) Hematocrit (%) BUN (mg/dl) Creatinine (mg/dl) Bicarbonate (mmol/l) Sodium (mmol/) Potassium (mmol/l) SAP (IU/l) Amylase (U/l) Lipase (U/l) AST (IU/l) ALT (IU/l) CRP (mg/dl)
40.2 5.1 19.1 9.9 1.08 0.55 23.6 3.2 138.4 4.7 3.9 5 0.51 161.4 120.6 892.7 827.0 11065.1 14185.4 309.8 529.1 208.9 275.5 6.02 7.90
42.8 5.9 15.2 12.5 1.08 1.28 22.4 4.2 137.1 4.6 3.96 0.45 122.6 78.0 663.6 1136.6 7634.4 11225.7 160.2 278.0 149.2 240.4 6.85 9.00
0.001 0.014 0.966 0.057 0.041 0.866 0.004 0.085 0.066 0.006 0.100 0.499
Notes: Obesity was defined as a BMI 25.
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Table 2 The etiology of the patients with acute pancreatitis, n(%).
Number Alcoholic acute pancreatitis Biliary acute pancreatitis Idiopathic acute pancreatitis Miscellaneous acute pancreatitis
Elderly
Non-elderly
p<
85 15(17.6) 48(56.5) 22(25.9) 0(0)
142 65(45.8) 42(29.6) 34(23.9) 1(0.7)
0.001 0.001 0.743 0.438
Table 3 The severity of the patients with acute pancreatitis, mean S.D.
Number CT severity index APACHE II APACHE II-age
Elderly
Non-elderly
p<
85 1.7 1.5 9.3 2.5 4.0 2.7
142 2.2 1.3 4.9 2.9 3.6 2.6
0.015 0.001 0.326
Note: APACHE II-age was defined as an APACHE II score except the age factor.
mellitus, chronic obstructive pulmonary disease (COPD), coronary heart disease, liver cirrhosis and malignant disease were not different between both groups. For the laboratory findings, the BUN, bicarbonate, sodium, SAP and AST levels were significantly higher in the elderly patients. The hematocrit was lower in the elderly patients.
Table 5 The etiology and severity of the patients who had necrotizing pancreatitis according to the age group, n, n(%), or mean S.D.
Number Alcoholic acute pancreatitis Biliary acute pancreatitis Idiopathic acute pancreatitis CT severity index APACHE II APACHE II-age
Elderly
Non-elderly
p<
3 1(33) 0(0) 2(67) 5.6 2.1 11 0.0 5.3 0.6
9 7(78) 1(11) 1(11) 4.6 1.3 6.0 2.7 5.1 2.8
0.151 1.000 0.127 0.459 0.023 0.454
Table 6 The clinical outcomes of the patients with acute pancreatitis, n, mean S.D. or n(%).
Hospital stay (days) Overall acute pancreatitis (n = 227) Alcoholic acute pancreatitis (n = 80) Biliary acute pancreatitis (n = 90) Idiopathic acute pancreatitis (n = 56) Miscellaneous acute pancreatitis (n = 1) Mortality
Elderly
Non-elderly
p<
10.3 9.6 9.6 4.9 8.8 7.7 14.0 14.3 NA 3(3.5)
11.0 10.1 13.0 13.5 9.4 5.1 9.2 6.0 5 1(0.7)
0.619 0.115 0.663 0.153 NA 0.117
Note: NA = not applicable.
3.3. The severity evaluation of the patients according to the age group 3.2. The etiology of patients according to the age group The etiology of the elderly patients was significantly different from that of the non-elderly patients. For the elderly patients, biliary pancreatitis was the most common cause (56.5% vs. 29.6%, respectively, p < 0.001), but alcoholic pancreatitis (45.8% vs. 17.6%, respectively, p < 0.001) (Table 2) was the most common cause for the non-elderly patients. Idiopathic pancreatitis was the second most common etiology for the elderly patients (25.9%). For the non-elderly patients, the second most common cause was biliary pancreatitis (29.6%). There was I case of autoimmune pancreatitis in the non-elderly group.
Table 4 The clinical features and laboratory data of the patients having necrotizing pancreatitis according to the age group, n, mean S.D., n(%).
Number Age (years) Male/female Current smoker Heavy drinker BMI Obesity Diabetes mellitus Hypertension COPD Previous stroke Coronary heart disease Liver cirrhosis Malignant disease White blood cell count (103/dl) Hematocrit (%) BUN (mg/dl) Creatinine (mg/dl) Bicarbonate (mmol/l) Sodium (mmol/l) Potassium (mmol/l) SAP (IU/l) Amylase (U/l) Lipase (U/l) AST (IU/l) ALT (IU/l) CRP (mg/dl)
Elderly
Non-elderly
p<
85 72.3 1.5 1/2 0(0) 1(33) 22.8 3.4 0(0) 1(33.3) 1(33.3) 0(0) 0(0) 0 (0) 0 (0) 1(33.3) 16.5 2.8 41.1 3.1 17.3 4.5 0.70 0.44 22.7 1.5 136.4 4.0 3.97 0.65 95.7 7.5 1000.7 1117.7 8245.7 10483.3 51.3 26.0.1 48.7 38.1 12.5 6.3
142 40.6 13.7 7/2 4(44) 7(78) 22.8 3.4 0(0) 1(11.1) 2(22.2) 0(0) 1(11.1) 0 (0) 0 (0) 0 (0) 12.6 5.5 43.9 5.6 19.4 19.3 1.36 1.79 21.1 4.0 142.7 3.5 3.82 0.50 106.1 40.9 1701.6 3921.9 4547.6 4600.6 122.1 117.9 56.3 33.4 8.7 11.2
0.001 0.151 0.157 0.151 0.433 1.000 0.455 1.000 1.000 0.546 1.000 1.000 0.250 0.137 0.642 0.307 0.457 0.710 0.064 0.750 0.679 0.644 0.782 0.518 0.644 0.433
In our study, three severity scores (the APACHE II score, the CT severity index score and the APACHE II-age score (the APACHE II except the age score)) were determined and collected (Table 3). The mean CT severity index score was 1.7 1.5 for the elderly patients and 2.2 1.3 for the non-elderly patients, respectively. The CT severity index score was significantly higher for the non-elderly patients (p = 0.015). But the APACHE II score was 9.4 2.4 for the elderly patients and 4.9 2.9 for the non-elderly patients, respectively. The APACHE II score was significantly higher for the elderly patients (p < 0.001). Interestingly, the APACHE II-age score was not significantly different between both groups (p = 0.326). We further compared the clinical characteristics of necrotizing pancreatitis in both groups (Tables 4 and 5). We found no difference in the demographic features and laboratory findings between both subgroups (Table 4). The etiology, CT severity index and APACHE II-age score were not different between both subgroups. Only the APACHE II score was significantly higher for the elderly patients with necrotizing pancreatitis (Table 5). The hospital stay was not significantly different between both subgroups (the elderly group: 16.3 10.4 days vs. the non-elderly group: 11.6 6.9 days, p = 0.519). The mortality rate was not significantly different either between both subgroups (0% vs. 0%, respectively). 3.4. Evaluation of the clinical outcome of the patients according to the age group The hospital stay was not significantly different between the elderly group and the non-elderly group (10.3 9.6 days vs. 11.0 10.1 days, respectively, p = 0.641) (Table 6). The hospital stay according to the etiology was not significantly different between both groups. The morality rate was not significantly different between both groups (3.5% vs. 0.7%, respectively, p = 0.148) (Table 6). 4. Discussion Due to the steadily increasing lifespan, the elderly patients with acute pancreatitis comprise an increasingly large portion of population. However, there have been relatively few reports in the recent years about acute pancreatitis in the elderly, as well as
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the limited available clinical data about elderly patients with acute pancreatitis. In this retrospective study, we compared the clinical characteristics between the elderly patients (65 years old) and the non-elderly patients (<65 years old). We paid special attention to the age-related clinical differences of patients with acute pancreatitis and to the question of whether age is an independent risk factor. We showed that chronological age itself had no significant influence on the clinical outcome in spite of the different etiologies and severity among the two age groups. In our study, biliary pancreatitis was the most common cause for acute pancreatitis in the elderly group. However, alcohol was the most common etiology in the non-elderly group. In most studies, two etiological factors, biliary disease and alcohol abuse, together accounted for more than 80% of the acute pancreatitis patients (Gloor et al., 2001; Flint et al., 2004). Breakdown of the incidence by etiology and gender gave a consistent picture across these previous studies: biliary acute pancreatitis was more common in the female subjects; alcoholic acute pancreatitis was more common in the middle-age male subjects (Eland et al., 2000; Floyd et al., 2002; Yadav and Lowenfels, 2006). The incidence of biliary acute pancreatitis increased in both genders (and especially in the female subjects) with age, and especially after 65 years of age (Yadav and Lowenfels, 2006). Our results are in accordance to this incidence trend. Concerning the incidence of idiopathic pancreatitis, the frequencies of idiopathic pancreatitis in the elderly (22.5%) and non-elderly (23.9%) in our study were similar to those reported from other previously published studies (Lee et al., 1992; Steinberg and Tenner, 1994; Ballinger et al., 1996; Bai et al., 2007a,b). Although most patients with acute pancreatitis have a mild and self-limited clinical course, it is generally known that elderly patients with acute pancreatitis have a severe and life threatening disease (De Beaux et al., 1995; McKay et al., 1999). There are many methods that can be used to assess the severity of acute pancreatitis. In study by Kaya et al. (2007), it has recently been demonstrated that the APACHE II score is the best predictor of mortality among the Ranson, Imrie and APACHE II scores (Ranson, 1982; Blamey et al., 1984). We found that the APACHE II score was significantly higher for the elderly patients. Unexpectedly, the CT severity index of the elderly patients was lower than that for the non-elderly patients. It seems that the average local pathological conditions in the elderly were less serious than those in the young patients. One study suggested that the likelihood of prolonged pancreatitis or serious complication is negligible when the CT severity index is 1 or 2 (Balthazar, 2002). In our current study, the mean CT severity index score was 1.7 1.5 for the elderly patients and 2.2 1.3 for the non-elderly patients, respectively. Most of the patients in both groups had mild acute pancreatitis. However, even if contrast-enhanced CT is considered the gold standard for diagnosing pancreatic necrosis, early scanning for predicting the severity is limited because the full extent of pancreatic necrosis may not develop within the first 48 h of presentation (Ryu, 2009). As described above, the CT index score could be underestimated. But our data showed that the non-elderly group with alcoholic pancreatitis has a tendency of showing a severe CT grading score. These findings are in agreement with those of some previous studies, which showed that patients with idiopathic pancreatitis and those with alcoholic pancreatitis had a higher risk of developing severe pancreatitis than did the patients with biliary pancreatitis or other disease etiologies (Singh and Simsek, 1990; Chen et al., 2006). In our study, chronological age had no significant influence on mortality and the length of the hospital stay. As we did not consider the elderly patients’ physiologic age, it seems that the APACHE II score system overestimated the severity of acute pancreatitis for the elderly patients, as compared to their clinical outcome. There was no clear trend toward higher mortality and a
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longer duration of the hospital stay for the elderly patient. Age alone was not an independent risk factor. Regarding age and the mortality rates, no obvious association was found between these 2 factors, and we have not firmly reached a consensus about this. This is dissimilar to the report by Frey et al. (2006) which, to the best of our knowledge, is the largest sample size clinical study of acute pancreatitis, and it indicated that an advanced age was significantly related to morality and that age was an independent factor for mortality. However, their study’s limitations were the striking differences in the observed racial and age distributions among the subgroups; there were predominant differences of the incidence rates of the etiologies among the different racial/ethnic groups. Because of these limitations, it was impossible to directly compare Frey et al. (2006)’s study with our study. Our clinical outcome results are in line with the study by Lankisch et al. (1996), who revealed that the increase in the mortality rate with age was only weakly significant, which is also similar with results of Fan et al. (1988), who reported that the mortality rate of acute pancreatitis was not significantly different between the elderly patients and the young patients (Bai et al., 2007a,b). When only considering those who died of acute pancreatitis in Fan et al.’s study, there was no difference between the age groups: 5.9% of the patients <50 years died and 10.6% of the patients >75 years died (Fan et al., 1988). In the study by Lankisch et al. (1996), there was no linear correlation between the age groups, nor was the duration of the hospital stay significantly different among the age groups. One potential weakness of the APACHE II is that the patients older than 65 years have very high scores and there is a possibility of a false-positive score in that age group (Kaya et al., 2007). It was reasonable to presume that age alone cannot affect the outcome of acute pancreatitis due to other confounding factors such as gender, etiology and comorbidities, which can determine the outcome (Bai et al., 2007a,b). The limitations of our study were its retrospective design and a single center experience. However, our subjects were a consecutively enrolled cohort without arbitrary selection, and our review of the medical and radiological data was meticulously performed. The etiology, severity and clinical outcome of acute pancreatitis were evaluated by strict criteria, and complete data was obtained based on the evaluation and management protocol of our institute. All the subjects were ethnic Koreans. In conclusion, chronological age had no significant influence on the clinical outcome in spite of the different etiologies and severity of disease. The influence of age on the clinical outcomes of patients with acute pancreatitis is as yet uncertain. Conflict of interest statement None. Acknowledgements Jang Eon Kim and Jin-Hyeok Hwang contributed equally to this work as first author. This study was supported by grant no 112010-002, the Seoul National University Bundang Hospital Research Fund. References Bai, Y., Jia, L., Wang, B., Yang, B., Wang, L., Shi, X., Zhang, W., Liu, Y., Zou, D., Li, Z., 2007. Acute pancreatitis in the Guangdong Province, China. Digestion 75, 74– 79. Bai, Y., Liu, Y., Jia, L., Jiang, H., Ji, M., Lv, N., Huang, K., Zou, X., Li, Y., Tang, C., Guo, X., Peng, X., Fang, D., Wang, B., Yang, B., Wang, L., Li, Z., 2007. Severe acute pancreatitis in China: etiology and mortality in 1976 patients. Pancreas 35, 232–237.
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