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Descriptive Analysis of Infective Colitis in A Large Hospital Cohort, Features in IBD and Non-IBD Patients

Saqib Mumtaz, Sarah Kelly, Simon Everett

Saqib Mumtaz, Sarah Kelly, Simon Everett, Leeds Gastroenterology Institute, Leeds Teaching Hospitals, Leeds, the United Kingdom

Conflict-of-interest statement: The author(s) declare(s) that there is no conflict of interest regarding the publication of this paper.

Open-Access: This article is an open-access article which was selected by an in-house editor and fully peer-reviewed by external reviewers. It is distributed in accordance with the Creative Commons Attribution Non Commercial (CC BY-NC 4.0) license, which permits others to distribute, remix, adapt, build upon this work non-commercially, and license their derivative works on different terms, provided the original work is properly cited and the use is non-commercial. See: http: //creativecommons.org/licenses/by-nc/4.0/

Correspondence to: Saqib Mumtaz, Leeds Gastroenterology Institute, St James University Hospital. Beckett Street, Leeds. LS97TF, the United Kingdom.
Email: drsaqibmumtaz@gmail.com
Telephone: +441132433144
Fax: +441132429722

Received: April 23, 2018
Revised: May 12, 2018
Accepted: May 17, 2018
Published online: June 21, 2018

ABSTRACT

BACKGROUND: Clinical features associated with infective colitis and flare up of Inflammatory Bowel Disease (IBD) are very similar and presents a challenge to gastroenterologists to distinguish the two. This is especially difficult in patients with established IBD disease in whom the incidence of bacterial infections is comparable to the general population.

METHODS: This was a retrospective analytical cohort study conducted at Leeds Teaching Hospitals (LTHT), UK. Subjects included were those with diarrhoeal symptoms, referred by the emergency department or primary care physicians to the Gastroenterology unit of LTHT, over an eight-year period between 2004-2012, with a positive stool culture for Campylobacter, Salmonella, Shigella or E.Coli O157.

RESULTS: We analysed 102 consecutive cases. Median duration of symptoms was 4 days (IQR 2-7). The most common reported symptom was abdominal pain 91 patients (91%), followed by rectal bleeding 53 patients (52%) and vomiting 44 patients (43%). Blood tests revealed that 98% patients had a substantially elevated C-reactive protein (CRP) concentration [median 95 mg/L (IQR 44-143)]. Thirteen patients had pre-existing IBD, who when compared to non-IBD patients, showed no difference in clinical presentation. In the IBD group, however, median platelet count was significantly higher [282 (IQR 225-415) vs 237 (IQR 194-281) p = 0.03] and haemoglobin concentration lower [12.1 (IQR 11-14) vs 14.3 (IQR 13-15) p = 0.01)].

CONCLUSIONS: In patients where infective diarrhoea is suspected a short duration of symptoms, abdominal pain and elevated CRP concentration are pointers that can support the diagnosis, whereas low Haemoglobin and high Platelet count favours a background of IBD.

Key words: Infective colitis; Diarrhoeal Inflammatory Bowel Disease

© 2018 The Author(s). Published by ACT Publishing Group Ltd. All rights reserved.

Mumtaz S, Kelly S, Everett S. Descriptive Analysis of Infective Colitis in A Large Hospital Cohort, Features in IBD and Non-IBD Patients. Journal of Gastroenterology and Hepatology Research 2018; 7(3): 2587-2591 Available from: URL: http://www.ghrnet.org/index.php/joghr/article/view/2319

INTRODUCTION

Infectious diarrhoea (ID) is any diarrhoeal illness due to an infectious aetiology and has been traditionally classified as “acute” if the duration of symptoms is less than 14 days, “persistent” if lasting more than 14 days and “chronic” if lasting more than three months[1]. Although worldwide diarrhoeal disease is the second leading cause of death[2,3], in the developed countries it is a condition that carries low mortality and morbidity. All the same, this is a major economic burden on resources in the form of absentia and accessing the health care: According to the Longitudinal study of infectious intestinal disease in the UK (IID2 study) 1 in 5 people in the UK are affected by intestinal infection with approximately 1 million GP consultations each year[4].

Globally viruses are the most common cause of ID, presenting mainly as acute watery diarrhoea, followed by bacterial pathogens that are commonly implicated in clinically severe and/or bloody diarrhoea[3]. Observational studies have reported a frequency between 2-10% of positive bacterial stool culture in cases of acute diarrhoea[5,6]. However, in the setting of foodborne outbreaks or in patients with severe or bloody diarrhoea, identification of bacterial pathogens increases significantly[7,8]. The IID2 study showed that most commonly identified microorganisms found in stool samples from those with ID are Norovirus, Sapovirus, Campylobacter and Rotavirus.

Infectious diarrhoea is most commonly managed expectantly in primary care. When severe, however, patients may be admitted to a variety of hospital-based specialties, commonly general medicine, infectious diseases and gastroenterology. Whilst the presentation of ID is well established in primary care, there are few studies that have rigorously analyzed the characteristics of a single cohort of patients with documented bacterial gastroenteritis in secondary care. This subject is of importance for gastroenterologists for whom a significant challenge is to determine whether an episode of bloody diarrhoea is infectious or due to another cause such as IBD. This can be particularly difficult in patients with established IBD disease in whom the incidence of bacterial infections, apart from Clostridium Difficile (C.Diff), is comparable to the general population[9-11].

The primary aim of this study is to describe the clinical features of a large, continuous unselected cohort of patients presenting to an acute gastroenterology ward with culture positive bacterial gastroenteritis, excluding C Diff. The purpose is to identify those characteristics that will enable the clinician to make a positive diagnosis of infective colitis in advance of the results of investigations such as stool culture or sigmoidoscopy. A secondary objective was to compare the clinical features of culture positive bacterial ID in patients with established IBD to those without IBD.

METHODS

Study design and setting

This was a retrospective analytical cohort study conducted at Leeds Teaching Hospitals (LTHT), which is one of the largest NHS Trusts in the UK. LTHT provides secondary and tertiary care services to a local population of approximately 800,000 and delivers specialist services to the West Yorkshire region with a population of almost 2 million. Acute and elective Gastroenterology services are spread across two sites, St James University Hospital and Leeds General Infirmary respectively providing a 24-hour Gastroenterology cover.

Patient selection and data collection

Subjects included in this study were those with diarrhoeal symptoms, referred by the emergency department or primary care physicians (GP) to the Gastroenterology unit of LTHT with a positive stool culture for Campylobacter, Salmonella, Shigella or E.Coli O157. Patients under the age of 18 years or with C. Diff infection were explicitly excluded.

Patients were identified through a search of the Leeds microbiology database for all the stool specimens positive for these microbes over an eight-year period from 2004 to 2012 for patients admitted under a gastroenterology consultant. Case notes were reviewed and patient demographic data, clinical presentation, investigations and outcome at discharge were collated and tabulated. For a twelve month follow up period post discharge, we cross checked our hospital electronic data base, discharge letters and clinic letters for subsequent admission into any speciality or any notification of death.

Statistical methods

Nonparametric tests were used. The Mann-Whitney U test was used to compare two continuous variables. To compare categorical variables, chi-squared test was used, or Fishers exact test, where there were expected cell counts of less then 5. Tests were 2-tailed and considered significant if p < 0.05. We dealt with missing data by assuming it to be the average for that value in the sample.

Ethical consideration

Anonymised data were stored on a password protected PC. Ethical approval was deemed unnecessary for a retrospective case note review.

RESULTS

The database identified 109 cases of stool culture positive bacterial gastroenteritis presenting to the gastroenterology service over the eight-year period, 13.6 cases per annum. Out of these, 6 case notes could not be retrieved and 1 patient did not present with diarrhoeal symptoms. The final analysis therefore included 102 cases. Median age was 34 years (IQR 23-61) with the majority (57%) of patients being male. Thirteen patients (13%) had pre-existing IBD whereas thirty-eight patients (42%) of the remaining 89 had at-least one clinically significant chronic condition; Diabetes Mellitus 7 patients (8%), Hypothyroidism 6 patients (7%) and Ischaemic Heart disease 6 patients (7%) being the most common conditions. Bacterial agents identified in stool microscopy were; Campylobacter 84 cases (82%), Salmonella 13 cases (13%), E Coli 4 cases (4%) and Shigella 2 cases (2%).

Clinical Features

Median duration of symptoms, from onset to hospital presentation, was short at 4 days (IQR 2-7). The most common reported symptom was abdominal pain 91 patients (91%), followed by rectal bleeding 53 patients (52%) and vomiting 44 patients (43%). (Figure 1). A relevant food history, as a trigger for the acute illness, was given by 28 patients (27%) and a recent travel history of less than three months, was present in 9 (9%) cases. Thirty five patients (34%) were documented to be on a Proton Pump Inhibitor (PPI) at the time of admission and 23 patients (22%) gave a history of variable weight loss.

Clinical observations at the time of presentation revealed; Pyrexia (Temperature > 37.5 Celsius) in 35 patients (35%), tachycardia in 28 patients (27%) and hypotension (systolic BP < 90) in 5 patients (4%).

Figure 1 Frequency of reported symptoms in patients presenting with infective colitis.

Investigations

Routine blood tests revealed that almost all patients (98%) had a substantially elevated C-reactive protein (CRP) concentration [median 95 mg/L (IQR 44-143)] yet only 16% had a raised total white cell count (WCC) [median 7.8 × 109/L (IQR 6.4-10.2)]. Median platelet count was 241 × 109/L (IQR 198-285) and haemoglobin concentration was 14 g/L (IQR 13-15). Coeliac serology was checked in 18 patients (18%) and it was positive in one case. Forty-seven patients (46%) underwent further investigations: Flexible sigmoidoscopy 34 patients (33%), Computerised tomography (CT) 7 patients (7%), Colonoscopy 2 patients (2%) and 4 patients (3%) had both CT scan and a sigmoidoscopy.

Treatment and outcome

The majority of patients did not receive any specific treatment. Antibiotics were given to 30 (29%) patients, mainly receiving either Ciprofloxacin 17 (16%) or Macrolides 9 (9%). Two patients were given Metronidazole, 2 had a combination of Cefuroxime and Metronidazole where as 1 patient was given Co-Amoxiclav. There were no major differences between the groups of patients who received antibiotics and those who did not with respect to median duration of symptoms [5 days (IQR 2-10) vs 3 days (IQR 2-5) p = 0.64], WCC [7.6 (IQR 3.9-11.9) vs 8.2 (IQR 6.6-10.7) p = 0.64] or CRP concentration [94 (IQR53-157) vs 76 (IQR 39-119) p =0.14].

Median length of hospital stay was 4 days (IQR 3-6). While most patients had an uncomplicated stay and were successfully discharged, 2 patients required admission to the High Dependency Unit. There were three in-patient deaths. Two of these patients had decompensated alcohol related liver disease (ALD) and the third was a 78 year old lady with diabetes who had a 30-day hospital admission. No patient was diagnosed as a first presentation of IBD during his or her admission with infective colitis.

During the 12 months follow up period there were no admissions with re-infection but there were 2 deaths. One patient who had decompensated ALD and the second was a 103-year-old male. Only one patient was diagnosed with Ulcerative Colitis approximately three months after the acute episode.

IBD vs. non-IBD patients

There were 13 patients in the IBD cohort (7 Ulcerative Colitis, 6 Crohn’s Disease) and 89 in the non- IBD cohort. The mean duration of symptoms was 4 days in both groups (Table 1). Both sets of patients reported symptoms with similar frequency; Abdominal pain [10 (77%) vs 81 (90%) OR 0.37 (0.08-1.6)], Vomiting [5 (38%) vs 39 (43%) OR 0.81 (0.24-2.71)], PR Bleed [6 (46%) vs 47 (52%) OR 0.78 (0.24-2.5)].

Blood tests showed that both IBD and non-IBD patients had elevated median CRP concentration [56 (IQR 36-126) vs. 87 (IQR 46-143) p = 0.46]. In the IBD group, median platelet count was significantly higher [282 (IQR 225-415) vs 237 (IQR 194-281) p =0.03)] and haemoglobin concentration lower [12.1 (IQR 11-14) vs 14.3 (IQR 13-15) p =0.01)] than the non-IBD group. Not surprisingly, a higher proportion of patients with IBD were treated with steroids [10 (77%) vs 15 (16%) OR 16.6 (95% CI 4.0-61)] and given antibiotics [7 (54%) vs 23 (25%) OR 3.3 (95% CI 1.03-11.1)] than patients without IBD.

Median length of stay was 5 days (IQR 2-6) in the IBD cohort and 4 days (IQR 2-5) in non-IBD cohort and almost all patients in both cohorts had an uncomplicated discharge. There was 1 HDU admission in each group and three inpatient deaths in the non-IBD group.

Table 1 Comparison of clinical features of infective diarrhoea between IBD and non-IBD patients.
  IBDnon-IBD 
Demographics
Age (mean/IQR)52 years (37 - 66) 31 years (22 - 60)p = 0.06
Gender (n/%) 6 (46) Males 52 (58) Males 
Stool pathogens isolated (n/%)

Camp 11 (84);

Salmonella 2 (16)

Camp 72 (81);

Salmonella 11 (12);

Ecoli 4 (4);

Shigella 2 (2)

 
History
 N = 13N = 89OR (95% CI)
Duration of symptoms (Median / IQR) 4 days (3 - 6) 4 days (2 - 7)p = 0.46
Abdominal pain (n/%) 10 (77) 81 (90) 0.37 (0.08 - 1.6)
Vomiting (n/%) 5 (38) 39 (43)0.81 (0.24 - 2.71)
PR bleed (n/%) 6 (46) 47 (52)0.78 (0.24 - 2.5)
Investigations
Routine tests  p-value
CRP (mg/L) (median/IQR) 56 (36 - 126) 87 (46 - 143)0.47
WCC (x 109 / L) (median/IQR) 7.0 (5.7 - 9.2) 7.8 (6.5 - 10.2)0.23
Plat (x 109 / L) (median/IQR) 282 (225 - 415) 237(194 - 281)0.03
Hb (g/dL) (median/IQR) 12.1 (11 - 14) 14.3 (13 - 15)0.01
Additional tests  OR (95% CI)
Flexi Sig (n/%) 6 (46) 31 (34) 1.6 (0.4 - 5.1)
Colonoscopy (n/%)02 
CT Scan (n/%) 4 (30) 6 (7) 6.1 (1.4 - 25)
Treatment
   OR (95% CI)
Steroids (n/%) 10 (77)15(16) 16.6 (4.0 - 61)
Antibiotics (n/%) 7 (54)23(25) 3.3 (1.03 - 11.1)
Outcome
Length of stay (Median / IQR) 5 days (3 - 7) 4 days (2 - 5)p = 0.20
No of Deaths03 
IBD: Inflammatory bowel disease; Camp: Campylobacter; IQR: Intra-Quartile range; OR: Odds-ratio; CI: confidence interval; CRP: C-reactive protein; WCC: White cell count; Plat: Platelet count; Hb: Haemoglobin concentration.

CONCLUSION

In this study, we have analysed a large cohort of patients presenting with bacterial ID to a gastroenterology unit in secondary care. Our findings show that ID affects all age groups with no gender predisposition. Patients admitted to hospital with bacterial ID frequently had chronic medical co-morbidities, which might either predispose to or exacerbate bacterial infections.

An important clinical feature of infective colitis demonstrated in this study is that it is usually associated with a short duration of symptoms and abdominal pain. These features remained consistent for patients with and without IBD. An unexpected finding was that patients with ID tended to have a high CRP concentration compared with usually a normal total white cell count. This is in keeping with the inflammatory nature of ID, and probably reflects the severity of the patients admitted to hospital compared with those manage in the community.

In our cohort, almost a third of patients were on a PPI. Although we cannot conclude any causal relation by our study, but the role of PPIs in the aetiology of bacterial ID remains contentious. Whereas there is good evidence that PPIs are associated with increased incidence of C Diff Infection[12,13], there is less clarity regarding their part in contributing to other enteric infections. A systematic review conducted by Leonard et al[14] showed that there was an increased risk of taking acid suppression in those with enteric infections while Brophy et al[15] concluded from their study that people who go on to be prescribed PPIs have a greater underlying risk of gastrointestinal infection beforehand.

Just under a third of patients in our study were treated with antibiotics, mainly after the culture results became available. The role of antibiotics in treating ID in immunocompetent patients in not well established. Two randomised controlled trials found that the empirical usage of antibiotics in ID shortened the duration and severity of symptoms, by a day or two, in clinically severe cases but their usage was also associated with side effects and delayed clearance of the pathogens[16,17]. A Cochrane review of use of antibiotics in non-typhoid salmonella found that in otherwise healthy people, treatment with antibiotics did not have any benefit over placebo. Treatment with antibiotics made it more likely that patients would continue to excrete the same organisms for up to one month after treatment, so treatment in healthy individuals was not recommended by the review panel[18]. However, whether a select group of hospitalized patients with more severe disease merit antibiotic treatment has not been studied.

Although our numbers were small but this study suggests that ID presents in a similar way in IBD patients as it does in non-IBD patients. This has implications as treatments are often escalated in IBD patients presenting with diarrhoeal symptoms as evidenced by the higher proportion of steroids used as initial treatment in the IBD group. Nevertheless, this did not result in any adverse outcomes, which suggest that this may not be an unreasonable strategy to employ.

The aetiology of IBD has been a matter of debate for many decades. In addition to genetic and environmental factors, microorganisms have been discussed as possibly playing an important role. A large population-based Danish study reported an incidence of 1.2% for a first-time diagnosis of IBD following a documented episode of Salmonella or Campylobacter gastroenteritis, as compared with an age- and gender-matched background population incidence of 0.5%[19]. Other studies have also drawn similar conclusions and the risk of IBD has been reported to be highest in the first-year post exposure[20,21]. Although our study was not powered to detect this, in our follow up period one patient was diagnosed with IBD, which is compatible with these data.

The strength of our study was to analyse most aspects of infective diarrhoea in a large consecutive cohort of patients. We attempted to review ID from a Gastroenterology prospective. A comparison between IBD and non-IBD group is not something that has been attempted before. The main limitation was including only culture positive episodes of ID because of the potential to miss culture negative patients owing to the reported variability in stool culture yields in acute diarrhoea, as mentioned above[5-8]. However, for a retrospective analysis, the only definite method of reliably identifying episodes of ID was to include culture positive episodes only. We excluded virus etiology of ID from our study because they are less likely to mimic IBD.

It can be challenging to diagnose infective diarrhoea at the outset, not only in patients with no pre-existing bowel conditions but especially in patients with IBD. After having reviewed a large cohort of patients with culture positive gastroenteritis presenting to a gastroenterology department, we conclude that in patients where ID is suspected a short duration of symptoms, abdominal pain and elevated CRP concentration are pointers that can support the diagnosis.

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Peer Reviewer: Luis Rodrigo

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