Appendicitis

Appendicitis presenting as the ! rst manifestation of

colorectal carcinoma: a 13-year retrospective study

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Rebecca J Shine, Abigail Zarifeh, Chris Frampton, Jeremy Rossaak

Colorectal cancer (CRC) rates in New Zealand are among the highest in the Western world, with an overall rate of ~50/100,000 person years and between 1,100 and 1,200 deaths each year.1,2 Early diagnosis and treatment are paramount to improving outcomes for colorectal cancer. However, symptoms can be vague, and patients often have advanced disease at presentation.

Acute appendicitis in older adults is relatively uncommon and could represent the fi rst presentation of an underlying colorectal carcinoma, affording the oppor- tunity for earlier diagnosis and treatment. Colorectal carcinoma may cause acute appendicitis either by way of direct obstruction of the appendiceal lumen or as a result of adjacent infl ammation and oedema. Also, a partial downstream colonic obstruction may result in increased luminal pressures and thus predispose to acute

appendicitis. Alternatively, immune-me- diated lymphoid hyperplasia associated with malignancy may lead to appendiceal obstruction and appendicitis.3,4

In the early 1980s, a number of small studies and case reports indicated increased rates of CRC in older patients presenting with appendicitis.4–8 Interest waned with the advent of computed tomography and laparoscopic surgery in the management of appendicitis with the theory one could visualise the cecum through these interventions. However, a Taiwanese study in 2006 reported an almost 40-fold increase in odds ratio for under- lying colorectal cancer in patients over 40 presenting with acute appendicitis.9 Given the higher rates of colorectal cancer and a predominance of left-sided malignancies in the western world,1,2 it is diffi cult to interpret the results of the Taiwanese study in the New Zealand population.

ABSTRACT AIM: Appendicitis in older adults may present as the first sign of underlying colorectal cancer. We aim to determine whether there was a di! erence in the rate of diagnosis of colorectal carcinoma for patients “45 years following a presentation with appendicitis, compared with New Zealand standardised rates. METHOD: Retrospective study of patients “45 years with a confirmed diagnosis of appendicitis from 2003 to 2015 inclusive. The rate of colorectal carcinoma diagnosed during the 36-month follow-up period was calculated and compared to standardised rates, as per the New Zealand cancer registry. RESULTS: Six hundred and twenty-nine patients were included for analysis, 15 had a diagnosis of colorectal cancer in the follow-up period. Patients “45 years had a 6.3-fold (CI 3.6–10.2) increased risk of colorectal carcinoma than predicted given the population demographics. Those patients aged between 45–60 years had a 17-fold (95% CI 8–32.2) increased standardised risk ratio. CONCLUSION: This is the first study of its kind conducted in Australasia. This study found patients “45 years who present with appendicitis have significantly increased risk of underlying colorectal cancer. Until further research is conducted the authors recommend clinicians consider colonic investigation for older adults following a diagnosis of appendicitis.

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A recent survey presented at the New Zealand Association of General Surgeons (NZAGS) conference10 (March 2016) has shown a signifi cant dichotomy in practice among general surgeons with regards to colonic investigation in older adults following appendicitis. The survey found almost a 50:50 split with regards to colonic investigation following appendicitis in older adults, indicating the current uncertainty and limited evidence relating to this issue.

The aim of this study was to determine whether there was a difference in the rate of diagnosis of colorectal carcinoma for patients ≥45 years in the 36 months following a presentation with appendicitis to the Bay of Plenty DHB, compared with the New Zealand population standardised rates.

Methods All patients ≥45 years with a certain

pathological or radiological diagnosis of appendicitis from January 2003 to April 2015 inclusive were eligible to be included in the study. Cases were identifi ed through a database code for ‘Appendicitis’ or related codes from the Bay of Plenty District Health Board’s (BOPDHB) admission and theatre database. Diagnostic and demographic data for all patients were extracted, and this information was cross-referenced with the pathological (PATHLAB) database for ‘appendicitis’ and ‘colorectal cancer’ in patients ≥45 years to ensure no cases were missed. Each case was then reviewed both electronically and from paper charts for date of diagnosis of appendicitis, subsequent colonoscopy date and fi ndings, pre-existing risk factors for colorectal cancer and, for those patients diagnosed with colorectal cancer, histology, staging and date of diag- nosis. Stage of colorectal cancer was defi ned according to the American Cancer Society TNM staging 7th edition.

The study focus was to identify patients who had colorectal cancer at the time of presentation with appendicitis, with the theory being that the tumour may have precipitated the appendicitis. For this reason, a 36-month follow-up period was elected. This was chosen to minimise the

bias that would be created by a longer follow-up, as patients may ‘develop’ a new cancer during a longer follow-up that was unrelated to the episode of appendicitis. A 36-month follow-up period was thought most appropriate as cancers existing at the time of appendicectomy would likely have become symptomatic and been diagnosed by three years, and those that may have developed subsequently would be less likely to be diagnosed.

A rate ‘per person years’ was deter- mined for each patient dependent on the duration they were included in the study (duration until diagnosis of CRC, death, or for 36 months maximum) and from this, the ‘observed rate’ for this study popu- lation was established. An ‘expected rate’ of colorectal carcinoma was calculated for each patient based on age, gender, year of diagnosis and ethnicity (Māori or non- Māori) status as extracted from the New Zealand cancer register ICD codes 9 and 10. The ‘standardised rate ratio’ was then calcu- lated as the ratio of ‘observed’ rates over the ‘expected’ population rate. The Poisson approximation was used to estimate the 95% confi dence limits for the standardised ratio estimates.

Results A total of 667 patients were identifi ed

initially from the BOPDHB database with a diagnosis of acute appendicitis within the study period. This was cross-referenced with the PATHLAB database, and no addi- tional patients were identifi ed. 38 patients were excluded (25 with a normal appendix on histology, 10 patients had an alternative diagnosis such as diverticulitis or undiffer- entiated abdominal pain and three patients had acute appendicitis diagnosed intra-op- eratively during a bowel resection for an already known colorectal cancer). Two patients were diagnosed with colorectal cancer >36 months after their admission for appendicitis, and these patients were included only as ‘appendicitis’ patients. The average follow-up period was 30.36 months as patients presenting towards the end of the study period did not have a full 36-month follow-up period.

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Table 1 highlights the demographic profi le for this patient group, which is represen- tative of the BOPDHB population during this period. ‘Acute appendicitis’ was the most common histological fi nding, although an alternative neoplastic process other than colorectal carcinoma was found in 4.1% of specimens (Table 2). Thirty-six patients had their appendicitis managed non-operatively, 14 of whom (39%) went on to have either a CTC or colonoscopy at the request of the consultant surgeon. One of these patients had a diagnosis of caecal carcinoma detected at the time of colonoscopy four weeks later, the CT of this patient had shown an infl am- matory mass and acute appendicitis. There was no protocol or guideline in place in BOPDHB at the time of this study to dictate whether patients had colonic investigation after non-operative management of appen- dicitis, and this decision was at the surgeons’ discretion. Interval appendicectomy was not common practice, and only two patients who were managed non-operatively initially, went on to have further surgery—the patient who had cecal cancer detected and another who had an ongoing appendiceal abscess that was treated with a right hemi- colectomy (histology benign).

The expected risk of colorectal cancer was established for each patient in this study, dependent on their age, gender, ethnicity and year of diagnosis. From this, the ‘study-population’ expected rate of cancer was calculated. The expected number of colorectal cancers among this study popu- lation was two (0.4%). However, 15 patients (2.4%) were found to have colorectal cancer in the study period (Table 3). This equated

Table 1: Demographic profi le.

Demographic profile

N Percentage

Age (median, range)

57 years (45–97 years)

45–59 years 358 57.1%

60–79 years 227 36.2%

80+ years 42 6.7%

Gender

Male 330 52.5%

Female 299 47.5%

Ethnicity

NZ European 528 83.9%

M#ori 72 11.4%

Asian 14 2.2%

Other 15 2.4%

Table 2: Findings, management and location of colorectal cancer.

Initial findings, management and location

N Percentage

Appendix histology

Acute appendicitis 541 86%

Chronic appendicitis

19 3.0%

Mucinous cystadenoma

15 2.4%

Neuroendocrine tumour

4 0.6%

Acute appendicitis and benign polyp

7 1.1%

Acute appendicitis and Adenocarcinoma

8 1.3%

No operation 36 5.7%

Pre-operative CT scan

263 41.8%

Colonoscopy (within 36 months)

74 * Mean = 8 months

11%

Follow-up period Mean = 30.36 Months

Location of CRC N (%)

Appendix 4 26.7%

Caecum 6 40%

Ascending/ transverse

2 13.3%

Sigmoid/rectum 3 20%

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to a six-fold increased standardised risk ratio (SR 6.3, 95% CI 3.6–10.2) of under- lying colorectal malignancy than would be expected given the population demo- graphics. They were all European and predominantly male (male n=13, 86.6%) with a median age of 59 (46 to 84) years. Right-sided malignancies accounted for 74%. Ten of the 15 patients had cancer located in the cecum or appendix (six and four respectively), two in the ascending/trans- verse colon and three located in the sigmoid/ rectum (Table 2). The median duration to diagnosis was 12.7 months with a range of one to 30 months. Within the age group 45 to 60 there was a 17.3-fold increased stan- dardised risk ratio (CI 8.02–32.79) as shown in Table 3. Across all age ranges there was an increased risk, though this did not reach statistical signifi cance for patients over 80 (SR 2.09, CI 0.1–10.3).

Eight patients (53%) with CRC were diag- nosed as a result of the histology from the initial specimen. Of these, four patients had cancer arising from the appendix, and the other four were found to have cecal cancer that involved the base of the appendix. Of the remaining two patients with cecal cancers; one was the patient managed non-operatively who was diagnosed on

colonoscopy one month later (performed for appendiceal abscess on initial CT), the other presented 28 months later with abdominal pain due to a T4 cecal cancer.

After excluding those patients diagnosed on initial histology, Table 4 demonstrates 7/621 (1.1%) patients were subsequently diagnosed with CRC. This represented a three-fold increased standardised risk ratio (SR 2.96, 95% CI 1.2–5.8). Patients age 45–60 continued to have more than a six-fold increased risk (SR 6.52, 95% CI 1.7–17.7) of underlying colorectal cancer, with an inci- dence of 2.2%.

Of the 629 patients included in the study, only 74 (11%) had a colonoscopy/colonog- raphy within 36 months of appendicitis, with the average duration to colonoscopy being eight months (Table 2). The indications for colonoscopy for those patients found to have malignancy varied. Aside from the patient already mentioned above, fi ve patients had ‘adenocarcinoma diagnosed on initial histology’ and required complete colonoscopy. Two patients underwent surveillance colonoscopy for chronic colitis (ulcerative and chrons) and were diagnosed with CRC two and six months post-appendi- citis. One patient presented with PR bleeding 12 months later and was found to have a

Table 3: The number of expected and observed colorectal carcinoma cases by age group.

Age range Expected number

Observed number

Standardised risk ratio (SR)

Confidence interval (95%)

All 2.37 15 6.4 3.67–10.2

45–60 0.46 8 17.27 8.02–32.79

60–80 1.43 6 4.20 1.70–8.73

>80 0.48 1 2.09 0.10–10.30

Table 4: The number of expected and observed colorectal carcinoma cases by age group after excluding those diagnosed on initial histology.

Age range Expected number

Observed number

Standardised risk ratio (SR)

Confidence interval (95%)

All 2.36 7 2.96 1.29–5.6

45–60 0.46 3 6.5 1.6–17.75

60–80 1.2 4 3.33 1.06–8.4

Expected number = Expected number of colorectal cancers derived from the national age, gender, year of diagnosis and ethnicity population rates. Observed number = Actual number of cancers observed. Standardised risk ratio = Ratio of the number of observed over the expected colorectal carcinoma cases based on national age, gender, year of diagnosis and ethnicity population rates.

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T3 rectal cancer. One patient presented six months later with a large bowel obstruction secondary to a T3, N2 rectosigmoid cancer and underwent completion colonoscopy post-Hartmann’s procedure. Finally, the last patient with a CRC presented 28 months later with change in bowel habit, and a colonoscopy found a T2, N2 tumour at the splenic fl exure.

The four remaining patients diagnosed with CRC did not have colonic investigation within BOPDHB. One patient underwent an acute right colectomy for an appendiceal abscess that contained malignancy and then moved out of area; another was diagnosed with metastatic disease on staging CT scan after appendiceal histology found malig- nancy and was palliated. The third patient was diagnosed with a T4, N0, M0 cecal cancer two and a half years later and ulti- mately died from their disease. This patient did have a colonoscopy eventually, but it was >36 months after diagnosis and eight months post-diagnosis of CRC. Finally, the last patient diagnosed with CRC on appendiceal histology was too co-morbid to undergo any further investigations or surgery.

Discussion Patients aged between 45–60 years

presenting with acute appendicitis had more than a 17-fold increased risk of an underlying CRC than would be expected given the study population demographics. Throughout all age groups, there was an increased risk of CRC with an overall risk six times greater than expected. This study supports the hypothesis that a presentation with appendicitis in patients ≥45 years may constitute a sign of underlying colorectal malignancy. After excluding those diag- nosed on initial histology there remained an increased risk especially in the age group 45–60 with over a six-fold increased risk of underlying malignancy.

It may be stated if the patient has had a reassuring pre-operative CT scan then no further investigation is required, however, in this study seven patients who were ultimately diagnosed with colorectal cancer underwent a pre-operative CT scan, only two of which raised the suspicion of colorectal cancer. A CT scan is a poor diagnostic tool with only 70% sensitivity for detecting colonic malignancies in an

unprepared bowel and even less so in the setting of acute appendicitis.11,12

Shears fi rst entertained the relationship of right-sided colon cancer presenting with acute appendicitis in 1906.5 Since then there have been a number of small case reports highlighting this relationship.4–6,8 This study supports the work by Lai HW et al in demon- strating an increased risk of underlying colon cancer in older adults with appendi- citis. Our study has a lower risk than was identifi ed in this Taiwanese study, which found an almost 40-fold increased odds ratio of colon cancer in over 40-year-olds.6 However, that study did not control for age, gender or ethnicity as was done in our study and compared only to the overall national incidence of colorectal cancer in Taiwan in the year 2000, and is therefore likely to have overstated the relationship. It also had a longer follow-up period of fi ve years and may have bias associated with this.

Although appendiceal adenocarcinoma is rare, with an expected incidence of 0.08–0.2%,13,14 within this study popu- lation, four patients (0.6%) were diagnosed with adenocarcinoma of the appendix. The study may be criticised for including these patients in the analysis as 60–70% will present with symptoms suggestive of appendicitis12 and the diagnosis will ulti- mately be confi rmed by histology. However, appendiceal adenocarcinomas are included in the ICD codes 9 and 10 for CRC as per the New Zealand Cancer Registry and therefore were included in the case defi nitions for this analysis as they are included in the baseline population rate used for comparison. Synchronous colonic neoplasms are found in up to three percent of patients with appendiceal tumours,13 and this in itself should warrant complete colonic investi- gation before defi nitive surgery.

Eight patients of the 10 patients with right-sided malignancies were diagnosed as a result of the histological fi ndings from the initial surgery, which included 70% of the cecal tumours. This supports the hypothesis that an underlying colorectal cancer, especially a right-sided cancer, can lead to appendicitis. Of the two remaining patients with right-sided malignancies; one was diagnosed one month later on follow-up colonoscopy, and the other was diagnosed 28 months later with abdominal pain due

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to a T4 cecal cancer. The remaining fi ve patients (33%) were detected a median of 12 months later, suggesting these cancers were also present at the time of appendicitis. After excluding those patients diagnosed on initial histology, there remained a three-fold increased risk among remaining patients (1.1% observed rate of CRC, expected rate 0.38%), and a six-fold increased risk in patients aged 45–60 years (2.2% observed rate, excepted rate 0.13%).

Seventy-four percent of tumours were located on the right side (Table 2) with the majority within the cecum. This distribution differs from that of the general population for colonic tumours in New Zealand,2 with right-sided tumours making up less than 30% of all colorectal malignancies. This supports the theory of obstruction of the appendiceal lumen, either through direct tumour contact or infl ammatory change around the tumour. However, the majority of these tumours were diagnosed as a result of initial histology or early after diagnosis due to abnormal imaging, indicating our current detection of these lesions is rela- tively safe. The remaining fi ve tumours located in the transverse and recto-sigmoid region still represent higher than expected numbers (Table 4). As mentioned earlier, the hypothesis of immune-mediated lymphoid hyperplasia leading to appendicitis has been raised previously and may account for this increased rate, however, given the numbers are small in this study it is diffi cult to make any clear conclusions.

Limitations included the nature of the study design, being a single-centred study, which limits its generalisability. However, despite variation in CRC rates throughout New Zealand, the Bay of Plenty has an age-standardised rate equivalent to national rates, and the results of this study should therefore be comparable to those of the general population.15 The study could also be susceptible to a type two statistical error, given the smaller study size with a rare event as the outcome studied. However, the results are similar to and supported by other studies in this area.4–9

Thorough cross-referencing between electronic clinical records and the pathology database mitigated some of the potential limitations due to the retrospective database nature of the study. Also, patients were

included in this study up until January 2015, and consequently some patients had only a short period of follow-up. If anything, this would minimise the fi ndings of this study as it may have missed a CRC diagnosis for these patients during the subsequent follow-up period.

It is also important to emphasise that given this is a retrospective non-ran- domised study the difference in CRC demonstrated in this population group could be due to a number of underlying factors that cannot be controlled for in this study design. However, this study is unique in that it standardised for age, gender and ethnicity, and therefore these attributing factors should be minimised.

The fi ndings of this study support the hypothesis that appendicitis is associated with an increased rate of underlying colorectal malignancy and may be a sign of an undiagnosed colorectal cancer. This increased risk may be attributed to those patients with appendiceal/cecal cancers with the majority of patients these diagnosed on initial histology or abnormal imaging. All patients diagnosed with colorectal cancer as a result of their initial histology warrant completion colonoscopy prior to defi nitive surgical intervention.

In those whom the histology from appen- dicectomy was benign, colonic investigation is more controversial. Three patients were ultimately diagnosed with CRC due to classic symptoms attributed to bowel cancer; large bowel obstruction, PR bleeding and change in bowel habit (six, 12 and 28 months later respectively). Two patients were diag- nosed through surveillance programmes for colitis, which has a known increased risk of CRC, and one patient presented >2 years later with abdominal pain due to a T4 caecal cancer. After excluding those diag- nosed on initial histology, there remained a three-fold increased SR (1.1% incidence) in patients >45 years and a six-fold increased risk in patients aged 45–60 (2.2% incidence). Given the numbers are small within this population group, it is diffi cult to make any defi nitive conclusions. The association of distal CRC attributing to appendicitis could be theoretically explained by either distal partial colonic obstruction or immune-me- diated lymphoid hyperplasia within the appendix, however, with small study

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numbers susceptible to type two error it would be a bold statement to recommend universal colonic investigation for these patients until further prospective studies are completed.

This is the fi rst study of its kind conducted in Australasia. The study reinforces the limited evidence that appendicitis is asso- ciated with increased risk of underlying CRC in middle-aged and older adult patients. In patients ≥45 years who present with symptoms of appendicitis, the possibility of a co-existent colonic neoplasm should

always be kept in mind, and clinicians should pay particular attention to any factors that may raise the suspicion of CRC. If a patient is managed non-operatively or the histology of the initial specimen reveals malignancy, these patients should all be offered colonic investigation. In adult patients with benign histology following appendicitis, the authors recommend clini- cians consider colonic investigation, taking into consideration individual risk factors and symptoms, particularly for those in the age range of 45–60 years.

Competing interests: Nil.

Author information: Rebecca J Shine, Registrar General Surgery, Bay of Plenty DHB; Abigail Zarifeh, House

Offi cer, Bay of Plenty DHB; Chris Frampton, Biostatistician, University of Otago, Christchurch; Jeremy Rossaak, Consultant Upper Gastrointestinal and General Surgeon, Bay

of Plenty DHB, Senior Lecturer, University of Auckland, Auckland. Corresponding author:

Dr Rebecca Jasmine Shine, 3/22 Verbena Road, Birkdale, Auckland. rshi027@gmail.com

URL: http://www.nzma.org.nz/journal/read-the-journal/all-issues/2010-2019/2017/vol-130-no-1459-

21-july-2017/7314

1. Center MM, Jemal A, Smith RA, Ward E. Worldwide Variations in Colorectal Cancer. CA: A Cancer Journal for Clinicians. 2009; 59(6):366–378.

2. Shah AB, Sarfati D, Blakely T, Atkinson J, Dennett ER. Trends in colorectal cancer incidence rates in New Zealand, 1981–2004. ANZ Journal of Surgery. 2012; 82(4):258–264.

3. Gaetke-Udager K, Maturen KE, Hammer SG. Beyond acute appendicitis: imaging and pathologic spectrum of appendiceal pathology. Emerg Radiol. 2014; 21(5):535–542.

4. Peltokallio P. Acute appen- dicitis associated with carcinoma of the colon. Diseases of the Colon & Rectum. 1966; 9(6):453–456.

5. J Hill DJL. Acute appen- dicitis and carcinoma of the colon. Journal of the Royal Society of Medicine. 1986; 79(11):678–680.

6. Arnbjörnsson E. Acute appendicitis as a sign of a colorectal carci- noma. J Surg Oncol. 1982; 20(1):17–20.

7. Temple DF, Carnevale N. Acute appendicitis as an early manifestation of carcinoma of the cecum: a case report and review of

the literature. J Natl Med Assoc. 1981; 73(5):449–451.

8. Fabri PJ, Carey LC. Cecal carcinoma presenting as acute appendicitis: a reappraisal. Journal of clinical gastroenterology. 1980; 2(2):173–4.

9. Lai HW, Loong CC, Tai LC, Wu CW, Lui WY. Incidence and odds ratio of appendicitis as fi rst manifestation of colon cancer: A retrospective analysis of 1,873 patients. J Gastroenterol Hepatol. 2006; 21(11):1693–1696.

10. A Zarrifeh, R Shine, J Rossaak. Current Practice Of Colonic Investigation

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