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Original Articles: Gastroenterology: Inflammatory Bowel Disease

Rising Incidence of Paediatric Inflammatory Bowel Disease in Canterbury, New Zealand, 1996–2015

Lopez, Robert N.; Appleton, Laura; Gearry, Richard B.; Day, Andrew S.

Author Information
Journal of Pediatric Gastroenterology and Nutrition: February 2018 - Volume 66 - Issue 2 - p e45-e50
doi: 10.1097/MPG.0000000000001688
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Abstract

What Is Known

  • The incidence of paediatric inflammatory bowel disease is increasing globally.
  • Canterbury, New Zealand has one of the highest documented rates of Crohn disease and the incidence rate of inflammatory bowel disease in Canterbury has risen over time.
  • There is a relative scarcity of epidemiological data pertaining to paediatric inflammatory bowel disease from the Southern Hemisphere.

What Is New

  • The incidence rate of paediatric inflammatory bowel disease in Canterbury, New Zealand has dramatically increased between 1996 and 2015.
  • The annual incidence rates of paediatric inflammatory bowel disease in 2014 and 2015 are among the highest published worldwide.
  • The preponderance of Crohn disease over ulcerative colitis and inflammatory bowel disease unclassified in the present study is the highest that has ever been documented.

Inflammatory bowel disease (IBD) consists of Crohn disease (CD), ulcerative colitis (UC), and IBD unclassified (IBDU). A 2011 systematic review concluded that the incidence of paediatric-onset IBD was rising globally (1). Although the reasons for this remain unclear, this increase in disease burden is likely to be due to environmental factors (2).

Until recently, there has been a relative scarcity of population-based epidemiological data on IBD available on the Southern Hemisphere. The Canterbury region of New Zealand is known to have a high (3) and increasing (4) rate of IBD and especially of CD. The only study looking specifically at paediatric IBD in New Zealand (5) found that the national incidence rate was low compared with that found in Western Europe (6–13) and North America (14–16).

Recent Australian data have shown that the incidence of CD (17) and UC (18) has increased dramatically between the latter half of last century and the beginning of this one. The pattern of incidence over time in New Zealand has not yet been ascertained. The present study aimed to delineate the trend in annual incidence of paediatric IBD in Canterbury over the last 2 decades.

METHODS

Approval for this study, part of the overarching Paediatric IBD in New Zealand (PINZ) study, was obtained from the Health and Disability Ethics Committee of the Ministry of Health of New Zealand, and also from the Human Research Ethics Committee of the University of Otago.

Study Population

The inclusion criteria for the present study consisted of having a diagnosis of IBD (according to widely accepted criteria (19,20)) made in Canterbury, while aged under 16 years and resident in Canterbury at the time of diagnosis, between January 1, 1996 and December 31, 2015. New referrals to the paediatric service in Canterbury are only accepted if the patient is younger than 16 years. Relevant details on each patient were entered into a secure Microsoft Access database (Microsoft Office Professional Plus 2013, Redmond, Washington, USA).

Specific details included basic demographic details, year of IBD diagnosis, diagnostic modalities employed, and worst-ever disease phenotype (classified according to the Paris modification of the Montreal classification system (21)).

Details on family history, surgical intervention, and extraintestinal manifestations of IBD were sourced from clinical notes and letters within patient files, in keeping with the ethical approval obtained for the study. The ethnic groups used in the present study are the recognized major ethnic groups in New Zealand, namely European, Maori, Asian, Pacific peoples, and Middle Eastern/Latin American/African. In the majority of cases, each patient had only 1 ethnic group listed. In instances where more than 1 was applicable, the patient was classified as belonging to all applicable ethnic groups. In cases in which there was more than 1 family member affected, the closest degree of kinship was noted for the purposes of the present study.

Canterbury

Canterbury is located in the South Island of New Zealand and is home to 12.7% of the nation's population (22). The vast majority of Canterbury residents are ethnically European (86.9%).

The public health system in New Zealand provides nondiscretionary care to all citizens and permanent residents of the country. In addition, elective care is available for a fee in the private sector. Approximately one quarter of New Zealanders under the age of 16 years have private health insurance (23). In Canterbury, public hospital-level care is provided by the Canterbury District Health Board (CDHB) and the South Canterbury District Health Board.

Within the Canterbury region, there is only 1 paediatric gastroenterologist (A.S.D.). Before his appointment in 2009, paediatric gastroenterological care in Canterbury was jointly provided by adult gastroenterologists, general paediatricians, and paediatric surgeons.

Specialized paediatric gastroenterological care is only available through the public system in Canterbury. There are 2 adult gastroenterologists based at Christchurch Hospital who also see a small number of older children in their private practices.

Case Recruitment

Information on every patient receiving paediatric gastroenterological care for IBD in the South Island since 2009 has been prospectively collected by one of the study authors (A.S.D.). All patients from that source meeting the inclusion criteria for this study were entered into the PINZ database.

A second database known as the Canterbury IBD project formed the basis of another author's PhD research and contained information on every patient diagnosed with IBD who was resident in Canterbury in 2004, that is, a prevalent cohort at that point in time. Again, this database was searched for patients who met the inclusion criteria of the present study.

Further to that, a list of every patient seen and treated in Christchurch Hospital between 1990 and 2015 with a clinically coded diagnosis of either “CD,” “Crohn,” “UC,” “colitis,” “proctitis,” “inflammatory bowel disease,” “IBD,” or “IBDU” or a slight variation of any of those, was obtained from the CDHB. Beyond that, histology results between 1996 (when Christchurch Hospital pathology results started becoming computerized) and 2015 were sought on any patient ages 16 and under that contained the above-mentioned terms.

To account for the bias of having a prospectively collected database since 2009, patients diagnosed from that year onwards were also searched for in the clinical-coding and histology lists. Using this approach, 93.4% of cases, which ended up in the final numbers were able to be identified. This provided excellent internal validity of the study methodology employed.

To ensure a complete capture of patients, every adult gastroenterologist and paediatric surgeon practising in Christchurch and Canterbury, respectively was contacted and informed about the present study. The vast majority of them either did not provide care for paediatric patients or said that the patients younger than 16 years with IBD that they have seen will have been referred to Christchurch Hospital. Patients who met the inclusion criteria and cared for by 2 of them were entered into the PINZ database.

Notes on each identified patient were then examined methodically. Those who did not meet criteria for IBD diagnosis or who were diagnosed either outside of the study time period, nonresident or diagnosed outside of Canterbury, or when older than 16 years of age were excluded. In every instance, electronic patient records were studied. If there was any ambiguity, the hard-copy case notes were retrieved to ensure accuracy of data collection.

Data Analysis

Population estimates for every year between 1996 and 2015 (inclusive) were obtained from Statistics New Zealand (22). During this 20-year time frame, 4 nationwide census were carried out—in 1996, 2001, 2006, and 2013. For years where no census was conducted, a population estimate of 0 to 15 year olds as of the 30th of June of each of those years was provided. The figures obtained were stratified by sex and age.

Annual incidence rates were calculated for IBD, CD, UC, and IBDU for each of those 20 years with the respective number of new diagnoses within the calendar year serving as the numerator and the population estimate for that year serving as the denominator. Incidence rates are reported per 100,000 population.

All raw information was analysed descriptively. Age ranges and follow-up period are given as median with relevant interquartile ranges. Exact binomial confidence intervals for the incidence rates were calculated because of the low numbers in some of the age groups. The Mann-Whitney and Kruskal-Wallis tests were used to compare mean incidence rates between different time frames. Linear regression analysis was performed to evaluate the trend in annual incidence rates. Statistical significance was accepted if P < 0.05. All statistical analysis was performed using GraphPad Prism version 6.00 (GraphPad Software, La Jolla, CA).

RESULTS

Overview of Paediatric Inflammatory Bowel Disease in Canterbury, 1996–2015

A total of 161 children were diagnosed with IBD in Canterbury between 1996 and 2015. Of these 143 had CD (3 were reclassified after initial diagnosis as IBDU [n = 2] or UC [n = 1]), 17 had UC and 1 IBDU. The annual incidence rate over the time period is given in Table 1. The median follow-up period, calculated as whole years between the year of diagnosis and December 31, 2015, was 7 years (3–12 years). The set-up of the health system meant that notes on all included patients being managed by adult services within the CDHB were readily available. In a small number of cases, follow-up data were incomplete (data not shown).

TABLE 1
TABLE 1:
Number of new diagnoses of paediatric inflammatory bowel disease, Crohn disease, ulcerative colitis, and inflammatory bowel disease unclassified, per year, in Canterbury, New Zealand between 1996 and 2015

Canterbury had a population increase of 0 to 15-year olds between 1996 and 2015. In 1996, the population of 0- to 15-year olds in the region was 104,320. That figure had increased to 114,780 in 2015. During the 20-year study period, the mean population of 0- to 15-year olds in Canterbury was 110,716.

Annual Incidence of Paediatric Inflammatory Bowel Disease in Canterbury, 1996–2015

The lowest annual incidence during the study period was 2.81/100,000 (0.56–8.20), in 2001. The highest annual incidence rate was in 2014—13.17/100,000 (7.37–21.73). The mean annual incidence of paediatric IBD in Canterbury between 1996 and 2015 was 7.18/100,000 (5.55–8.81). During the last 10 years of the study period (2006–2015) the mean annual incidence was 9.73/100,000 (7.97–11.48), whereas for the last 5 years of the study period (2011–2015) the mean annual incidence was 10.54/100,000 (7.25–13.84).

When the mean annual incidence rates during 5-year time frames were analysed, there was a significant increase in the difference between the mean annual incidence of paediatric IBD in Canterbury between 1996 and 2000 and 2006 and 2010 (P < 0.05), and between 1996 and 2000 and 2011 and 2015 (P < 0.01; Fig. 1). Linear regression analysis revealed a statistically significant increase in the annual incidence rates during the 20-year study period (P < 0.01; Fig. 1).

FIGURE 1
FIGURE 1:
Trend of PIBD annual incidence in Canterbury from 1996 to 2015 (r = 0.677; P < 0.0001). PIBD = paediatric inflammatory bowel disease.

Demographics of Paediatric Inflammatory Bowel Disease in Canterbury

There were 100 (62.1%) boys with IBD during the study period. Of the 143 cases of CD, 91 (63.6%) were boys and the rest girls, whereas 9 (52.9%) of the 17 cases of UC were boys. The sole case with IBDU was girl.

An exact age at diagnosis, taken as the date of initial endoscopic assessment, was available in 88 cases (83 CD, 5 IBDU/UC). The median age of diagnosis overall was 12.6 years (9.4–14.6) with the age at diagnosis of CD being 12.6 years (9.4–14.6) and of UC/IBDU being 12.3 years (9.6–15.2).

The majority of patients included in the study identified as being European (86.5%). Five (3.1%) identified as Maori, 6 (3.7%) identified as Asian and 2 (1.2%) as Pacific Islander. In 14 (8.7%) cases, ethnicity data were not available. To provide some perspective, in 2013, 86.9% of the Canterbury population was European, whereas the percentage of Maori, Asian, and Pacific Islander peoples was 8.1, 6.9, and 2.5, respectively (13).

Among the study cohort, 40 (24.8%) patients had a documented family history of IBD. In 14 cases, the affected family member was a first-degree relative, whereas in 11 cases the affected family member was a second-degree relative. In 14 cases the affected family member was a third-degree relative or greater, whereas in 1 case the affected family member was not documented.

Paris Classification of Paediatric Inflammatory Bowel Disease in Canterbury

All cases with CD were classified according to their disease location (Table 2). In 4 (2.8%) instances, patients had CD affecting either their upper gastrointestinal (GI) tract and/or perianal region without any lower intestinal involvement.

TABLE 2
TABLE 2:
Age, disease location, and disease behaviour of 143 children with Crohn disease using Paris classification

Nearly one-fifth of patients with CD had perianal involvement, whereas 80 (55.9%) had known upper GI involvement. The latter figure is likely an under-representation as in 33 cases of CD, upper GI endoscopy was either not performed or the result not available.

The vast majority (81.1%) of cases had inflammatory CD with 17 (11.9%), 5 (3.5%), and 5 (3.5%) patients having a stricturing, penetrating, and stricturing and penetrating phenotype, respectively.

Of the cases with UC, 3 had proctitis, 1 had left-sided colitis, 10 had pancolitis, and in the remaining 3 cases, disease extent information was unavailable.

Surgery for Paediatric Inflammatory Bowel Disease in Canterbury

Of the 161 cases with paediatric IBD included in the study, 36 (22.4%) required IBD-related surgery. Of those who required surgery, 32 had CD whereas the rest had UC. The children with CD had a range of procedures (Table 3). All 4 patients with UC who underwent surgery had colectomies. Two had ileoanal pouches formed, whereas 2 others had an ileostomy with a rectal stump remaining.

TABLE 3
TABLE 3:
Surgical intervention in 36 children with inflammatory bowel disease since diagnosis

Extraintestinal Manifestations of Paediatric Inflammatory Bowel Disease in Canterbury

Of the patients newly diagnosed with paediatric IBD between 1996 and 2015, 22 (13.7%) had a history of extraintestinal involvement at some point after diagnosis. All of these patients had CD. Five patients had IBD-related arthralgia, systemic arthritis, and ankylosing spondylitis. Dermatological involvement, which consisted of erythema nodosum and nonspecific cutaneous manifestations, was noted in 5 patients. Nonspecific liver dysfunction, autoimmune hepatitis, and/or primary sclerosing cholangitis were documented in 6 cases. Orofacial involvement, defined in the present study as mouth ulcers and orofacial granulomatosis (with intestinal IBD) was present in 5 patients, whereas 3 patients had episcleritis.

Investigation Modalities Used at the Time of Diagnosis

Of the 161 new diagnoses of paediatric IBD between 1996 and 2015, complete diagnostic information was available on 143 (88.8%). Of these, all had colonoscopy and 106 (74.1%) had an upper GI endoscopy at the time of diagnosis.

Two of the 137 children were strongly suspected of having IBD at laparoscopy and this was confirmed at endoscopy shortly thereafter. Another patient had a CT abdomen suggestive of CD, which was again confirmed endoscopically. One patient was diagnosed on small bowel imaging in spite of normal endoscopy and histology in the context of a suggestive clinical and biochemical presentation.

Fifty-seven (39.9%) of the 143 cases had dedicated small bowel imaging within 6 months of a formal diagnosis. Thirty-eight of these patients had magnetic resonance enterography, 13 had barium meal and follow-through, 3 had capsule endoscopy, and a further 3 had a CT abdomen, as part of their work-up, which provided adequate visualization of the small bowel. One child had distal colitis and did not require dedicated small bowel imaging based on national guidelines (24).

DISCUSSION

The annual incidence of paediatric IBD in Canterbury has risen dramatically during the 20-year study period. There was a more than 4-fold increase in the incidence rate between the first and last years of the study period—the incidence of paediatric IBD in Canterbury in 1996 being 2.88/100,000 versus 13.06/100,000 in 2015. There were also significant increases in the mean annual incidence rates of each 5-year block of the last 2 decades and, between the first and last 5-year blocks over the same time frame. Results from the present study are among the highest incidence rates of paediatric IBD documented anywhere in the literature.

Much of the published descriptive epidemiology of paediatric IBD has come from Western Europe and North America. In Scotland, the incidence of paediatric IBD had increased by 76% to 7.82/100,000 children between 2003 and 2008 compared to an incidence of 4.45/100,000 between 1990 and 1995 (6). Similarly in Wessex, in the south of England, the incidence of paediatric IBD between 2008 and 2012 was 9.37/100,000 compared to an incidence of 6.39/100,000 between 2002 and 2006 (25). Both these British studies included patients younger than 16 years of age, as with the present study. In Ireland, a retrospective population-based survey (7) found a national, age-adjusted mean annual incidence of 3.9/100,000 children. A Welsh survey (8), run via the Welsh Paediatric Surveillance Unit (similar to the only previous New Zealand study (5) looking at paediatric IBD), reported an annual incidence rate of paediatric IBD of 2.6/100,000 children.

From Scandinavia, annual incidence rates of paediatric IBD reportedly vary from 5.65/100,000 children in a north-eastern region of Norway (9) to 7.0/100,000 children in Southern Finland (13). Of note, the latter study included children up to the age of 17 years in its calculations. A prospective 12-year study (11) conducted in northern France reported a mean annual incidence of paediatric IBD of 3.1/100,000 children, whereas a retrospective Spanish study reported an increase to 2.8/100,000 children in 2009 (12).

To our knowledge, the highest incidence rates of paediatric IBD reported in the literature is that of 12.8/100,000 children per year, which was documented in northern Stockholm (26). It is here worth noting that the incidence rates reported in the present study in 2014 and 2015 were 13.17 and 13.06/100,000 children, respectively. Population-based data from Ontario, Canada have shown an increase in IBD incidence rates (15) with paediatric-specific incidence (including young children up to 18 years) rising from 9.5 to 11.4 per 100,000 between 1994 and 2005 (14). The most significant population-based study to emerge from the United States on paediatric IBD documented a state-wide incidence of paediatric IBD of 9.5/100,000 children in Wisconsin in 2009 (16).

A retrospective Australian study (17) reported an increased incidence rate of paediatric CD from 0.13 to 2.0 per 100,000 children between 1971 and 2001. This same group documented an 11-fold increase in the incidence of paediatric-onset UC between 1950 and 2009 (18).

Between 2002 and 2003, a prospective survey was undertaken via the New Zealand Paediatric Surveillance Unit with the aim of ascertaining the incidence, presentation, and initial management of paediatric IBD in the country (5). The estimated incidence rates during the study period were 2.9, 1.9, and 0.2 per 100,000 children per year for IBD, CD, and UC, respectively. Among the 52 new cases of paediatric IBD included in the study, 66% comprised CD, 17% UC, and 17% IBD-U.

Another remarkable finding from the present study is the preponderance of CD over UC among paediatric IBD in Canterbury. The 8.4:1 ratio of CD to UC among all paediatric patients with IBD in the region is the highest reported in the literature. This striking disparity is in keeping with the previously reported exponential and ongoing (4) rise of CD in the region, in contrast to the relatively stable incidence of UC (3). Complete histopathological results from initial endoscopy were available on 103 (72%) of the CD cases included. Thirty-six (35%) of those patients had granulomas present on biopsy. The low number of patients diagnosed with IBDU in the present study (3; including 2 who were later reclassified as CD) is also noteworthy.

With regards to disease phenotype, the predominance of inflammatory, ileocolonic CD and that of pancolonic UC amongst the current cohort is in keeping with other similar studies (10,27–29). The rate of surgical intervention and extraintestinal manifestations of IBD in the present study are again comparable with previous reports (27,29).

Insofar as data retrieval for the present study is concerned, more than 1 methodology was employed permitting internal validation. In the main, the present study's design was retrospective in nature, although information on paediatric IBD diagnoses in Canterbury since 2009 have been collected in a prospective fashion. Although no effort was spared in ensuring the completeness of information gathered (both from the public and private sectors), it is possible that some cases may have been overlooked. Also, some of the required details were not available from a small number of the cases included.

The nature of healthcare practices in Canterbury makes the likelihood of IBD care for local children being sought, exclusively, in another centre almost nonexistent. The centralization of paediatric gastroenterology in the region and the co-operation between paediatric and adult medicine in Canterbury, and among the CDHB and South Canterbury District Health Board, ensured that the present study was well-supported and truly population based.

The rates of upper gastrointestinal tract endoscopy and small bowel imaging at diagnosis, although relatively low, are probably reflective of historical practice and care provided before the appointment of a specialist paediatric gastroenterologist. Each of the 37 children who did not have initial upper gastrointestinal tract endoscopy was diagnosed by adult gastroenterologists. The rate of small bowel imaging did not change during the course of the study, although many of these children went on to have this investigation later in the course of their illness (data not shown). Magnetic resonance enterography is only attempted in children aged 8 years and older, whereas the use of barium meal and follow-through is variable among paediatric gastroenterologists in New Zealand. The incomplete assessment of small bowel involvement in many cases may account for the low proportion of patients with L4b involvement based on the Paris classification system.

There are a few factors, which could explain the increased incidence of paediatric IBD in Canterbury. The appointment of a full-time paediatric gastroenterologist to the region in 2009 may well account for an increase in the number of referrals to tertiary paediatric care. It is conceivable that a greater proportion of patients are being diagnosed at a younger age as opposed to experiencing a lag to eventual diagnosis by an adult gastroenterologist. Also the earlier study (3) which reported, for the first-time, the significant burden of IBD among the Canterbury population will have invariably increased awareness of these conditions amongst medical professional and laypeople alike. The impact of the Canterbury earthquakes on the physical and emotional health of Cantabrians and on the composition of its citizenry may also be contributory.

It is very likely, however, that the increased incidence of paediatric IBD in Canterbury does represent a true increase in the occurrence of the disorder. This is particularly true when the results of other population-based epidemiological studies also, almost universally, point to an increase in disease burden. This fact lends even greater credence to the notion that environmental factors play an undeniable role in the pathophysiology of the condition.

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Keywords:

epidemiology; inflammatory bowel disease; New Zealand; paediatric

Copyright © 2017 by European Society for Pediatric Gastroenterology, Hepatology, and Nutrition and North American Society for Pediatric Gastroenterology, Hepatology, and Nutrition