Abstract
Background and aims
This study aimed to describe Crohn’s disease perianal fistulizing lesions in patients undergoing surgery over 60 years to compare clinical presentation, management and outcomes with those observed in younger patients.
Methods
Between January 2012 and December 2022, all patients over 60 years old who underwent a first surgical intervention for anal fistula at two medical centers were included. For each patient included, two younger patients who underwent the same surgical procedure during the same period in the same centers were matched for comparison.
Results
Among 536 patients who underwent surgery, 6% (n = 30) aged over 60 years at first surgery were included. Compared with their younger counterparts, older patients had: i) a diagnosis of Crohn’s disease and fistula more often in the same year: 63% vs 26%, p = 0.001; ii) combined therapy and anti-TNF alpha optimization less often (p = 0.0002 and p = 0.0001); iii) fewer surgical interventions: 3 vs 4.5, p = 0.008; iv) sparing surgery less frequently: 30% vs 58%, p = 0.01; v) fistulotomy more often: 27% vs 5%, p = 0.003. The rates of anal fistula closure were comparable between the two groups: 60% vs 62%, p = 0.93.
Conclusion
Synchronous diagnosis of anal fistula and Crohn’s disease within the first year of care is not uncommon after 60 years of age, suggesting that Crohn’s disease should not be overlooked in older individuals developing an anal fistula. Despite receiving less aggressive medical management due to age-related factors, elderly patients achieved similar fistula closure rates, through a more pragmatic surgical approach, including more fistulotomies in selected patients.
Keywords: Crohn’s disease, Anal fistula, Elderly
Introduction
Diagnosis of Crohn’s disease (CD) peaks during the third decade of life [1, 2], but disease onset can occur at any age, notably among the elderly [3]. Prevalence in this older population, often defined as people aged over 60 [4, 5], is increasing globally, particularly in Europe [6, 7].Studies focusing on the elderly population have shown a milder course of luminal CD, with fewer stenotic and fistulizing forms, a majority (52 to 78%) of inflammatory forms, and less use of anti-TNF alpha therapy and immunosuppressants [8–11].Perianal fistulizing Crohn’s disease (pfCD) is less frequent in this age group with an estimated prevalence of 12 to 16% [10, 12] while rates vary from 19 to 26% in younger patients [13, 14].
Several studies have investigated luminal CD in the elderly but very few have focused on pfCD in this age group.
This study aims to describe characteristic features, management practices, clinical courses, and outcomes of pfCD in patients over 60 years old, and to compare them with those observed in a younger population receiving care in the same centers during the same period of time.
Materials and methods
Data from two referral centers, Diaconesses Croix Saint-Simon Hospital Group in Paris, and the University Hospital Pontchaillou in Rennes, France were collected retrospectively from the program of medicalization of information systems (Programme de médicalisation des systèmes d’information, PMSI) databases or department registries.
Elderly patients (EPs) aged 60 years or older at the time of their first anal surgery, who underwent surgery for an anal fistula between January 2012 and December 2022, and presenting with a known or confirmed diagnosis of CD, were included in the study. Patients initially followed for ulcerative colitis (UC) or indeterminate colitis, whose diagnosis of inflammatory bowel disease was corrected to CD after the fistula onset, were also included. All patients without available postoperative follow-up, or for whom the duration of CD was not known, were excluded. Each EP was then matched with two younger patients (YPs) with CD who underwent anal surgery in the same center within a one-month interval.
Data collection included CD history, luminal disease localization (ileal, colonic or both) and phenotype according to the Montreal classification [15]. Extraintestinal manifestations, perianal fistula onset and type according to Cardiff and AGA classifications [16, 17], medical management, surgical interventions, fistula drying and closure, fistula recurrence, and clinical evaluation at the last follow-up were also recorded.
Medical management included use of immunosuppressants (azathioprine, methotrexate, purinethol) and/or biotherapy (anti-TNF alpha, antiinterleukin 23, anti-integrin, Jak inhibitors). Surgical management involved drainage with fistulectomy and placement of a non-cutting seton, or, in case of low fistulas, fistulotomy. After appropriate medical management, occlusion treatments could be used, including techniques like advancement flap, ligation of inter-sphincteric fistula tract (LIFT), radiofrequency, biological glue injection, plug, or mesenchymal stem cell injection.
Fistulas were considered dried up when they were no longer productive either spontaneously or under digital pressure. A fistula was considered clinically closed if it was dried up with a healed external opening. Recurrence was defined as the appearance of a new abscess or undrained suppuration requiring surgical reintervention, either more than six months after fistula closure following a sphincter-sparing technique, or at any time after the last drainage. The study was conducted according to national ethical guidelines.
Statistical analysis
Quantitative variables are presented as medians and interquartile range (IQR for the 25th and 75th percentiles). Categorical variables are presented as numbers and percentages of the cohort. Statistical analysis included non-parametric Wilcoxon and non-parametric exact Pearson or Fisher tests, and log-rank tests to compare fistula closure probabilities.
A p-value ≤ 0.05 was considered significant. Statistical analyses were performed using JMP Pro 13.0.0 software. Multivariate analysis was not performed due to the population size.
Results
Among 536 patients who underwent anal surgery for pfCD between January 2012 and December 2022 in the study centers, 30 (6%) were aged 60 years and older (EPs) and were included and matched with 60 YPs (Fig. 1). (Table 1)
Fig. 1.
Flow chart
Table 1.
Population characteristics
| Elderly patients (EPs), n = 30 | Young patients (YPs), n = 60 | p | |
|---|---|---|---|
| Age at diagnosis of Crohn’s disease (years) | |||
| Median [IQR 25–75] | 67 [62–76] | 25 [18.7–32] | 0.0001 |
| Age at 1 st surgery in our centers (years) | |||
| Median [IQR 25–75] | 69 [63–76] | 34 [26–40] | |
| Sex ratio M/F | 2.0 | 1.2 | 0.28 |
| Male, n (%) | 20 (66.7%) | 33 (55.0%) | |
| Female, n (%) | 10 (33.3%) | 27 (45.0%) | |
| Comorbidities | 24 (80%) | 8 (13.3%) | < 0.0001 |
| Diabetes, n (%) | 7 (23.3%) | 0 (0%) | 0.0001 |
| Cardiovascular disease, n (%) | 23 (76.7%) | 3 (5.0%) | 0.0001 |
| - Hypertension | 18 (60%) | 1 (1.7%) | 0.0001 |
| - Ischemic heart disease | 6 (20%) | 1 (1.7%) | 0.0022 |
| - Cardiac rhythm disorder | 3 (10%) | 2 (3.3%) | 0.19 |
| - Peripheral artery disease of the lower limbs | 2 (6.7%) | 0 (0%) | 0.04 |
| - Use of antiplatelet agents | 12 (40%) | 1 (1.7%) | 0.0001 |
| - Use of anticoagulants | 3 (10%) | 2 (3,3%) | 0.19 |
| Cancer, n (%) | 9 (30%) | 5 (8.3%) | 0.008 |
| Kidney failure, n (%) | 2 (6.7%) | 0 (0%) | 0.03 |
| Smoking (n = 86) | 0.02 | ||
| No, n (%) | 14 (46.7%) | 21(35%) | |
| Former smoker, n (%) | 12 (40%) | 17 (28.3%) | |
| Yes, n (%) | 2 (6.7%) | 20 (33.3%) | |
| ASA score | 0.02 | ||
| ASA 1, n (%) | 7 (23.3%) | 28 (46.7%) | |
| ASA 2, n (%) | 14 (46.7%) | 27 (45%) | |
| ASA 3, n (%) | 9 (30%) | 5 (8.3%) | |
| Body mass index (n = 88) | 0.10 | ||
| Median [IQR 25–75] | 25.6 [22.7–27.7] | 22.6 [20.6–25.9] | |
IQR interquartile range, EPs age at first surgery ≥ 60; YPs age at first surgery < 60; ASA score American Society of Anesthesiologists score
Among EPs, 83% (25/30) were diagnosed with CD after the age of 60, and 63% (19/30) reported their fistula at the time of the CD diagnosis or within the following year. Among YPs, 52% (31/60) reported their anal fistula more than one year after the CD diagnosis (Table 2). Most fistulas were complex and high, comparably in both groups: 93% (28/30) vs 93% (56/60), p = 1 and 93% (28/30) vs 83% (50/60), p = 0.18.
Table 2.
Perianal fistulizing Crohn’s disease characteristics
| Elderly patients (EPs), n = 30 | Young patients (YPs), n = 60 | p | |
|---|---|---|---|
| Time between Crohn’s disease diagnosis and fistula onset, in months, median [IQR] | 0 [0–5.5] | 36 [0–99] | |
| < 0 months | 23% | 17% | |
| 0 to 12 months | 63% | 26% | |
| 1 to 10 years | 7% | 30% | |
| < 10 years | 7% | 22% | |
| Anal fistula classification | |||
| Cardiff 13 | 0.18 | ||
| 1, n (%) | 2 (6.7%) | 10 (16.7%) | |
| 2, n (%) | 28 (93.3%) | 50 (83.3%) | |
| AGA 14 | 1.0 | ||
| Simple, n (%) | 2 (6.7%) | 4 (6.7%) | |
| Complex, n (%) | 28 (93.3%) | 56 (93.3%) | |
| Associated anoperineal lesions | 0.3 | ||
| None, n (%) | 17 (56.7%) | 31 (51.7%) | |
| Ulceration*, n (%) | 13 (43.3%) | 25 (41.7%) | |
| Stenosis*, n (%) | 2 (6.7%) | 13 (21.7%) | |
IQR interquartile range, EPs age at first surgery ≥ 60, YPs age at first surgery < 60
*Two EPs and nine YPs had both an anal ulceration and a stenosis
No significant difference in the use of corticosteroids and biologic therapies was observed between the two groups: 47% (14/30) vs 62% (37/60), p = 0.17 and 87% (26/30) vs 97% (58/60), p = 0.07. Among the 26 EPs and the 58 YPs who received anti-TNF alpha therapy, the regimen was less frequently optimized or used in combination therapy for EPs: (38% (10/26) vs 76% (44/58), p = 0.0002 and 54% (14/26) vs 88% (51/58), p = 0.0001. EPs received immunosuppressant monotherapy less frequently than YPs: 33% (10/30) vs 58% (35/60), p = 0.02. The most frequently used immunosuppressant in both groups, whether as monotherapy or combination therapy, was azathioprine (Table 3).
Table 3.
Medical management
| Elderly patients (EPs), n = 30 | Young patients (YPs), n = 60 | p | |
|---|---|---|---|
| Corticosteroids, n (%) | 14 (46.7%) | 37 (61.7%) | 0.17 |
| Immunosuppressants | |||
| monotherapy, n (%) | 10 (33.3%) | 35 (58.3%) | 0.02 |
| Azathioprine, n (%) | 10/10 (100%) | 33/35 (94.3%) | |
| Methotrexate, n (%) | 3/10 (33.3%) | 5/35 (14.3%) | |
| Other, n (%) | 1/10 (10%) | 2/35 (5.7%) | |
| Anti-TNF alpha, n (%) | 26 (86.7%) | 58 (96.7%) | 0.07 |
| Optimization | 10/26 (38.5%) | 44/58 (75.9%) | 0.0002 |
| use in combination therapy | 14/26 (53.9%) | 51/58 (87.9%) | 0.0001 |
| agent: | |||
| - Infliximab, n (%) | 22/26 (84.6%) | 55/58 (94.8%) | |
| - Adalimumab, n (%) | 11/26 (42.3%) | 39/58 (67.2%) | |
| - Golimumab, n (%) | 0/26 (0%) | 5/58 (8.6%) | |
| Other biotherapies, n (%) | 12 (40%) | 24 (40%) | |
| - Vedolizumab, n (%) | 1/12 (8.3%) | 9/24 (37.5%) | |
|
- Ustekinumab, n (%) -Other§, n (%) |
11/12 (91.7%) 1/12 (8.3%) |
20/24 (83.3%) 6/24 (25%) |
|
EPs age at first surgery ≥ 60, YPs age at first surgery < 60
§Certolizumab, Filgotinib
EPs had fewer surgical interventions than YPs: median 3 [2-4] vs 4.5 [3–6.2], p = 0.008. Among patients who underwent drainage surgery, fistulotomy was more frequent in EPs: 28% (8/29) vs 5% (3/59), p = 0.003 (Table 4). Among the EPs treated with fistulotomy, 75% (6/8) were men, 12.5% (1/8) had a simple fistula, 25% (2/8) initially had a simple fistula at the time of fistulotomy, but later developed more complex fistulas that required additional treatment. Fistulotomy was performed after a previous fistulectomy with a non-cutting seton in 25% (2/8). Lastly, 37.5% (3/8) of patients treated with fistulotomy had at least two fistulas, one of which was complex and treated with fistulectomy with a non-cutting seton, while the other was simple and treated with fistulotomy during the same procedure. No fistulotomy was performed on high trans-sphincteric or supra-sphincteric fistulas.
Table 4.
Surgical management and outcome
| Elderly patients (EPs), n = 30 | Young patients (YPs), n = 60 | p | |
|---|---|---|---|
| Drainage, n (%) | 29 (96.7%) | 59 (98.3%) | 0.61 |
| Fistulotomy/lay-open*, n (%) | 8/29 (27.6%) | 3/59 (5.1%) | 0.003 |
| Fistulectomy/seton placement*, n (%) | 28/29 (96.5%) | 59/59 (100%) | 0.21 |
| Redo drainage, n (%) | 11 (36.7%) | 33 (55%) | 0.10 |
| Number of procedures, median [IQR] | 1 [1-2] | 2 [1-3] | |
| Simplification, n (%) | 13 (43.3%) | 22 (36.7%) | 0.54 |
| Number of procedures, median [IQR] | 1 [1-1] | 1 [1-1] | |
| Sphincter sparing surgery, n (%) | 9 (30%) | 35 (58.3%) | 0.01 |
| Total number of operations (in study centers and other centers), median [IQR] | 3 [2-4] | 4.5 [3–6.2] | 0.008 |
| Stoma for pfCD control, n (%) | 4 (13.3%) | 5 (8.3%) | 0.65 |
IQR interquartile range, EPs age at first surgery ≥ 60, YPs age at first surgery < 60
Sparing techniques were used less often in EPs compared to YPs : 30% (9/30) vs 58% (35/60), p = 0.01 (Table 4).
The median follow-up duration for anal fistulas was 58 [23.3–98.1] months. Median number of lines of medical treatment required to dry the fistulas was 1 [1-2] in EPs and 2 [1-3] in YPs, with no significant difference between the two groups (p = 0.17). The time to dry the fistulas was longer in YPs with a median of 25.5 [14, 60] months compared to 13 [9, 27] months in EPs (p = 0.02).
At last follow-up, 60% (18/30) of EPs, and 62% (37/60) of YPs had a closed anal fistula, with a shorter median time for fistula closure in EPs : 2.5 [7, 22] months versus 26 [14.5–47.2] months in YPs (Fig. 2).
Fig. 2.
Probability of fistula closure according to age
Overall mortality rate among EPs was 17% (5/30), primarily due to aplastic anemia and hepatocellular carcinoma, and no deaths occurred among YPs.
Discussion
To our knowledge, no previous study has specifically addressed the severity and clinical course of pfCD in the elderly, particularly concerning the rates and times to drying and closure of anal fistulas. This study is one of the first to specifically focus on medical-surgical management and outcomes of pfCD in older versus younger patients. Our study reveals age-related differences in the management of anal fistulas. Our older patients (EPs) underwent fewer surgical interventions overall but had a higher frequency of fistulotomies and fewer sphincter sparing procedures. This difference could be explained by a more pragmatic therapeutic strategy, favoring a reduction in the number of procedures under general anesthesia because of their iatrogenic adverse impact in this more fragile population, without systematically resorting to sphincter-sparing techniques, but always restricting fistulotomy to cases with low incontinence risk. Graham Williams et al. demonstrated that this more aggressive management strategy led to 93% of fistula healing within six months of treatment in patients aged 14 to 72 years old [18]. Papaconstantinou et al. showed that fistulotomy was effective with no recurrence and a low risk of anal incontinence in a well-selected population of CD patients presenting with simple fistulas [19].
In our series, EPs were more frequently treated with biologics compared to previous studies; 87% (26/30) were given anti-TNF alpha. Viola et al. reported only 5% of patients over 65 receiving biologics, and Danielou et al. found use in 15% of patients over 60 [8, 12]. This higher rate of biologics use in our study may be explained by greater clinical experience, leading to a deeper understanding of side effects and treatment tolerance, and allowing for broader and more frequent prescription in this population.
The rate of immunosuppressants use was lower in EPs, with 33% exposure, compared to (58%) in YPs. In previous studies, rates of use in the elderly population have ranged from 12 to 37% [8, 11, 12]. In our series, azathioprine was the most frequently used immunosuppressant in both age groups, although ECCO (European Crohn's and Colitis Organisation) recommendations suggest more cautious use in the elderly due to a higher risk of complications, notably lymphoma, as demonstrated in the CESAME study by Baugerie et al. [20, 21].
The frequency of stoma creation was comparable between the two groups, but was lower than in previous studies [12], likely due to the more frequent use of biologics, contributing to better disease control and reducing the need for a stoma.
Clinical presentation of pfCD was similar in the two groups, but the time to onset of pfCD after CD diagnosis differed: CD diagnosis and fistula onset occurred in the same year in 63% of EPs, while the anal fistula was reported more than one year after diagnosis of CD in 52% of YPs. The presence of fistulas early in the course of CD is a sign of severity, indicating an initially severe form of the disease in our elderly population [22]. Danielou et al. also highlighted this early manifestation of pfCD, noting that more than half (57%) of elderly patients reported their anal fistula before or at the time of CD diagnosis [12].
Our study identified characteristic features similar to those reported in previous studies, although our EPs had more frequent colonic involvement and inflammatory luminal disease, more comorbidities, and higher mortality rates [8, 10, 11, 23, 24]. The latter appears to be consistent with those reported in the general population for the same age group, likely reflecting a higher burden of comorbidities [24].
We found that extra- intestinal manifestations were more frequent in our YPs, a finding not noted by Viola et al. who reported similar percentages of extra-intestinal manifestations in patients under and over 65 years old [8]. Conversely, other studies have shown higher rates of extra-intestinal manifestations in elderly patients, with a predominance of skin and joint involvement in 57% and 37%, respectively [11, 12] (Table 5).
Table 5.
Crohn’s disease characteristics
| Elderly patients (EPs), n = 30 | Young patients (YPs) n = 60 | p | |
|---|---|---|---|
| Initial type of diagnosed IBD | 0.05 | ||
| Ulcerative colitis, n (%) | 8 (26.7%) | 5 (8.3%) | |
| Crohn’s disease, n (%) | 21 (70%) | 54 (90%) | |
| Indetermined colitis, n (%) | 1 (3.3%) | 1 (1.7%) | |
| Crohn’s disease localization* | 0.003 | ||
| L1 ileal, n (%) | 1 (3.3%) | 14 (23.3%) | |
| L2 colonic, n (%) | 21 (70%) | 20 (33.3%) | |
| L3 ileo-colonic, n (%) | 8 (26.7%) | 25 (41.7%) | |
| Anoperineal with no luminal involvement, n (%) | 0 (0%) | 1 (1.7%) | |
| Rectal involvement n (%) | 23 (76.7%) | 34 (56.7%) | 0.06 |
| Crohn’s disease phenotype* | 0.23 | ||
| B1 inflammatory, n (%) | 21 (70%) | 37 (61.7%) | |
| B2 stricturing§, n (%) | 3 (10%) | 16 (26.7%) | |
| B3 penetrating§, n (%) | 7 (23.3%) | 9 (15%) | |
| Extra-intestinal manifestations, n (%)‡ | 1 (3.3%) | 18 (30%) | 0.004 |
| rheumatological, n (%) | 0/1 (0%) | 11/18 (61.1%) | |
| skin/mucosal, n (%) | 0/1 (0%) | 8/18 (44.4%) | |
| Ocular, n (%) | 0/1 (0%) | 1/18 (5.6%) | |
| Other∫, n (%) | 1/1 (100%) | 0/18 (0%) |
IQR interquartile range, EPs age at first surgery ≥ 60, YPs age at first surgery < 60, IBD inflammatory bowel disease
*According to Montreal Classification12
§1 EP and 2 YPs had both stricturing and penetrating forms
‡2 patients had 2 types of extra-intestinal manifestations simultaneously: one presented with both cutaneous-mucosal and articular manifestations, while the other presented with ocular and articular manifestations
∫The only EP who had an extra-intestinal manifestation, had a diagnosis of primary sclerosing cholangitis
It should be noted that our study had certain limitations inherent to its methodology and retrospective nature. This was a small series of only 30 patients recruited from two centers over 10 years, representing about 6% of the treated population. This confirms that pfCD remains rare in individuals over 60, even in expert centers. But there is reason to speculate about an increase in prevalence related to the rise of CD in the elderly, with an aging global population and increasing life expectancy [25]. Active smoking was more prevalent in YPs, potentially biasing towards a less favorable outcome. Although active smoking has been associated with higher disease activity, increased risk of complications, recurrence, and need for luminal surgical treatment, its effect on pfCD is less well known [26].
The prevalence of complex fistulas seems higher in our series than in the literature, possibly due to the recruitment bias of expert centers [12]. Our EPs underwent fistulotomy more frequently, but only for selected simple tracts. However, due to the retrospective nature of the study and the lack of available data, we could not assess the risk of anal incontinence. Though, during follow-up, there was no record of patients requiring anoperineal rehabilitation or surgical interventions for anal incontinence, such as sacral neuromodulation, suggesting the absence of severe postoperative anal incontinence in our population.
Previous research has shown that fistulotomy is associated with an increased risk of anal incontinence [27]. However, Papaconstantinou et al. found that fistulotomy carried a low risk of anal incontinence in a well-selected population with simple fistulas [19]. The impact of preserving anal continence may vary with age, as the trade-off between longer healing times and increased risk of iatrogenic effects may be less significant for individuals over 60 than for younger patients. Therefore, the most effective treatment strategy should be tailored to each individual patient, considering their specific benefit-risk balance and primary concerns.
Conclusions
This study highlights the importance of considering underlying Crohn's disease in patients over 60 presenting a perianal fistula. It also disclosed disparity in the medical management of older patients with perianal fistulizing Crohn’s disease, who, in our series received combination therapy and optimization of anti-TNF alpha less often than their younger counterparts, largely due to age-related factors and comorbid conditions. Nevertheless, we found that a more pragmatic surgical approach, characterized by more fistulotomies in selected patients with low tract fistulas and less sparing techniques, compensated for this difference in management practices. A tailored therapeutic strategy thus led to comparable fistula healing rates between younger and older patients, demonstrating the efficacy of adapting surgical interventions to meet the unique age-related needs of older patients.
Author contributions
Dr Isabelle Etienney: conception of the study, overall supervision of data collection and analysis. Dr Oumniya Arjafallah Goulet : patient screening, data collection and analysis, writing the manuscript. Dr Charlène Brochard: patient screening, data collection and analysis. Pr Laurent Siproudhis: project supervision. All authors discussed the results, provided critical feedback and helped shape the research and contributed to the final manuscript.
Data availability
No datasets were generated or analysed during the current study.
Declarations
Competing interests
Dr. Isabelle Etienney declares having served as a speaker for Takeda, Tillotts, and MSD. Pr. Laurent Siproudhis declares having received educational support from Takeda, AbbVie, Janssen, and Ferring, as well as research support from Takeda and Janssen. Additionally, he has acted as a consultant for Takeda. The other authors declare no conflicts of interest.
Conference poster presentation
19th Congress of the European Crohn’s and Colitis Organization (ECCO), 21-24/02, 2024, Stockholm, Sweden.
Journées Francophones d’hépato-gastroentérologie et d’oncologie digestive (JFHOD), 14-17/03/2024, Paris, France.
Footnotes
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
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Associated Data
This section collects any data citations, data availability statements, or supplementary materials included in this article.
Data Availability Statement
No datasets were generated or analysed during the current study.