Techniques in Coloproctology (2023) 27:897–907 https://doi.org/10.1007/s10151-023-02840-z ORIGINAL ARTICLE Clinical characterization of patients with anal fistula during follow‑up of anorectal abscess: a large population‑based study E. Sanchez‑Haro1 · E. Vela2 · M. Cleries2 · S. Vela1 · I. Tapiolas1 · J. Troya1 · J.‑F. Julian1 · D. Parés1 Received: 16 May 2023 / Accepted: 19 June 2023 / Published online: 7 August 2023 © The Author(s) 2023 Abstract Purpose Approximately 15–50% of patients with an anorectal abscess will develop an anal fistula, but the true incidence of this entity is currently unknown. The aim of the study was to determine the incidence of anorectal abscess and development of a fistula in a specific population area and to identify potential risk factors associated with demographic, socioeconomic and pre-existing disease (e.g. diabetes and inflammatory bowel disease). Methods A longitudinal observational study was designed including a large cohort study in an area with 7,553,650 inhabit- ants in Spain 1st january 2014 to 31st december 2019. Adults who attended for the first time with an anorectal abscess and had a minimum of 1-year follow-up were included. The diagnosis was made using ICD-10 codes for anorectal abscess and anal fistula. Results During the study period, we included 27,821 patients with anorectal abscess. There was a predominance of men (70%) and an overall incidence of 596 per million population. The overall incidence of anal fistula developing from abscesses was 20%, with predominance in men, and a lower incidence in the lowest income level. The cumulative incidence of fistula was higher in men and in younger patients (p < 0.0001). On multivariate analysis, patients aged 60–69 years (hazard ratio 2.0) and those with inflammatory bowel disease (hazard ratio 1.8–2.0) had a strong association with fistula development (hazard ratio 2.0). Conclusions One in five patients with an anorectal abscess will develop a fistula, with a higher likelihood in men. Fistula formation was strongly associated with inflammatory bowel disease. Keywords Anal abscess · Anal fistula · Risk factors Introduction cause of a long-term anorectal fistula. In a non-inflammatory bowel disease clinical setting, this clinical process was sup- Anorectal abscesses are a common surgical emergency ported by the cryptoglandular hypothesis [2, 3]. treated by incision and drainage [1]. In several series, it There are limited data on the incidence of anal fistula has been reported that approximately 15–60% of patients following anorectal abscess in large populations. In West- with an anorectal abscess developed a chronic anal fistula ern countries, the true incidence of this condition has not during follow-up, which represents a huge variation. There- been calculated and the data provide only an approximation fore, anorectal abscess had been considered an origin or the derived from statistical inference based on other European countries [4]. Recently, a well designed study was carried out in the * D. Parés UK using the Hospital Episode Statistics from all National dapares@gmail.com Health Service hospitals in the country. The study demon- 1 Section of Colorectal Surgery, Department of General strated an incidence rate of 15.5% for anal fistula following Surgery, Hospital Germans Trias I Pujol School of Medicine, an episode of abscess and also indicated the influence of Universitat Autònoma de Barcelona, C/ Canyet S/N 08916, certain factors such as inflammatory bowel disease [5]. Badalona, Barcelona, Spain Knowledge of the risk factors for developing anal fis- 2 Àrea de Sistemes d’informació, Servei Català de la tula could allow clinicians and health systems to identify Salut (CatSalut), Digitalization for the Sustainability those individuals at risk of fistula formation in the future. of the Healthcare System (DS3), IDIBELL, Barcelona, Spain 13 Vol.:(0123456789) 898 Techniques in Coloproctology (2023) 27:897–907 This information could then be of paramount importance to thus provides carefully monitored population-based health design strategies for diagnosis and appropriate management data on morbidity and mortality for more than 7.5 million of these patients. The information would also be important people in southern Europe and has already been used for to update clinical guidelines [6, 7]. several research studies [8–10]. Patients with anal fistulas are currently referred to pri- mary care after treatment of the abscess to continue wound healing and follow-up. Therefore, these patients are obliged Inclusion and exclusion criteria to seek repeated medical attention before the final diagnosis of anal fistula is made by a proctology specialist. Some risk All adult patients (aged 18 years and older) with a first factors for anal fistula after an episode of anorectal abscess clinical episode of anorectal abscess (ICD-9-CM code 566) have been described; however, some of them such us diabe- during the study period (from 1st Jannuary 2014 to 31st tes mellitus and socioeconomic status are controversial [6]. december 2019) were included in the analysis. Table 1 lists The aim of this study was to analyse the incidence of the codes used for the study. Patients with a diagnosis of an anorectal abscesses in a large cohort of patients in an area anorectal abscess prior to the inclusion period or who were of Spain and to identify which patients later developed anal also diagnosed with an anal fistula at the time of the abscess fistula, using a population registry. We also aimed to identify were excluded from the study (ICD-9-CM code 565.1). the main risk factors associated with the clinical develop- ment of anal fistula after a first episode of anal abscess. Study variables Materials and methods We gathered the demographic characteristics of the patients, including age and gender. The patients’ comorbidity burden Study design at the time of anorectal abscess occurrence, mainly diabe- tes mellitus and inflammatory bowel disease (IBD; Crohn’s We performed an observational longitudinal study. Sociode- disease and ulcerative colitis), was assessed using the health- mographic and clinical data were collected from the local risk assessment tool for adjusted morbidity groups (AMG), health department (CatSalut) dataset of Catalonia (north- which takes into account the type of disease (i.e. acute or east Spain), including all clinical episodes from Catalan chronic), the number of patients with anal fistula and the hospitals from an area of 7,553,650 inhabitants. complexity of each condition [11–13]. The primary endpoint was the development of an ano- Patients were classified into four AMG strata based on rectal fistula after an established diagnosis of an anorectal their morbidity-related risk. Baseline risk (healthy stratum) abscess. Therefore, each episode of anorectal abscess was was assigned to the AMG score range, which comprised registered and follow-up data were collected from each 50% of the total population. Cut-off points of 50%, 80% patient whenever an anal fistula was detected, or at the end and 95% were used to define the population at low, moder- of the study period (31 December 2019), or at the time of ate and high, respectively. In addition to morbidity-related death (if applicable) January 2022. risk, we also noted the occurrence of specific diseases that we considered relevant to describe the health status of our Data source population. Socioeconomic status was stratified into four categories The Catalan Health Service (CatSalut) provides universal of pharmaceutical co-payment: very low (recipients of social public health coverage to all residents of Catalonia. Since security beneficiaries), low (annual income below €18,000), 2011, the Catalan Health Surveillance System has stored diagnostic information collected according to an MDS based on the International Classification of Diseases (ICD-9-CM), Table 1  ICD-10 coding used to register and search diagnosis which was valid until 2017, when it was replaced by the ICD-10-CM. The registry also includes information on drug Anorectal abscess Anal fistula prescriptions, outpatient visits, outpatient rehabilitation and ICD-10 Clinical diagnosis ICD-10 Clinical diagnosis many other patient services. It includes an automated data K 61.0 Perianal abscess K 60.3 Anal fistula validation system that checks the consistency of the data and K 61.1 Perirectal abscess K 60.3 Rectal fistula identifies potential errors. Moreover, because this informa- K 61.2 Anorectal abscess K 60.3 Anorectal fistula tion is used for provider payment purposes, external audits K 61.3 Ischiorectal abscess are regularly conducted to ensure the quality and reliability K 61.4 Intersphincteric abscess of the data. The Catalan Health Service Surveillance system 13 Techniques in Coloproctology (2023) 27:897–907 899 moderate (annual income €18,000 to €100,000) and high Table 2  Clinical and epidemiological distribution of studied popula- (annual income above €100,000) [11]. tion. HTA: High Blood Pressure; COPD: Crhonic obstructive pulmo- nary disease; HIV: Human immunodeficiency virus Statistical analysis Characteristics Population Perianal Perianal fistula (2014– abscess inci- incident cases 2019) dent cases Continuous variables are reported as mean (standard devi- ation) and/or median (interquartile range [IQR], defined Age group (years) as 25th and 75th percentiles) and categorical variables as < 20 851,406 723 45 number and percentage. Comparisons between categorical 20–29 4,589,242 4336 563 variables were made using the chi-square test. Survival 30–39 6,808,792 5655 1130 analysis was performed using the Kaplan–Meier method. 40–49 7,533,348 5981 1346 Subsequently, using the variables with a significant dif- 50–59 6,142,222 4818 1101 ference between categories (Gehan test), a multivariate 60–69 4,798,025 3175 749 model was constructed by calculating Cox proportional 70–79 3,420,728 1908 395 hazards with robust standard errors. The threshold for 80–89 2,220,362 1014 166 statistical significance was set at a two-sided α-value of > 90 561,080 211 17 0.05 and all analyses were performed in R version 4.0.3 Total 36,925,205 27,821 5512 [12, 13]. Gender Male 17,952,845 19,437 4020 Female 18,972,360 8384 1492 Ethical considerations Total 36,925,205 27,821 5512 Income level Because data were collected anonymously from administra- Very low 1,921,189 1448 259 tive information in a non-personal way, informed consent Low 28,974,437 19,042 3641 was not required. The management of data had been done Moderate 14,495,394 7239 1595 following the European rules of data protection. This study High 440,191 92 17 was reviewed and evaluated by the ethics and research com- Total 36,925,205 27,821 5512 mittee of our hospital and was supervised according to the Main pathologies identified Declaration of Helsinki agreements (1975) [14]. HTA 7,606,592 7233 1587 Depressive disor- 4,135,623 4006 728 ders Diabetes mellitus 2,880,166 3422 623 Results Asthma 2,437,064 1920 408 COPD 1,698,559 2226 557 Sample characteristics and incidence of anal abscess Stroke 1,144,681 1057 187 Cirrhosis 184,626 278 61 During the study period, 27,821 adult patients were treated HIV 147,701 723 154 for anorectal abscesses in the population area: 19,437 men Ulcerative colitis 110,776 389 138 (69.8%) (median age 45 years 18-102) and 8384 women Crohn's disease 73,850 362 138 (30.2%) (median age 44 years 18-100), who were included in the analysis (Table 2). The overall incidence was 596.5 abscesses per 1,000,000 inhabitants in the year with the 85–89 years, respectively. In contrast, in women, there were highest percentage. During follow-up, 4020 men and 1492 four periods of high incidence in the age groups of 20–24, women had an anal fistula identified (Fig. 1). 40–44, 70–74 and 90–94 years, with values of 677, 513, 337 The most common comorbidity present in the patient’s and 337 abscesses per 1,000,000 inhabitants, respectively. cohort was hypertension, followed by a history of cancer and The incidence of anorectal abscess also varied by socio- diabetes mellitus (up to 30%). The incidence of anorectal economic level in Catalonia. The lower the income level abscess varied by age and sex, with older adults and women was, the higher the incidence rate was. The incidence rate being less frequently affected. ranged from 209 abscesses per 1,000,000 inhabitants within The incidence of anorectal abscess declined with age in the high income level to 753 abscesses per 1,000,000 inhab- both sexes. However, in men there were three periods of high itants in the very low income level (Fig. 2). incidence with values of 1301, 1183 and 699 abscesses per 1,000,000 inhabitants in the age groups of 25–29, 50–54 and 13 900 Techniques in Coloproctology (2023) 27:897–907 Fig. 1  Incidence rate of anorectal abscess according to age group and sex Fig. 2  Incidence of anorectal abscess and anal fistula according to income level 13 Techniques in Coloproctology (2023) 27:897–907 901 Incidence of anal fistulas after anorectal abscesses The cumulative incidence rate of fistula varied by age and was very low in people younger than 30 years compared During follow-up, 4020 men (median age 49 years 18-97) with other age groups, reaching 9.6% in the first year and and 1492 women (median age 44 years 18-94) were diag- 14.8% in the fifth (p < 0.0001). nosed with anal fistula, representing 19.81% of patients in In this study, the clinical conditions possibly associated our population who developed anal fistula after an initial with the development of anal fistula were diabetes mellitus episode of anorectal abscess. and inflammatory bowel disease (IBD). The cumulative inci- Figure 1 shows the distribution of the percentages of dence was lower, but not significantly so, in patients with clinical detection of anal fistula by age group in men and diabetes mellitus than in those without (p = 0.24) (Fig. 4), women. The rate was significantly higher in men than in while the cumulative incidence rate was significantly higher women. in patients with IBD than in the general population (Figs. 5 Fistula formation after an abscess also varied by socio- and 6). These features differed slightly depending on the type economic level. Fistulas developed in 22% of patients with of IBD. The cumulative incidence rate varied little between a moderate income and in 17.9% of those with a very low distinct types of IBD, being 33.4% in the first year and 43.4% income (Fig. 2). in the fifth year of follow-up in patients with Crohn’s disease (p < 0.0001) and 32.6% in the first year and 43.3% in the fifth Timing of anal fistula development in patients with ulcerative colitis (p < 0.0001). The cumulative incidence rate of clinical detection of anal fistula following an episode of anorectal abscess increased Risk factors for anal fistula in both men and women during follow up. The distribution showed an increasing pattern from the first year of follow-up The results of the multivariate analysis are shown in after the abscess episode. The cumulative incidence rate was Fig. 7. Age was strongly associated with the development 21.3% and 24.8% in the fifth year, for both women and men, of fistula among patients aged 60–69 years (HR 2.05, respectively (p < 0.0001) (Fig. 3). 95% CI 1.82–2.30). Other age groups with a significantly Fig. 3  Cumulative incidence rate of anal fistula diagnosis during study period according to sex 13 902 Techniques in Coloproctology (2023) 27:897–907 Fig. 4  Cumulative incidence rate of anal fistula diagnosis during follow-up in patients with or without diabetes mellitus higher incidence of fistula development were those aged were age, gender, socioeconomic status, some comorbidities 40–49 years (HR 1.96, 95% CI 1.78–2.16) and those aged and prior diagnosis of IBD. 50–59 years (HR 1.96, 95% CI 1.77–2.18). In addition, sex A similar study to our own, based on a national data- also affected the risk of abscess formation, with women hav- base in England with a 15-year follow-up, calculated an ing a lower likelihood of developing a fistula after abscess incidence of 202 abscesses per 1,000,000 inhabitants and formation (HR 0.88, 95% CI 0.83–0.93). a progression rate from abscess to fistula of 17.2% [5]. The risk of fistula development after anal abscess was Another study of anorectal abscess recurrence in a cohort significantly lower in persons with very low incomes (HR of patients who completed 12 years of follow-up and 0.86, 95% CI 0.75–0.98) and in those with diabetes mellitus based on data from the Swedish National Patient Registry (HR 0.79, 95% CI 0.72–0.87). reported an incidence of 161 per 1,000,000 inhabitants In contrast, IBD increased the risk of developing fistula, per year [15]. These figures indicate differences between which was significant in patients with ulcerative colitis countries, which could be attributed to several factors such (HR 1.76, 95% CI 1.47–2.11) and even higher in those with as genetics, diet and some as yet unknown factors. Crohn’s disease (HR 1.98, 95% CI 1.66–2.37). There is wide variation in the incidence of fistula among countries. The first published series calculated a mean incidence of anal fistula of 86 per 1,000,000 inhabit- Discussion ants, 104 per 1,000,000 inhabitants and 232 per 1,000,000 inhabitants in Finland, Spain and Italy, respectively [16]. From 2014 to 2019, there were 27,821 new cases of ano- A systematic review and population-based database analy- rectal abscesses in Catalonia (mean incidence of 618.2 per sis to estimate the incidence and prevalence of anal fistula 1,000,000 inhabitants per year) and 5512 anal fistulas during by aetiology (Crohn’s disease, cryptoglandular, traumatic follow-up. Thus, approximately one in five patients (19.8%) or other) in European countries reported a global incidence with abscess developed a clinically detectable anal fistula. In rate estimate of 115 per 1,000,000 population per year [4]. addition, risk factors for the development of an anal fistula Interestingly, we also observed a wide range of per- centages of fistula formation after anal abscess in the 13 Techniques in Coloproctology (2023) 27:897–907 903 Fig. 5  Cumulative incidence rate of anal fistula diagnosis during follow-up in patients with diagnosis of Crohn’s disease Catalan population during the study years. This variation Previous studies have hypothesized the existence of has also been reported in other series. A possible expla- a hormonal effect on abscess/fistula formation support- nation is given by the hypothesis of climate changes, but ing the observation of a higher incidence of this clinical this could be related to mistakes in codification or misdi- condition in men [5]. We found that incidence of ano- agnosis due to the difficulty of identifying a fistula. We rectal abscesses was more likely in men (19,437 (69.8%) therefore believe that these results should be interpreted abscesses) than in women (8384 (30.2%) abscesses). In with caution. addition, anal fistula formation was more frequent in men Anorectal abscesses and fistula formation in the popula- (4020 (20.7%) fistulas) than in women (1492 (17.8%) fistu- tion in Catalonia have been clinically defined. In the present las). These data, as well as those from other studies, were study, we found higher rates of anal fistulas in men (69.9%) supported by the results of our univariate (p < 0.0001) and than in women (30.1%). In addition, this clinical condition multivariate analyses of risk of fistula formation in women was especially present in the fourth decade of life in patients (HR 0.88, 95% CI 0.83–0.93). The data are also supported with associated comorbidities (a past medical history of by the results of a previous study [5]. That study hypoth- hypertension, cancer and diabetes mellitus). esized the existence of gender-based differences, based on Patient age was identified as a strong factor in the diag- a previous study that considered anatomical differences nosis of anal fistula, but with different cut-off values. We among men and women [5, 18]. Other hypotheses have found a significant association between patient age and fis- been postulated, such as possible differences in the types tula formation among patients older than 30 years (with the of abscess affecting men vs. women [7] and the aforemen- highest incidence in patients aged 60–69 years), but a similar tioned role of hormones in the local perineal area. Along study with data from 158,713 individuals found the highest these lines, a previous study analysed samples of anal incidence in patients aged 41–60 years [5]. Another study, anatomy from men and pre- and postmenopausal women. with a series of 148 patients identified age as a risk factor for The authors reported a higher presence of all oestrogen, fistula formation (age group < 40 years, p < 0.01) on univari- progesterone and androgen receptors in smooth muscle ate and multivariate analyses [6]. These latter findings have and epithelial tissue in women than in men. Although the been supported by recent studies [17]. sample size was very small, these data suggest a possible 13 904 Techniques in Coloproctology (2023) 27:897–907 Fig. 6  Cumulative incidence rate of anal fistula diagnosis during follow-up of patients with a diagnosis of ulcerative colitis role of feminizing hormones in the development of differ- disease in IBD, there is limited epidemiological informa- ent anal problems [19]. Interestingly, other studies have tion on the progression of abscess to anal fistula in patients found that women with anal fistulas had significantly with IBD in the general population. Classically, anorectal higher circulating oestradiol levels (p = 0.03) and lower disease has been reported in 5% of patients with IBD [5, 21]. progesterone levels (p = 0.039) than female controls [19, Specifically, anal fistula was diagnosed in 47% of patients 20]. However, these studies did not find a positive asso- with Crohn’s disease and in 26.7% of those with ulcera- ciation between oestrogen/oestradiol action and fistula tive diagnosis [22]. Our results show that the percentage of development. fistula formation during the first year of follow-up after an Socioeconomic status is a controversial issue that has anal abscess is similar in patients with Crohn’s disease and been associated with several clinical disorders. An explana- in those with ulcerative colitis (33.4% and 32.6%, respec- tion of how it may influence different conditions is a matter tively). Our multivariate analysis showed that patients with of debate. Our multivariate analysis identified a significantly IBD had an almost twofold risk of fistula development lower association between very low income and fistula (HR 1.98 and 1.76 for Crohn’s disease and ulcerative coli- development. A previous study found a linear correlation tis, respectively). These findings are supported by those of between fistula incidence and income, with more frequent another study confirming that abscesses were more likely to anal fistula development in Q1 (high socioeconomic status) lead to fistula in patients with IBD, with the median time to and less frequent fistula formation in Q5 (very low socioeco- fistula diagnosis decreasing from 7 to 5 months, especially nomic status) [5]. There are several hypotheses that explain in Crohn’s disease [5]. Other studies have found no associa- this result. First, the low-income population may have less tion between a diagnosis of IBD and risk of anal fistula [17]. access to health services. However, other factors such as diet The similar percentages of anal fistula in both types of IBD and faecal microbiota have also been suggested to play a role in our study should be analysed with caution. The cause of in fistula pathogenesis [5, 6]. anal fistula in these patients may be multifactorial, including It is well known that there is a strong association between genetic, immunological and microbiological factors and is IBD and the risk of anal fistula development. Although many likely the result of a deep penetrating ulcer in the anorectum studies have reported the importance of fistulous anorectal [5, 22]. Therefore, our data could represent a codification 13 Techniques in Coloproctology (2023) 27:897–907 905 Fig. 7  Risk factors for fistula development after anorectal abscess misdiagnosis or, as previously suggested, the effect of in a multivariate analysis (OR 0.5, CI 0.3–0.9; p = 0.027) improved treatment of patients with ulcerative colitis, which [7]. A more recent study concluded that all patients with may have increased the diagnosis of cryptoglandular-type diabetes have an increased risk for anorectal abscess but not fistulas in these patients [5]. for recurrent disease [15]. Finally, a recent study of a large The influence of diabetes mellitus on anal fistula forma- population-based Swedish registry found that patients with tion after anorectal abscess has been investigated for the type I diabetes had a lower rate of anorectal abscess than last few decades but it is still a matter of debate. There is those with type II diabetes after adjustment in a multivariate information on worse outcomes of anal fistula surgery in analysis (OR 0.65, CI 0.6–0.7) [23]. In addition, the authors these patients, but little or no information on the influence of that study found that poor glycaemic control was directly of diabetes on fistula development. In our study, diabetes proportional to abscess formation, suggesting that metabolic was an important comorbidity in incident cases of abscess breakdown may be more important than autoimmune factors and fistula. However, multivariate analysis showed that in its pathogenesis [23]. Thus, prospective trials are war- diabetes mellitus as an isolated risk factor was associated ranted to investigate the relationship between diabetes and with a lower risk of fistula development (HR 0.79, 95% CI anorectal abscess–fistula formation. 0.72–0.87). In another series, patients without diabetes had This study is a general population study with a large sam- a two- to sevenfold higher risk of recurrence of anorectal ple that provides information on the real incidence of anal sepsis than patients with diabetes in a univariate analysis abscesses and the correlated incidence of anal fistulas in (p = 0.04) [6]. However, in a smaller study, diabetes mellitus some risk groups, and adds to the data provided by previous was associated with a lower likelihood of developing fistula studies with similar methodology [5]. However, there are 13 906 Techniques in Coloproctology (2023) 27:897–907 some limitations. First, the analysis was retrospective and the article's Creative Commons licence and your intended use is not diagnosis of anorectal abscess and anal fistula formation was permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a drawn from clinical registries of the public funded health copy of this licence, visit http://​creat​iveco​mmons.​org/​licen​ses/​by/4.​0/. system. The latter is relevant to the value of information related to influence of socioeconomic status. 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