Archives of Academic Emergency Medicine. 2022; 10(1): e69 OR I G I N A L RE S E A RC H Risk Factors of Recurrent Anal Abscess in Patients with Type 2 Diabetes Mellitus; a 4-Year Retrospective study Nasser Malekpour Alamdari1, Siamak Afaghi2, Farzad Esmaeili Tarki2, Mohammad Fathi3, Sara Besharat4, Fatemehsadat Rahimi1∗ 1. Clinical Research and Development Center, Department of Surgery, Shahid Modarres Hospital, Shahid Beheshti University of Medical Sciences, Tehran, Iran. 2. Research Institute of Internal Medicine, Shahid Modarres Hospital, Shahid Beheshti University of Medical Sciences, Tehran, Iran. 3. Critical Care Quality Improvement Research Center, Shahid Modarres Hospital, Shahid Beheshti University of Medical Sciences, Tehran, Iran. 4. Department of Radiology, Shahid Labbafinezhad Hospital, Shahid Beheshti University of Medical Sciences, Tehran, Iran. Received: June 2022; Accepted: July 2022; Published online: 24 August 2022 Abstract: Introduction: Anal abscess is considered as a relatively common compilation in type 2 diabetes mellitus (T2DM) patients. This study aimed to determine the risk factors of recurrent anal abscess in T2DM patients. Methods: In this 4-year retrospective cross-sectional study, T2DM patients hospitalized due to anal abscess in Shahid Modar- res Hospital, Tehran, Iran from December 2016 to December 2020 were studied. The independent risk factors of disease recurrence were determined among demographic factors, underlying diseases, diabetes-related factors, clinical factors, laboratory parameters, abscess type, and culture using multivariate stepwise logistic regression analysis. Results: 203 patients were enrolled in the study. 58 (28.6%) patients had at least one re-occurrence of anal abscess during four years. The recurrent episodes had occurred more frequently in the first year after the initial treatment (55.2%). The prevalence of comorbidities such as metabolic syndrome, coronary artery dis- ease, chronic kidney disease, end stage renal disease, and peripheral vascular disease was significantly higher amongst patients with abscess recurrence. The patients with recurrent anal abscess had statically significant poor glycemic control (HbA1C > 7.5), decreased levels of Estimated Glomerular Filtration Rate (e-GFR), and higher C-reactive Protein (CRP) upon the first admission. Presence of metabolic syndrome, HbA1c > 7.5%, WBC > 11.0 ×109/L, and CRP > 5 mg/l were amongst the independent risk factors of recurrence. HbA1c > 7.5% was the greatest independent risk factor of anal abscess recurrence (OR=2.68, 95% CI: 1.37-5.25; p < 0.001). The area under the receiver operating characteristic (ROC) curve (AUC) of HbA1C, CRP, and WBC in predicting the risk of abscess recurrence was 0.81, 0.71, and 0.64, respectively. Conclusion: Th recurrence rate of anal abscess in this series was 28.6 %. It seems that in T2DM patients with uncontrolled diabetes who have metabolic syndrome and increased CRP and WBC in their routine tests, the probability of anal abscess reoccurrence is high. Keywords: Diabetes mellitus; abscess; metabolic syndrome; leukocytosis; diabetes complications Cite this article as: Malekpour Alamdari N, Afaghi S, Esmaeili Tarki F, Fathi M, Besharat S, Rahimi F. Risk Factors of Recurrent Anal Abscess in Patients with Type 2 Diabetes Mellitus; a 4-Year Retrospective study. Arch Acad Emerg Med. 2022; 10(1): e69. https://doi.org/10.22037/aaem.v10i1.1692. 1. Introduction Anal abscess is among the most prevalent anorectal diseases, and it is more frequent amongst the youth in their fourth ∗Corresponding Author: Fatemehsadat Rahimi; Clinical Research and De- velopment Center, Department of Surgery, Shahid Modarres Hospital, Shahid Beheshti University of Medical Sciences, Tehran, Iran. Tel: +989128303107, Email: t.rahimi@sbmu.ac.ir, ORCID: https://orcid.org/0000-0001-8463-6214. decade of life (1). Its incidence rate is 16-20 per 100,000 with a 15% risk of future fistula development (2). Surgical therapy aids in decompression and pain alleviation of the abscess, as well as in prevention of the development of Fournier’s gan- grene or pelvic sepsis (3); Whilst, treatment with antibiotics alone is regarded as ineffective, resulting in therapeutic fail- ure, illness relapse, and the creation of a fistula (4). Some pa- tients only experience a single episode of the illness, while other patients have recurring instances. It has been estab- This open-access article distributed under the terms of the Creative Commons Attribution NonCommercial 3.0 License (CC BY-NC 3.0). Downloaded from: http://journals.sbmu.ac.ir/aaem N. Malekpour Alamdari et al. 2 lished that diabetes mellitus (DM) is related to occurrence of anal abscess (5). Also, the prevalence of anal abscess is recog- nized to be significantly more in cases afflicted with type 2 di- abetes mellitus (T2DM), than those with type 1 diabetes mel- litus (T1DM), indicating the fact that insulin resistance and metabolic syndrome associated with obesity and lifestyle is more important than autoimmune factors. It’s probable that, like several other diabetes sequelae, anal abscess is related to lower glycemic control and hyperglycemia, although the link isn’t apparent (5). Recurring anal abscess can last for months or years, and it’s linked to a decline in the patient’s condition and a decrease in their quality of life (6). More- over, these repeated anal abscesses raise the health-care sys- tem’s long-term expenses. Whilst some of the risk factors for occurrence of anal abscess, including high daily salt intake, active smoking, alcohol use, obesity, and DM have been rec- ognized, there is presently a scarcity of information about which patient-related characteristics are most prognostic of anal abscess recurrence (6-8). Moreover, determining the risk factors might also aid one to further comprehend the patho- genesis of anal abscess. Hence, the initial goal of our study has been to evaluate the risk factors for recurrence of anal ab- scess among T2DM patients with treated initial anal abscess. 2. Methods 2.1. Study design and setting This retrospective single-center cross-sectional study was conducted on medical records of T2DM patients hospital- ized with the diagnosis of anal abscess in Shahid Modarres Hospital, Tehran, Iran, from December 2016 to December 2020. Shahid Modarres hospital is a tertiary and referral cen- ter of general surgery in the west of Tehran, conducting spe- cial clinical visit programs for the management and follow- up of T2DM patients under consideration of both general surgeons and internal medicine specialist teams. The study protocol was reviewed and approved by ethics committee of shahid Beheshti university of medical sciences (ethical num- ber: IR.SBMU.MSP.REC.1398.956). All the patients who par- ticipated in this study, have provided a letter of consent to cooperate in this essay. 2.2. Participants All adult T2DM patients with diagnosis of anal abscess dur- ing the study period were enrolled using census sampling method. Meeting one of the following criteria was consid- ered as verification of diabetes mellitus during the initial ad- mission: 1. A level of fasting plasma glucose (FPG) exceeding 126 mg/dL (7.0 mm/L), or 2. Hb A1C greater than 6.5%. Anal abscess was defined based on International Classification of Diseases, Eleventh Revision (ICD-11)(9). Individuals infected with human immunodeficiency virus (HIV ) or afflicted with other immune-compromising condi- tions, including those with more than 2 mg/kg steroid drug intake/day, gastrointestinal malignancies, and Crohn’s dis- ease, and those who were expired during the first hospital- ization or had incomplete medical documentation were ex- cluded. All the patients received surgical treatment of inci- sion and drainage with or without fistulotomy/ fistulectomy and antibiotic therapy as appropriate. 2.3. Data gathering Potential risk factors of anal abscess recurrence were di- vided into 7 categories: 1. Demographic factors: age, gen- der, history of smoking and alcohol consumption, 2. Un- derlying diseases: metabolic syndrome, hypertension, dys- lipidemia, end stage renal disease (ESRD), coronary artery disease (CAD), chronic kidney disease (CKD), and periph- eral vascular disease, 3. Diabetes-related factors: diabetes duration, Hemoglobin A1c (HbA1c) levels, and diabetic foot ulcer, 4. Clinical status: presence of fever, length of hospi- talization, and surgical site infection 5. Laboratorial find- ings: white blood cell count (WBC), estimated glomerular filtration rate (e-GFR), C-reactive protein (CRP), creatinine, and albumin, 6. Types of anal abscess: perianal, ischiorec- tal, inter-sphincteric, supralevator, as well as fistula forma- tion, and 7. Microbiology based on abscess culture results. All data were gathered based on patients’ electronic medical documents, extracted by two skilled medical researchers, and were double-checked before being entered into analysis. 2.4. Statistical analysis SPSS version 25.0 (SPSS, Chicago, IL, USA) or R software ver- sion 3.6.3 were employed to carry out the statistical analysis. Data were analyzed using the Shapiro-Wilk test to confirm their normal distribution. Categorial and continuous vari- ables were presented as case number (percentage) and mean ± standard deviation, respectively. To compare the categor- ical variables, Chi-Squared or Fisher’s exact test was utilized as appropriate. Independent t-test, or Mann–Whitney U test was used for comparison of means between continuous vari- ables as necessitated. The mentioned potential risk factors for anal abscess have been assessed utilizing multivariate lo- gistic regression test and indicated as Odds Ratio (OR) and 95% confidence interval. Moreover, the receiver operating characteristic (ROC) curves were drawn to find the predictive values of HbA1c, CRP, and WBC levels regarding anal abscess relapse. Two-sided p-value of less than 0.05 has been deemed statistically significant. This open-access article distributed under the terms of the Creative Commons Attribution NonCommercial 3.0 License (CC BY-NC 3.0). Downloaded from: http://journals.sbmu.ac.ir/aaem 3 Archives of Academic Emergency Medicine. 2022; 10(1): e69 Table 1: Comparing the demographic, clinical, and laboratory parameters of diabetic patients with and without recurrent anal abscess Characteristics Recurrent anal abscess P Yes (n = 58) No (n = 145) Demographic Age (year) 45.9 ± 7.8 48.1 ± 8.3 0.08 Gender (male) 43 (74.1) 105 (72.4) 0.80 Active smoking (yes) 19 (32.7) 37 (25.5) 0.29 Smoking Pack-year 11.3 ± 5 .7 9.9 ± 4.7 0.07 Alcohol consumption 7 (12.1) 19 (13.1) 0.84 Comorbidities Metabolic syndrome 22 (37.9) 25 (17.2) 0.001 Hypertension 46 (79.3) 127 (87.6) 0.13 Dyslipidemia 32 (55.2) 102 (70.3) 0.06 Coronary artery disease 34 (58.6) 53 (36.5) 0.001 Chronic kidney disease 29 (50) 48 (33.1) 0.02 End stage renal disease 10 (17.2) 9 (6.2) 0.01 Peripheral vascular disease 10 (17.2) 11 (7.6) 0.04 Diabetes-related factors Diabetes duration 13.0 ± 4.6 11.9 ± 6.1 0.21 HbA1C 6.0 ± 1.4 5.8 ± 1.5 0.38 Poor glycemic control (HbA1C>7.5) 42 (72.4) 61 (42.1) 0.001 Diabetic foot ulcer 7 (14.6) 9 (6.2) 0.16 Clinical Fever 53 (91.4) 136 (93.8) 0.54 Length of hospital stay (days) 12.3 ± 2.7 11.2 ± 6.6 0.22 Surgical site infection 3 (5.2) 9 (6.2) 0.77 Laboratory findings White blood cell (/mm3 ) 15.5 ± 7.9 13.1 ± 6.1 0.02 C-reactive protein (mg/dl) 7.9 ± 3.1 6.7 ± 3.5 0.02 E*- glomerular filtration rate (ml/min) 88.3 ± 6.3 91.9 ± 10.7 0.02 Creatinine (mg/dl) 1.2 ± 1.3 1.0 ± 1.2 0.29 Albumin (g/l) 3.7 ± 1.6 4.0 ± 1.8 0.27 Data are presented as mean ± standard deviation or frequency (%). Hb: hemoglobin; *: estimated. Table 2: Comparing the abscess characteristics of diabetic patients with and without recurrent anal abscess Characteristics Recurrent anal abscess P Yes (n = 58) No (n = 145) Anal abscess type Perianal 34 (58.6) 91 (62.7) 0.58 Ischiorectal 13 (22.4) 24 (16.5) 0.32 Inter-sphincteric 5 (8.6) 21 (14.5) 0.26 Supralevator 6 (10.3) 9 (6.2) 0.30 Formation of fistula 19 (32.7) 39 (26.9) 0.40 Culture Gram-positive and Gram-negative aerobic bacteria 7 (12.1) 13 (8.9) 0.50 Gram-positive aerobic bacteria only 9 (15.5) 25 (17.2) 0.46 Gram-negative aerobic bacteria only 6 (10.3) 11 (7.6) 0.52 Anaerobic bacteria only 2 (3.4) 4 (2.7) 0.79 Mixed aerobic and anaerobic flora 25 (43.1) 50 (34.5) 0.25 No culture result 9 (15.5) 42 (28.9) 0.07 Data are presented as frequency (%). 3. Results 3.1. Baseline characteristics of studied cases A total of 252 cases, diagnosed with anal abscess based on ICD-11 definition, were evaluated. 49 cases were excluded and finally, 203 patients with T2DM who were hospitalized with the diagnosis of anal abscess for the first time were en- rolled in the study (figure 1). The perianal type was the most This open-access article distributed under the terms of the Creative Commons Attribution NonCommercial 3.0 License (CC BY-NC 3.0). Downloaded from: http://journals.sbmu.ac.ir/aaem N. Malekpour Alamdari et al. 4 Table 3: Multivariate stepwise logistic regression analysis for independent risk factors of recurrent anal abscess in type 2 diabetes mellitus patients Factor Unit/level OR 95% CI P-value HbA1C > 7.5% 2.68 1.37-5.25 0.00 C- reactive protein > 5 mg/L 2.04 1.05-3.94 0.01 White blood cells >11.0 ×109 /L 1.35 1.15-1.58 0.01 Metabolic syndrome Presence vs Absence 1.99 1.02-3.85 0.04 Hb: hemoglobin; OR: odds ratio; CI: confidence interval. common form of abscess. 58 (28.6%) patients had at least one re-occurrence of anal abscess in the following four years af- ter initial treatment. The recurrence episodes had more fre- quently occurred during the first year after the initial treat- ment (55.2%) compared to second year (18.9%), third year (15.5%), and fourth year (10.3%) (Figure 2). Fistula forma- tion was observed in 32.7% and 26.9% of patients with and without recurrence, respectively (p = 0.4). 3.2. Risk factors of recurrence Tables 1 and 2 compare the demographic, clinical, and lab- oratory parameters as well as abscess characteristics of dia- betic patients with and without recurrent anal abscess. The mean age of patients with and without recurrence was 45.9 ± 7.8 and 48.1 ± 8.3 years, respectively (p = 0.08). Also, both groups had similar sociodemographic characteristics in terms of male gender predominancy (47.1% vs. 72.4%, p = 0.80), smoking (32.7% vs. 25.5%, p = 0.29), severity of smok- ing (11.3 ± 5 .7 vs 9.9 ± 4.7 packyear, p = 0.07), and alcohol consumption (12.1% vs 13.1%, p = 0.07). The prevalence of metabolic syndrome, coronary artery disease, chronic kid- ney disease, end stage renal disease, and peripheral vascular disease comorbidities were significantly higher amongst pa- tients with abscess re-occurrence. The patients with recurrent anal abscess had statically signif- icant poor glycemic control (HbA1C > 7.5), decreased levels of Estimated Glomerular Filtration Rate (e-GFR), and higher C-reactive Protein (CRP) upon the first admission. On micro- biological evaluation, the mixed aerobic and anerobic bacte- ria flora was the most prevalent culture result (p = 0.25). Based on the multivariate step-by-step logistic regression analysis on all potential predictors of perianal abscess recur- rence (table 3), it was found that the independent risk factors were: presence of metabolic syndrome, HbA1c > 7.5%, WBC > 11.0 ×109/L, and CRP > 5 mg/l. Amongst them, HbA1c > 7.5% as indicator of poor glycemic control was the most im- portant independent risk factor of anal abscess recurrence (OR=2.68, 95% CI: 1.37-5.25; p < 0.001). The area under the ROC curve (AUC) of HbA1C, CRP, and WBC in predicting the risk of abscess recurrence was 0.81, 0.71, and 0.64, respec- tively (figure 3). 4. Discussion This 4-year retrospective single-center study of T2DM pa- tients with an initial treated anal abscess demonstrated a high incidence for anal abscess recurrence (28.6%). As men- tioned above, we discovered that amongst a wide range of possible risk factors, the ones consistently linked to recur- ring anal abscess were: 1. metabolic syndrome, 2. HbA1c > 7.5%, 3. WBC > 11.0 ×109/L, and 4. CRP levels of more than 5 mg/l. Unfavorable glycemic control, described as hav- ing HbA1c levels of more than 7.5%, was recognized as the most prominent predisposing factor for abscess recurrence in the present study. These findings are supported by previ- ous studies that stated HbA1c levels are markedly higher in those with relapse of both diabetic ulcer and anal abscess compared to those without re-occurrence (5, 10). Inade- quate long-term blood glucose control may hinder healing of wounds, but it might also represent lower patient adherence to different preventative strategies, such as glycemic control self-monitoring and compliance with anal abscess treatment guidelines (11). Poor psychological support and patient edu- cation and may also be linked to a greater likelihood of anal abscess relapse (12). Additionally, we discovered that high CRP levels were an established risk factor for re-occurrence of anal abscess. Since the patients had no additional inflam- matory or infectious disorders during our clinical evaluation, the increased CRP upon presentation was most likely due to infections. It was previously shown that increased amount of CRP was related to ensuing complications in a long-term analysis of peri-anal abscess (13-15). Although some stud- ies have shown that higher CRP levels are linked to an ele- vated risk of sequelae and re-occurrence of the anal abscess, there have not been any formerly published evidence on the prognostic accuracy of CRP for anal abscess relapse. Even- tually, we noticed that culture findings of patients with re- curring anal abscess were identical to those of non-recurring patients. Abscess cultures frequently feature mixed anaer- obic and aerobic microorganisms, as we discovered in our investigation. The skin and the gastrointestinal tract pro- vide the majority of microorganisms in an anal abscess (16). Pepto streptococcus spp. and Bacteroides spp. were preva- lent anaerobic pathogens in individuals, whereas Klebsiella This open-access article distributed under the terms of the Creative Commons Attribution NonCommercial 3.0 License (CC BY-NC 3.0). Downloaded from: http://journals.sbmu.ac.ir/aaem 5 Archives of Academic Emergency Medicine. 2022; 10(1): e69 Figure 1: Flowchart of patients’ enrollment in the study. Figure 2: Frequency of perianal abscess recurrence in diabetes mellitus type 2 patients during 4-year follow-up. This open-access article distributed under the terms of the Creative Commons Attribution NonCommercial 3.0 License (CC BY-NC 3.0). Downloaded from: http://journals.sbmu.ac.ir/aaem N. Malekpour Alamdari et al. 6 Figure 3: Area under the receiver operating characteristic (ROC) curve (AUC) of hemoglobin A1C (AUC = 0.81), C- reactive protein (AUC = 0.71), and white blood cells (AUC = 0.64) in predicting the recurrence of perianal abscess in patients with type 2 diabetes mellitus. pneumoniae, Staphylococci spp., and Escherichia coli, were prominent aerobic pathogens. T2DM patients are thought to have decreased adaptive and native immunity, according to current findings (17, 18). Hence, antibiotic treatment may be explored in all diabetic patients, even if post-surgical an- tibiotic therapy had a limited function in uncomplicated anal abscess. Both anaerobic and aerobic bacteria could be fully covered by empiric antibiotic therapy (19). We propose that, given the considerable risk of recurring anal abscess, preventative programs focusing on cases recognized to be in the high-risk categories would be suitable. This might entail endeavors to inform individuals and the corre- spondent healthcare professionals on treatments found to be successful in avoiding anal abscess development and relapse. Reoccurrence of rectal abscess is not reported to increase the rate of mortality per se, but could remarkably increase mor- bidity and influence life quality of patients. This event could be even more important as we found that the majority of pa- tients facing with anal abscess are in their youth (45.9 years ± 7.8). Of note, we found that the main risk factors of abscess recurrence are directly or indirectly related to metabolic dis- orders, such as obesity and uncontrolled plasma glucose lev- els. These variables are considerably preventable and man- ageable despite being extremely prevalent. Hence, the au- thors suggest that clinicians closely follow up patients with higher risk of abscess recurrence to better control their dia- betes mellitus, diets, and physical activity in order to reduce the burden of anal abscess and the resulting health care ex- penses. 5. Strengths and limitations Our study had some limitations: first, the relatively small number of included patients; second, the research being per- formed in a single center; and third, the retrospective ar- rangement of the study were the main limitations. Only 48 T2DM patients with recurrence of anal abscess were identi- fied during 4 years. Moreover, the addition of a tertiary center may have resulted in an unwanted selection bias. Indeed, we have to declare that our study could possibly face the flow- ing 2 concerns regarding study bias, if any, as the authors be- lieve they did their best to prevent any bias: 1. Selection bias: The presence of missing data can result in selection bias dur- ing the course of the study; and 2. Confirmation bias: This may occur during the interpretation of study data when the authors, consciously or unconsciously, look for information or patterns in their data that confirm the ideas they already hold. Notwithstanding, to the best of our knowledge, this is the first-ever analysis focusing on the distinct risk factors of recurring anal abscess in T2DM patients, which evaluates their prognostic validity for anal abscess re-occurrence. 6. Conclusion Our findings demonstrate a high rate of anal abscess recur- rence within four years in diabetic patients with anal abscess. The presence of metabolic syndrome, elevated WBC count, an increased CRP (at the time of diagnosing the first anal ab- scess) and inadequate glycemic management, were indepen- dent risk factors for recurring abscess. 7. Declarations 7.1. Acknowledgments The authors would like to take this opportunity to thank all the staff of Shahid Modarres Hospital for their effort and co- operation in providing the medical records data to conduct this study. This open-access article distributed under the terms of the Creative Commons Attribution NonCommercial 3.0 License (CC BY-NC 3.0). Downloaded from: http://journals.sbmu.ac.ir/aaem 7 Archives of Academic Emergency Medicine. 2022; 10(1): e69 7.2. 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Does adjuvant antibiotic treatment after drainage of anorectal abscess prevent development of anal fistulas? A randomized, placebo- controlled, double-blind, multicenter study. Dis Colon Rectum. 2011;54(8):923-9. This open-access article distributed under the terms of the Creative Commons Attribution NonCommercial 3.0 License (CC BY-NC 3.0). Downloaded from: http://journals.sbmu.ac.ir/aaem Introduction Methods Results Discussion Strengths and limitations Conclusion Declarations References