Risk factors of recurrent furunculosis1. Professor of Public Health
Abdel-Hady El-Gilany MB BCh MSc MD1, Hanan Fathy MB BCh MSc MD2
Dermatology Online Journal 15 (1): 16
2. Assistant Professor of Dermatology, Venereology and Andrology
Faculty of Medicine, University of Mansoura, Mansoura, Egypt. email@example.com
This is a case control study of recurrent versus non-recurrent furunculosis. The aim was to identify the risk factors and causative micro-organisms associated with recurrence of furunculosis. Data was collected through an anonymous questionnaire. Weight and height were measured to calculate body mass index and a specimen was drawn from a lesion for culture. A nasal swab was taken to identify nasal Staphylococcus aureus carriers. Staphylococcus aureus was the causative organism in 89 percent and 100 percent of recurrent and non-recurrent furuncles, respectively. No significant difference was detected in resistance to the commonly used antibiotics. Logistic regression analysis revealed that the most important independent predictor of recurrence was a positive family history. The other independent predictors were anemia, previous antibiotic therapy, diabetes mellitus, previous hospitalization, multiplicity of lesions, personal hygiene and associated skin diseases. Nearly all these risk factors are modifiable, preventable, and/or controllable by simple measures such as sound personal hygiene and a balanced diet. Further research is needed to study if the same organism is implicated in recurrent cases and to test the feasibility as well as cost-benefit of prophylactic use of antibiotics. It is not advisable to use antibiotics to clear nasal carrier of S. aureus in our culture with the large number of possible sources of re-infection other than nasal nares.
Furuncle (boil) is an acute usually necrotic infection of a hair follicle with coagulase positive Staphylococcus aureus [1, 2, 3]. Furunculosis accounted for 14.8 percent of dermatologic morbidities in the outpatient dermatology clinic, Mansoura University Hospital, Egypt . Skin infections tend to be recurrent in many patients and often spread to other family members . The course of furunculosis is variable; some patients suffer only one attack, whereas others continue to develop recurrence over months or years without a period free from outbreaks . Recurrent furunculosis is a miserable condition. Even mild lesions are painful and unsightly and often heal leaving a scar . There is no fixed duration established for the term, recurrent furunculosis . Systemic factors that lower resistance are commonly detectable, including diabetes, obesity, and hematologic disorders. However, in a high proportion of cases in healthy young adults, no convincing predisposing factor can be incriminated [1, 8].
The management of recurrent furunculosis is difficult and disappointing; additional lesions may develop after the end of each course of antibiotics [1, 8]. This represents a difficult clinical problem and the tendency for certain individuals to develop a furuncle is not fully understood . Staphylococcus aureus has the ability to acquire antimicrobial resistance easily, making treatment difficult. Knowledge of the antimicrobial resistance of S. aureus is important in the selection of antimicrobials for treatment .
The present work was conducted to study the etiologic organisms and resistance to the commonly used antibiotics as well as the risk factors associated with recurrent furunculosis.
Patients and methods
This is a case control study conducted in the dermatology outpatient clinic, Mansoura University Hospital during the period from May 1 to July 31, 2006. Seventy-four patients with recurrent furunculosis (cases) and an equal number of patients with non-recurrent furunculosis (control) were included in the study. Both cases and controls were sequentially recruited from the attendants of outpatient clinics who did not receive antibiotics within the previous week. Recurrence was operationally defined as three or more attacks of boils within the previous twelve months. Patients classified in the category, non-recurrent, were diagnosed with furunculosis for the first time. Both groups were followed-up until completely cured on weekly visits to the clinic.
There is no research ethics committee at Mansoura University at the moment. Approval was obtained from the Office of Patient Affairs of Mansoura University Hospitals as well as the patient's verbal consent.
After obtaining consent, data were collected through an anonymous questionnaire covering the socio-demographic characteristics, personal habits (frequency of hand washing and showering with soap and water, and sharing personal items such as towels, razors, clothes, gloves), past medical history (diabetes mellitus or other systemic diseases, drug history – including systemic antibiotics, systemic corticosteroid and immunosuppressive drugs), and previous hospital admission within the previous 12 months.
To evaluate an overall effect of personal hygiene practices on recurrent boils, a composite hygiene score was created on the basis of the sum of scores of 3 individual hygiene practices [frequency of hand washing per day (1: <5 times, 2: 5-10 times, 3: >10 times), frequency of a shower per week (1: <3 times, 2: 3-6 times, 3: >6 times), and number of personal items shared with other housemates (1: >2 items, 2: 1-2 items, 3: none)]. In this manner, lower composite hygiene scores indicate poorer personal hygiene practices. For this study, a composite hygiene score <6, which corresponds to the 25th percentile for the distribution of the composite score, was categorized as poor personal hygiene practice (modified after Turabelidze et al.) .
Weight and height were measured. Because it was simple, easy, and useful, Quetelet's body mass index was used to measure the degree of obesity depending on the World Health Organization criteria. Obesity was defined as BMI of 30 Kg/M² or greater . Hemoglobin was estimated using the Sahli technique. Patients with hemoglobin less than 11 G/dl were considered to be anemic.
Socioeconomic status was calculated according to Fahmy and El-Sherbini . This is the most commonly used social scoring system in health research. It encompasses education and occupation, monthly per capita income of the family, number of rooms in the home and availability of mass media and sanitary home appliances, e.g., safe water supply and waste disposal.
Sterile cotton swab specimens were taken from the pointing center of the furuncle as well as from the nose of each patient. Both the left and right anterior nares were swabbed by rubbing the swab four times around the inside of each nostril while applying an even pressure and rotating the swab without interruption. The swabs were immediately placed in Stuart's transport medium and kept at 4°C until inoculation.
Specimens were processed within one hour after collection. A Gram-stained smear was performed with all samples to determine the likely organisms. Specimens were inoculated on blood agar. The plates were incubated at 37°C for 24-48 hours and bacterial isolates were identified using standard procedure . Staphylococcus aureus was identified on the basis of colony morphology, Gram stain, catalase test, and slide coagulase test . All S. aureus isolates from pus obtained from boils were tested for antibiotic sensitivity using the disc agar diffusion method  on Muller-Hinton agar plates (BioMerieux®). The disc contained the commonly used antibiotics: Fusidic acid, Methicillin, Flumox, Cefadroxil, Erythromycin, Augmentin, Unasyn, Azithromycin, Clindamycin, Vancomycin, Rifampicin and Ciprofloxacin.
Statistical analysis: Data were analyzed using SPSS (Statistical Package for Social Sciences) version 10. Variables were presented as numbers and percents. Chi square (χ²) or Fisher's exact test was employed for comparison between groups as appropriate. Significant predictors of recurrent furunculosis in bivariate analysis were entered into the logistic regression model to detect the independent predictors of recurrence (OR) and their 95 percent confidence intervals were calculated. P≤0.05 was considered statistically significant.
Staphylococcus aureus was isolated from 89.2 percent and 100 percent of recurrent and non-recurrent boils, respectively (P=0.006). However, there is no significant difference in resistance of the isolated S. aureus from recurrent and non-recurrent boils to the 12 commonly used and tested antibiotics (Table 1).
Table 2 shows that patients with recurrent boils are more likely to be overcrowded at sleep, have poor personal hygiene, and to be obese. Patients with recurrent boils are more likely to have a positive family history, take immunotherapy or antibiotics, and to have been hospitalized, anemic, or diabetic; they are also more likely to have associated skin diseases and multiple lesions.
Logistic regression analysis revealed that positive family history is the strongest independent predictor of recurrence. Other independent predictors are diabetes mellitus, anemia, previous antibiotic therapy, previous hospitalization, poor personal hygiene, associated skin diseases, and a multiplicity of lesions (Table 3).
Staphylococcus aureus is a common cause of skin infection . Staphylococcus aureus was isolated from 89.2 percent and 100 percent of recurrent and non-recurrent furunculosis patients, respectively, in our series. The role of other pyogenic pathogens in recurrence was not documented in previous studies. It is possible that culture negative recurrent cases may be caused other pyogenic organisms.
Nasal carriage of S. aureus plays a key role in the development of S. aureus infections and is a major reservoir of Methicillin resistant Staphylococcus aureus (MRSA). Between 10-35 percent and 20-75 percent of healthy individuals are persistent and intermittent carriers, respectively [18, 19]. We found that both nasal staphylococcal carrier state and the resistance characteristics of isolated S. aureus from boils are not risk factors in recurrent furunculosis. However, Stulberg et al.,  had implicated S. aureus nasal carriers as the source of recurrence. Treatment of recurrent infections is controversial, but since the nostrils are the usual carrier sites, eradication of the carrier state is suggested. Mashhood et al.  recommended that nasal swabs for detection of S. aureus carrier state should be done in all patients with recurrent furunculosis. If nasal swab culture is positive, then as the infection resolves, the patient should receive a preventative course of antibiotics; this may eradicate the carrier state and prevent the recurrence of infection. Rifampin therapy for five to ten days (alone or in combination with others) is highly effective [22, 23]. Mupirocin nasal ointment (twice daily for five days) is effective in temporarily eradicating S. aureus from the nose . However, recent clinical trials found little or no efficacy in preventing nasocomial S. aureus infections [24-28].
In our locality with poor personal hygiene being common, the role of nasal S. aureus carrier may differ from communities with good hygienic practices. Staphylococcus aureus re-infection may result from contact with infected family members, contaminated fomites, or from other extra-nasal sites. This raises a suggestion to treat household contacts and close contacts if recurrence persists, because it is likely that one or more contacts are asymptomatic carriers of S. aureus. In addition to the increase in the cost of treatment in poor countries, the possibility of developing drug resistance must be considered.
The propensity for certain individuals to develop recurrent furunculosis is not fully understood. However, many factors are associated with recurrence. The most important independent predictor of recurrence is a positive family history. Boils are spread among individuals by touching or bursting a boil. Furunculosis is a common disease, particularly with deficient hygiene [8, 20, 29, 30]. A large number of S. aureus organisms are frequently present on the sheets and underclothing of patients with furunculosis and may cause re-infection of patients and infection of other members of the family .
The role of iron deficiency anemia in recurrent furunculosis was demonstrated. This agrees with Demircay et al.  who found that all patients were free from recurrence during the six months follow-up period after iron supplementation. However, the exact mechanism of the role of iron susceptibility to infection is unclear . It was postulated that T cells in iron-deficient individuals are reduced . A variety of host factors, such as abnormal neutrophil chemotaxis, deficient intra-cellular killing, and immuno-deficient states are of importance in a minority of patients with recurrent furunculosis .
Previous hospitalization is associated with increased risk of recurrence. It was found that a history of hospital admission was a significant predictor for acquiring methicillin resistant S. aureus (MRSA) [35, 36]. However, Hedstrom  studied 100 cases with recurrent staphylococcal furunculosis and revealed that recurrent furunculosis mostly has its origin outside the hospital.
Lack of personal hygiene invites recurrence . It was found that recurrence was significantly associated with poor personal hygiene. A previous study reported that MRSA infection was significantly associated with poor personal hygiene [11, 38]. The main reasons for bathing or showering are to remove dirt and micro-organisms . It was reported that frequent hand and body washing with water and antimicrobial soap solution decreases staphylococcus skin colonization .
Previous use of antibiotics is associated with a high risk of recurrence. This may be due to the development of resistance to the antibiotics used. Diabetes mellitus is a risk factor for recurrence, too. In practice, furunculosis is more extensive and recurrent in patients with diabetes mellitus [1, 6].
An associated skin disease favors recurrence. This may be attributed to the persistent colonization of abnormal skin with S. aureus strains, such as is the case in patients with atopic dermatitis . Also, associated skin diseases were reported to be a risk for MRSA in patients with boils .
In addition to the treatment of acute lesions, management involves steps in the prophylaxis of episodes of recurrence . This requires careful evaluation of the underlying cause. Identification and treatment of predisposing factors should be given the highest priority. Health education about sound personal hygiene and correction of anemia should be mandatory in management of furunculosis.
Large-scale studies are needed to explore the etiologic agents of recurrent furunculosis. Also, randomized controlled clinical trials are essential to test the feasibility and cost-benefit ratios of different types of antibiotic chemoprophylaxis in the prevention of recurrence in high risk patients.
References1. Highet AS, Hay RJ, Robert S. Bacterial infections. In: Textbook of Dermatology. Edited by Champion RH, Burton JL, Ebling FJG. 5th ed. Volume 2. Oxford, Blackwell Scientific Publication. 1992 P. 953-1030.
2. Sutjita D. Skin and soft-tissue infections. Topics in Emergency Medicine. 2003;25(2):117-122
3. Chigbu CO, Ezeronye OU. Antibiotic resistant Staphylococcus aureus in Abia state of Nigeria. Afr J Biotechnol. 2003; 2(10): 374
4. Fathy H, El-Gilany A. Pattern of skin diseases in Mansoura University Hospital. J Pan-Arab League of Dermatologists 2003;14(2):25-33
5. Steele RW, Laner SA, Graves MH. Recurrent staphylococcal infection in families. Arch Dermatology 1980; 116(2):189-90. [PubMed]
6. Hay RJ, Adriaans BM. Bacterial infections. In: Rook's textbook of dermatology. Edited by Burn T, Breathnach S, Cox N, Griffith C. Blackwell Publishing Company. 2004. P. 1-85
7. Kirmani N, Tauzon CH, Murray HW. Staphylococcus aureus carriage rate of patients receiving long-term hemodialysis. Arch Intern Med. 1978;138(11):1657-9. [PubMed]
8. Maibach HI, Aly R. Bacterial infection of the skin. In: Dermatology. Edited by Moschella SL, Hurley HJ. 3rd ed. Volume 1. W.B. Saunders Company. 1992 P. 724-25
9. Demircay Z, Eksioglu-Demiralp E, Ergun T, et al. Phagocytosis and oxidative burst by neutrophils in patients with recurrent furunculosis. Br J Dermatol. 1998;138(6):1036-38. [PubMed]
10. Nagaraju U, Bhat G, Kuruvila M, Pai GS, Babu RP. Methicillin-resistant staphylococcus aureus in community-acquired pyoderma. Int J Dermatol. 2004;43(6):412-14. [PubMed]
11. Turabelidze G, Lin M, Wolkoff B, Dodson D, Gladbach S, Zhu B. Personal Hygiene and Methicillin resistant Staphylococcus aureus Infection. Emerging Infectious Diseases 2006;12(3):422-7. [PubMed]
12. Garrow JS, Weber J. Quetelet's index (weight/height2) as a measure of fatness. Int J Obesity. 1985;9:147
13. Fahmy SI, El-Sherbini AF. Determining simple parameters for social classifications for health research. Bulletin High Institute of Public Health, Alexandria University1983; 13(5): 95-108
14. Kloos WE, Bannerman TL. Staphylococcus and micrococcus. In: Manual of Clinical Microbiology. Edited by Murray PR, Baron JE, Pfaller AM. 6th ed. Washington DC: American Society for Microbiology 1995. P. 282
15. Colle JG, Miks RS, Watt B. Tests for the identification of bacteria. In Mackie and MacCartney Practical medical microbiology. Edited by Colle JG, Feser AG, Mormion BP. 14th ed. New York: Churchill Livingstone. 1996. P. 131
16. National Committee for Clinical Laboratory Standards (NCCLS). Antimicrobial susceptibility. Press release 2004.
17. Wiese-Posselt M, Heuck D, Draeger A, et al. Successful termination of a furunculosis outbreak due to LukS-LukF-positive, Methicillin-susceptible staphylococcus aureus in a German village by stringent decolonization, 2002-2005. Clin Infect Diseases 2007;44(11):e88-95. [PubMed]
18. Kluytmans JA, Mouton JW, VabdenBergh MF, et al. Reduction of surgical-site infections in cardiothoracic surgery by elimination of nasal carriage of staphylococcus aureus. Infect Control Hospital Epidemiol. 1996;17(12):780-5. [PubMed]
19. Kluytmans JA, VanBelkum A, Verbrugh H. Nasal carriage of staphylococcus aureus: epidemiology, underlying mechanisms, and associated risks. Clin Microbiol Rev. 1997;10(3):505-20. [PubMed]
20. Stulberg DL, Penrod A, Blanty RA. Common bacterial skin infections. Am Fam Physician 2002;66(1):119-24. [PubMed]
21. Mashhood AA, Shaikh ZI, Qureshi SM, Malik SM. Efficacy of rifampicin in eradication of carrier state of staphylococcus aureus in anterior nares with recurrent furunculosis. J Coll Physicians Surg Pak 2006;16(6):396-399 [PubMed]
22. McAnnally TP, Lewis MR, Brown DR. Effect of rifampin and Bacitracin on nasal carriers of staphylococcus aureus. Antimicrobial Agents Chemotherapy 1984;25(4):422-426 [PubMed]
23. Arathoon EG, Hamilton JR, Hench CE, Stevens DA. Efficacy of short courses of oral novobiocin-rifampin in eradicating carrier state of methicillin-resistant staphylococcus aureus and in vitro killing studies of clinical isolates. Antimicrobial Agents Chemotherapy 1990;34(9):1655-1659 [PubMed]
24. Doebbeling B, Breneman H, Neu R, et al. Elimination of staphylococcus aureus nasal carriage in health care workers: analysis of six clinical trials with calcium mupirocin ointment. Clin Infect Dis 1993;17:466-474 [PubMed]
25. Wertheim HF, Verveer J, Boelens HA, Belkum A, Verbrugh HA, Vos MC. Effect of Mupirocin treatment on nasal, pharyngeal and perineal carriage of staphylococcus aureus in healthy adults. Antimicrobial Agent Chemotherapy 2005;49(4):1465-1467 [PubMed]
26. Kalmeijer M, Coertjens H, Van Nieuwland-Bollen P, et al. Surgical site infections in orthopedic surgery: the effect of mupirocin nasal ointment in a double-blind randomized, placebo-controlled study. Clin Infect Dis 2002;35:353-358 [PubMed]
27. Perl TM, Cullen JJ, Wenzel RP, et al. Intranasal mupirocin to prevent postoperative staphylococcus aureus infections. N Eng J Med 2002;346:1871-1877 [PubMed]
28. Wertheim HF, Vos MC, Ott A, et al. Mupirocin prophylaxis against nosocomial staphylococcus aureus infections in non-surgical patients: a randomized study. Ann Intern Med 2004;140:419-425 [PubMed]
29. Braun-Falco O, Plewig G, Wolff HH, Winkelmann RH. Diseases caused by bacteria. In: Dermatology. 4th ed. 2000 P.182-208
30. Fact sheet: boils and impetigo. NSW Public Health Bull. 2003;14(1-2):29
31. Swartz MN, Weinberg AN. Infections due to Gram positive bacteria. In: Dermatology in General Medicine. Edited by Fizpartick TB, Eisen AZ, Wolff K, Freedberg IM, Austin KF. 4th ed. Volume 2. McGrow-Hill Book Company. 1993 P. 2318-2320.
32. Weijmer MC, Neering H, Welten C. Preliminary Report: furunculosis and hypoferraemia. Lancet. 1990;336(8713):464-6. [PubMed]
33. Fuchs J, Harris Z. The pathologic role of iron in infection and immunity. Contemp Critic Care. 2005;3(1):1-9.
34. Fitzpatrick JE. Bacterial infection. In: Dermatology secrets. Edited by Fitzpatrick JE, Aeling JL. Hanley and Belfus, Inc. 1996. P 174
35. Lucet JC, Chevret S, Durand-Zaleski I. Prevalence and risk factors for carriages of methicillin-resistant staphylococcus aureus at admission to the intensive care unit: results of a multicenter study. Arch Inter Med. 2003;163(2):181-8. [PubMed]
36. Fathy H, Eid M, Abdel-Aal A, Kotb I. Antibiotic resistance pattern of staphylococcus aureus in furunculosis. J Pan-Arab League of Dermatologists 2005;17(1):71-81
37. Hedstrom SA. Recurrent staphylococcal furunculosis, Bacteriological finding and epidemiology in 100 cases. Scand J Infect Dis. 1981;13(2):115-19. [PubMed]
38. Sarker R. Surface and contact infections. In: Textbook of preventive and social medicine. Edited by: Gupta P, Gha OP. 2nd ed. CBS Publishers and Distributions. New Delhi, Bangalore (India). 2007. P. 312-20
39. Shah KS, Hansotia MF. Personal hygiene. In: Community medicine and public health. Edited by Iliyas M. Reprint. 2005. P. 557
40. Laube S, Farrell M. Bacterial skin infection in the elderly: diagnosis and treatment. Drugs and Aging 2002;19(5):331-42. [PubMed]
41. Hoegr H. Antimicrobial susceptibility of skin-colonizing staphylococcus aureus strains in children with atopic dermatitis. Pediatr Allergy immunol. 2004;15(5):474-7. [PubMed]
42. Dahl V. Strategies for management of recurrent furunculosis. South Med J. 1987;80(3):352-6. [PubMed]
© 2009 Dermatology Online Journal