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Research ArticlePediatric Rheumatology

Clinical Characteristics of Acne Fulminans Associated With Chronic Nonbacterial Osteomyelitis in Pediatric Patients

Ulrich Meinzer, Helene See, Brigitte Bader-Meunier, Caroline Juillard, Agnes Duquesne, Isabelle Melki, Albert Faye and Emmanuelle Bourrat for the Groupe de recherche de la Société Française de Dermatologie Pédiatrique and Société Francophone pour la Rhumatologie et les Maladies Inflammatoires en Pédiatrie (SOFREMIP)
The Journal of Rheumatology December 2020, 47 (12) 1793-1799; DOI: https://doi.org/10.3899/jrheum.191232
Ulrich Meinzer
1U. Meinzer, MD, PhD, Department of General Pediatrics, Pediatric Infectious Diseases and Pediatric Rheumatology, Hôpital Robert Debré, AP-HP, National Reference Centre for Rare Pediatric Inflammatory Rheumatisms and Systemic Auto-immune diseases (RAISE), and Université Paris Diderot-Sorbonne Paris-Cité, INSERM, UMR1149, and Biology and Genetics of Bacterial Cell Wall Unit, Institut Pasteur, Paris;
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  • For correspondence: ulrich.meinzer@aphp.fr
Helene See
2H. See, MD, I. Melki, MD, PhD, Department of General Pediatrics, Pediatric Infectious Diseases and Pediatric Rheumatology, Hôpital Robert Debré, Assistance Publique Hôpitaux de Paris AP-HP, National Reference Centre for Rare Pediatric Inflammatory Rheumatisms and Systemic Auto-immune diseases (RAISE), Paris;
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Brigitte Bader-Meunier
3B. Bader-Meunier, MD, Pediatric Hematology-Immunology and Rheumatology Department, Hôpital Necker-Enfants Malades, AP-HP, National Reference Centre for Rare Pediatric Inflammatory Rheumatisms and Systemic Auto-immune diseases (RAISE), Paris;
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Caroline Juillard
4C. Juillard, MD, Department of Dermatology, Hôpital Saint-Louis, Paris;
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Agnes Duquesne
5A. Duquesne, MD, Service de Néphrologie Rhumatologie Dermatologie Pédiatriques, National Reference Centre for Rare Pediatric Inflammatory Rheumatisms and Systemic Auto-immune diseases (RAISE), Hôpital Femme Mère Enfant, Hospices Civils de Lyon, Lyon;
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Isabelle Melki
2H. See, MD, I. Melki, MD, PhD, Department of General Pediatrics, Pediatric Infectious Diseases and Pediatric Rheumatology, Hôpital Robert Debré, Assistance Publique Hôpitaux de Paris AP-HP, National Reference Centre for Rare Pediatric Inflammatory Rheumatisms and Systemic Auto-immune diseases (RAISE), Paris;
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Albert Faye
6A. Faye, MD, PhD, Department of General Pediatrics, Pediatric Infectious Diseases and Pediatric Rheumatology, Hôpital Robert Debré, AP-HP, National Reference Centre for Rare Pediatric Inflammatory Rheumatisms and Systemic Auto-immune diseases (RAISE), and Biology and Genetics of Bacterial Cell Wall Unit, Institut Pasteur, Paris;
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Emmanuelle Bourrat
7E. Bourrat, MD, Department of General Pediatrics, Pediatric Infectious Diseases and Pediatric Rheumatology, Hôpital Robert Debré, AP-HP, National Reference Centre for Rare Pediatric Inflammatory Rheumatisms and Systemic Auto-immune diseases (RAISE), and Department of Dermatology, Hôpital Saint-Louis, Paris, France.
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Abstract

Objective Acne fulminans (AF) is a rare, explosive systemic form of acne. Chronic nonbacterial osteomyelitis (CNO) or chronic recurrent multifocal osteomyelitis (CRMO) is a primarily pediatric autoinflammatory disorder characterized by sterile osteolytic bone lesions. Concomitant occurrence of CNO/CRMO and AF is very rare, and little is known about the epidemiological and clinical particularities of this association. The aim of this retrospective observational study was to describe the characteristics of pediatric patients with CNO/CRMO associated to AF.

Methods Electronic mailing lists of French medical societies were used to call for patients with CNO/CRMO and AF. A search for published patients with CNO/CRMO and AF was performed by screening PubMed.

Results We identified 5 original patients and 10 patients from the literature. All patients were adolescent boys. Mean age at disease onset was 14.8 years. Nine of 15 patients had received isotretinoin before the sudden onset of AF. Osteoarticular symptoms appeared within < 1–3 months after the onset of AF. The mean numbers of clinical and radiological bone lesions were 3.6 and 5.6, respectively. The percentages of patients with involvement of vertebrae, pelvis, chest, and cranial were 40%, 40%, 33.3%, and 6.6%, respectively. Arthritis was observed in 69.2% of patients and sacroiliac arthritis in 46.2%.

Conclusion CNO/CRMO associated to AF occurs predominantly in male adolescents and is characterized by frequent involvement of the axial skeleton and arthritis. Epidemiological and clinical features of these patients differ from general CNO/CRMO cohorts. Clinical management requires careful handling of isotretinoin doses.

Key Indexing Terms:
  • acne fulminans
  • chronic nonbacterial osteomyelitis
  • chronic recurrent multifocal osteomyelitis
  • isotretinoin

Acne fulminans (AF) is a rare systemic disease that predominantly affects adolescent boys. Most patients previously have mild to moderate acne before the sudden onset of hemorrhagic ulcerative papules and nodules associated with a wide spectrum of systemic reactions (fatigue, malaise, arthralgias, myalgias, fever) and abnormal laboratory findings [anemia, leukocytosis, elevated C-reactive protein (CRP) and erythrocyte sedimentation rate (ESR)]1,2. It is extremely painful and results in extensive scarring. A recent review estimated that fewer than 200 cases are known2. AF should not be confused with acne conglobata or severe acne vulgaris (for comparison, see Supplementary Table 1, available with the online version of this article).

Chronic nonbacterial osteomyelitis (CNO) is an idiopathic, noninfectious inflammatory bone disorder. It covers a wide clinical spectrum with unifocal and timely limited courses at one end, and prolonged multifocal, recurrent, sometimes destructive disease courses at the other end, usually referred to as chronic recurrent multifocal osteomyelitis (CRMO)3. CNO/CRMO is primarily a pediatric disorder but can persist into adulthood or have an adult onset4. Its incidence has been estimated at 0.4/100,000/year5. Osteomyelitis is typically localized in metaphyses and epiphyses of long bones4,6. CNO/CRMO can be associated with inflammatory conditions of joints, the intestine, and the skin1,2,3.

Concomitant occurrence of CNO/CRMO and AF is extremely rare, and little is known about the clinical particularities of these patients. Therefore, we conducted a retrospective observational study to describe the epidemiological and clinical characteristics of pediatric patients with CNO/CRMO associated to AF.

MATERIALS AND METHODS

Patients were identified through calls to the French Society of Pediatric Inflammatory Diseases and the French Society of Pediatric Dermatology. Inclusion criteria were as follows: (1) at least 1 episode of AF as defined by published criteria2; (2) diagnosis of CNO/CRMO by the physician in charge of the patient, with the presence of at least 1 lesion [documented by magnetic resonance imaging (MRI) or skeletal scintigraphy, in favor of the diagnosis of osteomyelitis]; (3) absence of detectable infection; and (4) onset before 18 years of age.

We retrospectively collected the following data: age at onset of AF and CNO/CRMO, diagnostic delay, sex, personal and familial medical history, treatments, systemic signs, results from blood tests, description and localization of skin lesions, number of clinical and radiological bone lesions, presence of arthritis, treatment, and evolution. Osteolytic lesions and/or arthritis localized in vertebrae, sacrum, iliac bones, or rib cage were designated as “axial involvement.” All patients were informed about the study and gave consent. The study was approved by French regulatory authorities (CNIL n°2212602).

A search for published patients with AF and CNO/CRMO was performed by screening PubMed using the following research terms alone and their combinations: “chronic recurrent multifocal osteomyelitis”, “acne fulminans,” “fulminant acne,” “CNO,” “chronic non-bacterial osteomyelitis,” “CRMO,” and “SAPHO”. We considered only articles with data allowing confirmation of the inclusion criteria (same as above).

RESULTS

Five patients were included in the study. All of them were male. Patient 1 had a positive family history of severe, nonfulminant acne. Patient 3 had a family history of psoriasis. None had a personal medical history of pustulosis or inflammatory bowel disease. Antinuclear antibodies were negative in all patients. HLA-B27 was negative in 4 patients, and data were missing for patient 3.

The ages at onset of AF were 14.1, 16.4, 15.3, 15.1, and 14.3 years, respectively. In all patients, cutaneous lesions were localized on the thorax, back, and face. Patient 5 also had lesions on upper extremities. Some examples of cutaneous manifestations are shown in Figure 1A–C. All patients had mild or moderate acne for months or years before sudden exacerbation occurred. Two weeks before the onset of AF, patients 1 and 3 were treated with oral isotretinoin at a dose of 0.3 mg/kg/day and 0.6 mg/kg/day. Drugs administrated after exacerbation of AF are shown in Table 1. All patients had a scarring evolution of skin lesions (Figure 1C).

Figure 1.
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Figure 1.

Illustration of (A, B) active ulcerated, hemorrhagic, and crusted skin lesions, and (C) scarring evolution.

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Table 1.

Epidemiological and clinical characteristics of patients reported in this study and in the literature.

All patients showed elevated CRP levels (mean 82 mg/dL, range 20–134; Table 1). ESR was elevated in 4 patients (mean 54 mm/h, range 40–70) and was not available in 1 patient. Systemic symptoms (fever, asthenia, or emaciation) were observed in patients 1, 2, and 3.

Osteoarticular manifestations appeared within 1–3 months after onset of AF in all patients (Table 1). The delay from onset of osteoarticular manifestations to diagnosis of CNO/CRMO was < 1 month in all patients. The mean number of bone lesions with clinical manifestations was 3.6 (range 3–4) and the mean number of lesions detected on body MRI was 5.6 (range 4–9). The localizations of clinical and radiological bone lesions are shown in Table 1. Axial involvement was observed in patients 2, 3, 4, and 5. Arthritis was observed in all patients and affected the knees in patients 1 and 5; the sacroiliac joints in patients 2, 3, 4, and 5; and the ankles in patient 5. Treatments used for bone lesions are summarized in Table 1. At the last follow-up visit 12–30 months after the diagnosis, osteoarticular remission of CNO/CRMO was achieved for all patients. Patients 1, 2, 3, and 4 had complete remission of acne, whereas patient 5 had persistent nonsevere acne. All patients had cutaneous scars.

Using the same inclusion criteria, our literature research identified 7 articles reporting on 10 pediatric CNO/CRMO patients with AF7–13. Epidemiological and clinical data from these patients are summarized in Table 1. Several other reports did not provide sufficient data on skin lesions to establish the diagnosis of AF. All patients were male adolescents aged 13–17 years (Table 1). Three patients received isotretinoin before the onset of AF at doses of 0.5–1 mg/kg/day. Eight out of 10 patients had axial involvement. Arthritis occurred in 4 of 8 patients with available data. The localizations of bone lesions and arthritis, clinical data, treatments, and available biological data of these patients are shown in Table 1.

In order to further compare clinical characteristics of the study cohort and general CNO/CRMO populations, we arbitrarily chose to compare patients’ profiles to the 2 largest published CNO/CRMO cohorts (Table 2): the national French cohort (n = 178) and the international Eurofever registry cohort (n = 486)4,6. In our study cohort, the mean number of bone lesions detected by MRI was 4.2, resembling findings from the French and Eurofever cohorts (mean 3.5 and 4.1, respectively)4,6. However, the percentage of patients with involvement of vertebrae (40%), pelvis (40%), or chest (33.3%) was increased (Table 2). Further, we observed a high prevalence of arthritis (69.2%), when compared to the French and the Eurofever cohorts (11% and 32%, respectively; Table 2).

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Table 2.

CNO/CRMO patients with acne fulminans compared to general CNO/CRMO cohorts.

DISCUSSION

Our observations suggest that the epidemiological and clinical features of patients with CNO/CRMO associated with acne fulminans differ from general CNO/CRMO cohorts. The association of AF and CNO/CRMO was exclusively observed in male adolescents. In contrast, a female predominance has been reported in general CNO/CRMO cohorts4,6.

CNO/CRMO associated with AF is characterized by frequent involvement of the axial skeleton and arthritis. Our observations in pediatric patients with CNO/CRMO and AF are similar to patients with SAPHO (synovitis, acne, pustulosis, hyperostosis, and osteitis) syndrome, where development of peripheral arthritis can be observed in 23–44% of the patients, and axial arthritis in up to 91.9% of the adult patients14,15. Whether CNO/CRMO associated with AF may be considered as a subtype of SAPHO syndrome or part of an independent autoinflammatory disease remains to be determined.

Bone lesions appeared within less than 1–3 months after onset of AF in 10/11 patients. Synchronous exacerbation of severe acne and bone lesions has also been observed in the literature16. Further, Cutibacterium (formerly Propionibacterium) acnes has been proposed to play a role in the pathogenesis of CNO/CRMO and other autoinflammatory diseases17. Our observations further support the idea of a possible link between onset of acne and development of CNO/CRMO.

It is of note that 9 of 15 patients were treated with isotretinoin shortly before onset of AF and CNO/CRMO in order to treat severe, nonfulminant acne. Isotretinoin is known to increase metabolic burst from peripheral blood neutrophils and expression of genes relating to innate immune activation18,19. An ambiguous role of isotretinoin for the treatment of severe acne has been reported previously1,2,18,20. Treatment with isotretinoin needs to be initiated at low doses of 0.1 mg/kg/day, and only then are doses increased progressively1,2. When initiated directly at high doses, isotretinoin can exacerbate acne and induce AF1,2. In our study, cohort isotretinoin treatment was initiated at relatively high doses (0.3–1 mg/kg/day). Thus, one could hypothesize that the extent of inflammation induced by isotretinoin and/or AF may contribute to triggering CNO/CRMO. Further studies are required to confirm (or infirm) the role of isotretinoin and/or AF for the development of CNO/CRMO and to determine whether this clinical presentation corresponds to a particular monogenetic autoinflammatory disease21,22.

The recommended treatment for AF with systemic symptoms is a combination of corticosteroids and isotretinoin2. Oral corticosteroids should be started first, at high doses (0.5–1.0 mg/kg/day) for ≥ 4 weeks until lesions heal. Isotretinoin can then be started at the initial dose of 0.1 mg/kg/day in association with corticosteroids for 4 weeks. If no flare is observed, the same dose of isotretinoin is maintained for at least 4 more weeks, and corticosteroid doses are gradually tapered. Isotretinoin doses are then increased gradually over 3–5 months as tolerated. The typical isotretinoin cumulative dose is 120–150 mg/kg. Only 1 of 3 of patients presented in this study were treated accordingly. Management of AF associated to CNO/CMRO requires close collaboration between dermatologists and rheumatologists.

Our study has some methodological limitations. Identification of patients through mailing lists to medical societies may have caused selection bias. Further, the retrospective design of our study may have introduced information bias, especially because of the mode of data collection (questionnaire).

In conclusion, CNO/CRMO associated with AF occurs predominantly in male adolescents and is characterized by frequent involvement of the axial skeleton and arthritis. Epidemiological and clinical features of these patients differ from general CNO/CRMO cohorts. Clinical management requires careful handling of isotretinoin doses.

ONLINE SUPPLEMENT

Supplementary material accompanies the online version of this article.

Acknowledgment

The authors thank Allison Williams for proofreading of the manuscript.

  • Accepted for publication March 20, 2020.

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Clinical Characteristics of Acne Fulminans Associated With Chronic Nonbacterial Osteomyelitis in Pediatric Patients
Ulrich Meinzer, Helene See, Brigitte Bader-Meunier, Caroline Juillard, Agnes Duquesne, Isabelle Melki, Albert Faye, Emmanuelle Bourrat
The Journal of Rheumatology Dec 2020, 47 (12) 1793-1799; DOI: 10.3899/jrheum.191232

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Clinical Characteristics of Acne Fulminans Associated With Chronic Nonbacterial Osteomyelitis in Pediatric Patients
Ulrich Meinzer, Helene See, Brigitte Bader-Meunier, Caroline Juillard, Agnes Duquesne, Isabelle Melki, Albert Faye, Emmanuelle Bourrat
The Journal of Rheumatology Dec 2020, 47 (12) 1793-1799; DOI: 10.3899/jrheum.191232
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acne fulminans
CHRONIC NONBACTERIAL OSTEOMYELITIS
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