Reduction of skin innervation is associated with a severe fibromyalgia phenotype
Open accessAbstract
Objective: To assess patterns and impact of small nerve fiber dysfunction and pathology in patients with fibromyalgia syndrome (FMS). Methods: One hundred seventeen women with FMS underwent neurological examination, questionnaire assessment, neurophysiology assessment, and small fiber tests: skin punch biopsy, corneal confocal microscopy, microneurography, quantitative sensory testing including C‐tactile afferents, and pain‐related evoked potentials. Data were compared with those of women with major depressive disorder and chronic widespread pain (MD‐P) and healthy women. Results: Intraepidermal nerve fiber density (IENFD) was reduced at different biopsy sites in 63% of FMS patients (MD‐P: 10%, controls: 18%; p < 0.001 for each). We found 4 patterns of skin innervation in FMS: normal, distally reduced, proximally reduced, and both distally and proximally reduced (p < 0.01 for each compared to controls). Microneurography revealed initial activity‐dependent acceleration of conduction velocity upon low frequencies of stimulation in 1A fibers, besides 1B fiber spontaneous activity and mechanical sensitization in FMS patients. FMS patients had elevated warm detection thresholds (p < 0.01), impaired C‐tactile afferents (p < 0.05), and reduced amplitudes (p < 0.001) of pain‐related evoked potentials compared to controls. Compared to FMS patients with normal skin innervation, those with generalized IENFD reduction had higher pain intensity and impairment due to pain, higher disease burden, more stabbing pain and paresthesias, and more anxiety (p < 0.05 for each). FMS patients with generalized IENFD reduction also had lower corneal nerve fiber density (p < 0.01) and length (p < 0.05). Interpretation: The extent of small fiber pathology is related to symptom severity in FMS. This knowledge may have implications for the diagnostic classification and treatment of patients with FMS. ANN NEUROL 2019;86:504–516
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In a previous study, only 76% of women with FMS with comparable median pain intensity were taking analgesics.
“whilst in a previous study only 76% of women with FMS with a comparable median pain intensity were taking analgesics.15”
From Pain and small fiber pathology in men with fibromyalgia syndrome (2024) · cites this paper as [15]
The Clinical and Laboratory Findings section reports that 95 of 117 women with FMS (81%) were taking analgesics, not 76%. The cohort table gives a median current pain intensity of 5 on the numeric rating scale, but the claimed analgesic percentage is contrary to the reported figure; page numbers are unavailable in our copy. (LLM, conf=0.88)
Checked by a reasoning model — may be wrong.
Experimental — accuracy not yet measuredImpaired glucose tolerance occurred in almost a quarter of men with FMS, comparable to a previous study in female FMS patients, but was not related to extent of small fiber dysfunction or damage.
“Impaired glucose tolerance occurred in almost a quarter of men with FMS, comparable to a previous study in female patients with FMS,15 but was not related to the extent of small fiber dysfunction or damage.”
From Pain and small fiber pathology in men with fibromyalgia syndrome (2024) · cites this paper as [15]
The paper studied 117 women with FMS. Clinical and Laboratory Findings reports elevated two-hour OGTT glucose in 15 of them (about 13%), and the Discussion says small-fiber test results did not differ among patients with elevated glucose measures. It therefore supports the reference to a prior study in women and the lack of a small-fiber association, but its reported frequency is appreciably below the nearly one-quarter rate described as comparable in men. No page number is available in our copy. (LLM, conf=0.85)
Experimental — accuracy not yet measuredMere proximal denervation was hardly found in male FMS patients, whereas it was frequent in women with FMS.
“Furthermore, mere proximal denervation was hardly found in male patients with FMS, whilst this was frequent in women with FMS, indicating that these sex differences in skin innervation warrant further investigation.”
From Pain and small fiber pathology in men with fibromyalgia syndrome (2024) · cites this paper as [15]
The Methods describe a cohort of 117 women with FMS, and “Distinct Patterns of Skin Denervation in Patients with FMS” reports reduced proximal innervation without distal reduction in 31% of FMS patients. The paper therefore supports the finding in women, but it did not study male FMS patients and cannot support the claimed sex difference. Page numbers were not available in our copy. (LLM, conf=0.90)
Experimental — accuracy not yet measuredPrevious data on sensory profiles in FMS are divergent, possibly due to diversity in normative reference values and subjectivity of the psychophysical method.
“Previous data on sensory profiles in FMS are quite divergent,12,15,26,27,33,50 which may be due to diversity in the normative reference values and subjectivity of this standardized, but psychophysical method.”
From Pain and small fiber pathology in men with fibromyalgia syndrome (2024) · cites this paper as [15]
The Discussion (page unavailable) reports earlier findings of elevated thermal perception thresholds in small FMS subgroups, and the Results describe this study’s sensory profile. The paper thus contributes data on FMS sensory profiles, but the passages do not establish that previous profiles are divergent or attribute any divergence to differing normative reference values or the subjectivity of psychophysical testing. (LLM, conf=0.73)
Experimental — accuracy not yet measuredThe lack of correlation between quantitative small fiber reduction and dysfunction in QST, pleasant touch test, and questionnaire data was also reported.
“The lack of correlation between quantitative small fiber reduction and dysfunction in the remaining small fiber tests, namely QST and pleasant touch test, as well as questionnaire data was also reported.15,27,33”
From Pain and small fiber pathology in men with fibromyalgia syndrome (2024) · cites this paper as [15]
In “Corneal Denervation Parallels Skin Denervation” (page unavailable), QST profiles, including pleasant-touch perception, did not differ between patients with generalized skin-innervation reduction and those with normal innervation. But “Generalized Skin Denervation Is Associated with a More Severe FMS Phenotype” (page unavailable) reports differences in questionnaire measures of pain, disability, disease burden, and anxiety between those groups. The claim is therefore supported for QST and pleasant touch, but not for questionnaire data. (LLM, conf=0.90)
Experimental — accuracy not yet measured
Small fiber pathology has been well characterized in several independent cohorts of women with fibromyalgia syndrome.
“Thus, small fiber pathology has been well characterized in several independent cohorts of women with FMS,15,27”
From Pain and small fiber pathology in men with fibromyalgia syndrome (2024) · cites this paper as [15]
The pain phenotype in men with FMS is in line with that previously reported in women with FMS but contrasts with earlier studies that identified mostly stabbing and localized pain in men with FMS.
“These data are in line with the pain phenotype of women with FMS as previously reported,15 but in contrast with earlier studies, which identified a mostly stabbing and localized rather than widespread pain in men with FMS.38”
From Pain and small fiber pathology in men with fibromyalgia syndrome (2024) · cites this paper as [15]
In line with previous studies mainly in women with FMS, the authors found evidence for impaired small nerve fiber function in male FMS patients, reflected by elevated thermal detection thresholds, increased mechanical pain thresholds, and alterations in pleasant touch test.
“In line with previous studies mainly performed in women with FMS,12,15,26,33,50 we found evidence for impaired small nerve fiber function in male patients with FMS. This was reflected by elevated thermal detection thresholds, increased mechanical pain thresholds, and alterations in the pleasant touch test.”
From Pain and small fiber pathology in men with fibromyalgia syndrome (2024) · cites this paper as [15]
In the male FMS cohort, >50% had a generalized reduction in skin innervation, compared with 15% of women with FMS in the authors' previous study.
“Comparing skin innervation patterns in our male patient cohort with those of women with FMS investigated in our previous study,15 it is striking that >50% had a generalized reduction in skin innervation, while this occurred in only 15% of women.”
From Pain and small fiber pathology in men with fibromyalgia syndrome (2024) · cites this paper as [15]
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Non‐length‐dependent small fiber neuropathy: Not a matter of stockings and gloves
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The autoimmune aetiology of unexplained chronic pain
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Peripheral and central nervous system correlates in fibromyalgia
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Unbiased immune profiling reveals a natural killer cell-peripheral nerve axis in fibromyalgia
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Self-citationCorneal Confocal Microscopy to Image Small Nerve Fiber Degeneration: Ophthalmology Meets Neurology
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Self-citationInteraction of human keratinocytes and nerve fiber terminals at the neuro-cutaneous unit
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Self-citationSmall fibre pathology, small fibre symptoms and pain in fibromyalgia syndrome
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Central Sensitization and Small-fiber Neuropathy Are Associated in Patients With Fibromyalgia
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Small fiber pathology in fibromyalgia syndrome
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Self-citationPain-associated Mediators and Axon Pathfinders in Fibromyalgia Skin Cells
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Self-citationDistinguishing fibromyalgia syndrome from small fiber neuropathy: a clinical guide
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Self-citationCNS imaging characteristics in fibromyalgia patients with and without peripheral nerve involvement
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Self-citationAutoantibodies in patients with fibromyalgia syndrome
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Self-citationCharacterization of dermal skin innervation in fibromyalgia syndrome
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Epidermal Neurite Density in Skin Biopsies From Patients With Juvenile Fibromyalgia
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Analgesic Medication in Fibromyalgia Patients: A Cross-Sectional Study
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Small Fiber Neuropathy: A Clinical and Practical Approach
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Self-citationCentral sensitisation pain and autonomic deficiencies in fibromyalgia
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Fibromyalgia vs small fiber neuropathy: diverse keratinocyte transcriptome signature
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Self-citationSifting the wheat from the chaff? Evidence for the existence of an asymmetric fibromyalgia phenotype
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Self-citationAdvances in diagnosis and management of distal sensory polyneuropathies
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The cornucopia of central disinhibition pain – An evaluation of past and novel concepts
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MiR103a-3p and miR107 are related to adaptive coping in a cluster of fibromyalgia patients
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Self-citationLaser evoked potentials in fibromyalgia with peripheral small fiber involvement
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Subepidermal Schwann cell counts correlate with skin innervation – an exploratory study
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Self-citationSmall Fibre Pathology in Fibromyalgia: A review
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Aβ low threshold mechanoreceptors contribute to sensory abnormalities in fibromyalgia
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Tactile Detection in Fibromyalgia: A Systematic Review and a Meta-Analysis
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RetractedPain and small fiber pathology in men with fibromyalgia syndrome
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Self-citationQuantitative Sensory Testing in Fibromyalgia Syndrome: A Scoping Review
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Microneurography Reveals Unmyelinated Small Nerve Fiber Dysfunction in Long COVID
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Age-Dependent Small Fiber Neuropathy: Mechanistic Insights from Animal Models
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Increasing associations of long-COVID with small-fiber neuropathy
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The mirogabalin ALDAY phase 3 program in pain associated with fibromyalgia: the lessons learned
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Diagnosing nociplastic pain in cancer survivors: a major step forward
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Novel approaches for drug development against chronic primary pain: A systematic review
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The diagnostic assessment of fibromyalgia and the role of small fiber pathology
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- Authors
- Evdokimov, D., Frank, J., Klitsch, A., Unterecker, S., Warrings, B., Serra, J., Papagianni, A., Saffer, N., Meyer zu Altenschildesche, C., Kampik, D., Malik, R. A., Sommer, C., & Üçeyler, N.
- Affiliations
- University of Würzburg (DE)
- Neurosciences Paris-Seine (FR)
- Department of Neurology University of Würzburg Germany
- Weill Cornell Medical College in Qatar (QA)
- Corresponding author
- Üçeyler, Nurcan
- Venue
- Annals of Neurology
- Publisher
- Wiley
- Published
- 2019-08-21
- Volume
- 86
- Issue
- 4
- Pages
- 504-516
- ISSN
- 0364-5134 (ISSN-L)
- 1531-8249
- OpenAlex
- W2964507930
- Cited by
- 152
- References
- 45
- Citations by year
- 2026: 11 · 2025: 22 · 2024: 18 · 2023: 23 · 2022: 33 · 2021: 27 · 2020: 14 · 2019: 3 · 2014: 1
- FWCI
- 15.34
- Type
- journal article
- Language
- en
- Open access
- hybrid
- doi.org
- Licence
- Locations
- Annals of Neurology (publishedVersion, cc-by-nc)
- PubMed (publishedVersion)
- Online Publication Service of Würzburg University (Würzburg University) (submittedVersion, cc-by-nc)
- Funders
- Else Kröner-Fresenius-Stiftung (2014_A129)
- Deutsche Forschungsgemeinschaft (UE171/5‐1)
- Topics
- Health Sciences › Medicine › Psychiatry and Mental health › Fibromyalgia and Chronic Fatigue Syndrome Research
- Health Sciences › Medicine › Physiology › Pain Mechanisms and Treatments
- Health Sciences › Medicine › Anesthesiology and Pain Medicine › Pain Management and Treatment
- Keywords
- fibromyalgia, small fiber dysfunction, skin innervation, intraepidermal nerve fiber density, corneal nerve fiber density, C-tactile afferents, pain-related evoked potentials, microneurography, quantitative sensory testing, chronic widespread pain, major depressive disorder, mechanical sensitization, anxiety, disease severity
- MeSH terms
- Adult, Aged, Anxiety, Atrophy, Cornea, Major Depressive Disorder, Depressive Disorder, Major, Evoked Potentials, Female, Fibromyalgia, Humans, Middle Aged, Nerve Fibers, Pain Measurement, Phenotype, Sensory Thresholds, Skin, Case-Control Studies, Young Adult, Chronic Pain
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