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Revista Brasileira de Reumatologia

Print version ISSN 0482-5004On-line version ISSN 1809-4570

Rev. Bras. Reumatol. vol.57 no.1 São Paulo Jan./Feb. 2017

https://doi.org/10.1016/j.rbre.2016.03.014 

Original articles

Secondary hyperalgesia occurs regardless of unilateral or bilateral knee osteoarthritis involvement in individuals with mild or moderate level

Vanessa Martins Pereira Silva Moreiraa  * 

Saulo Delfino Barbozaa 

Juliana Borges Oliveirab 

Janser Moura Pereirac 

Valdeci Carlos Dionisioa 

aUniversidade Federal de Uberlândia (UFU), Faculdade de Medicina, Programa de Mestrado em Ciências da Saúde, Uberlândia, MG, Brazil

bUniversidade Federal de Uberlândia (UFU), Faculdade de Educação Física, Uberlândia, MG, Brazil

cUniversidade Federal de Uberlândia (UFU), Faculdade de Matemática, Uberlândia, MG, Brazil


ABSTRACT

Background:

Secondary hyperalgesia in individuals with less severe levels of knee osteoarthritis remains unclear. The objective of this study was to measure the pressure pain threshold of individuals with mild or moderate knee osteoarthritis and compare with no osteoarthritis.

Methods:

Ten healthy controls and 30 individuals with mild or moderate knee osteoarthritis divided into two groups (unilateral and bilateral involvement) were included. Dermatomes in lumbar levels (L1, L2, L3, L4 and L5) and sacral level (S1 and S2), myotomes (vastus medialis, vastus lateralis, rectus femoris, adductor longus, tibialis anterior, peroneus longus, iliacus, quadratus lumborum, and popliteus muscles), and sclerotomes in lumbar levels (L1-L2, L2-L3, L3-L4, L4-L5 supraspinous ligaments), over the L5-S1 and S1-S2 sacral areas, pes anserinus bursae, and at the patellar tendon pressure pain threshold were assessed and compared between individuals with and without knee osteoarthritis.

Results:

Knee osteoarthritis groups (unilateral and bilateral) reported lower pressure pain threshold compared to the control group in most areas (dermatomes, myotomes, and sclerotomes). There were no between group differences in the supra-spinous ligaments and over the L5-S1 and S1-S2 sacral areas of the sclerotomes. No difference was seen between knee osteoarthritis.

Conclusion:

These findings suggest that individuals with mild to moderate knee osteoarthritis had primary and secondary hyperalgesia, independent of unilateral or bilateral involvement. These results suggest that the pain have to be an assertive focus in the clinical practice, independent of the level of severity or involvement of knee osteoarthritis.

Keywords: Knee osteoarthritis; Pain; Pressure pain threshold; Secondary hyperalgesia

RESUMO

Introdução:

A ocorrência de hiperalgesia secundária em indivíduos com níveis menos graves de osteoartrite de joelho ainda é incerta. O objetivo deste estudo foi medir o limiar de dor à pressão (LDP) de indivíduos com osteoartrite de joelho (OAJ) leve ou moderada e comparar com indivíduos sem osteoartrite.

Métodos:

Foram incluídos 10 controles saudáveis e 30 indivíduos com OAJ leve ou moderada, divididos em dois grupos (envolvimento unilateral e bilateral). Foi avaliado e comparado o LDP em dermátomos (L1, L2, L3, L4, L5, S1 e S2), miótomos (músculos vasto medial, vasto lateral, reto femoral, adutor longo, tibial anterior, fibular longo, ilíaco, quadrado lombar e poplíteo) e esclerótomos (ligamentos supraespinais L1-L2, L2-L3, L3-L4, L4-L5), sobre as áreas sacrais L5-S1 e S1-S2, bolsa anserina e tendão patelar entre os indivíduos com e sem OAJ.

Resultados:

Os grupos OAJ (unilateral e bilateral) relataram menor LDP em comparação com o grupo controle na maior parte das áreas (dermátomos, miótomos e esclerótomos). Não houve diferenças entre os grupos nos ligamentos supraespinais e ao longo das áreas sacrais L5-S1 e S1-S2 dos esclerótomos. Não foi observada qualquer diferença entre os indivíduos com OAJ.

Conclusão:

Esses achados sugerem que os indivíduos com OAJ leve a moderada tinham hiperalgesia primária e secundária, independentemente do acometimento unilateral ou bilateral. Esses resultados sugerem que a dor precisa ser um foco assertivo na prática clínica, independentemente do grau de gravidade ou envolvimento da OAJ.

Palavras-chave: Osteoartrite de joelho; Dor; Limiar de dor à pressão; Hiperalgesia secundária

Introduction

The knee is the most common joint affected by osteoarthritis, and the prevalence increases with aging.1 Pain is the main symptom of knee osteoarthritis (KOA), and its presence and severity are important determinants of decreased functional capacity.2,3 Primary hyperalgesia has been defined as increased activity of primary afferent nociceptors at the site of a determined injured tissue, while secondary hyperalgesia is defined as presence of pain in areas beyond the original injured area.4 Primary and secondary hyperalgesia may occur in KOA and result in modulation of nociceptors and spinal horn neurons, respectively.5

The pressure pain threshold (PPT) has been considered the most reliable parameter to classify inflammation in osteoarthritis,6,7 and has been used to detect the presence of secondary hyperalgesia in dermatomes, myotomes, and sclerotomes.2,5 PPT seems to have different levels between individuals with and without osteoarthritis,2,8 however, current evidence does not answer if PPT levels are different between the different severities (e.g., mild or moderate) of KOA.2,9,10 In the past, Gerecz-Simon et al.11 evaluated individuals with knee OA, but just pain was mild and moderate. Also, they used only two points in lower limb. Recently, it has been demonstrated that individuals with moderate KOA present localized pain and not contralateral hyperalgesia,12 however, in this study, although not mentioned, the characteristics of the participants suggests that individuals had unilateral KOA. Therefore, assessing PPT in multiples points might bring meaningful information about the pain, as well as contribute to clinical approach. As joint damage occurs gradually in osteoarthritis (i.e., with progressive function loss of tissue stabilizers),13 secondary hyperalgesia would be expected to occur in the development process of osteoarthritis, and unilateral or bilateral involvement might play a role on this,14 resulting in different painful points. Thus, this study aimed to measure the PPT levels in mild or moderate KOA individuals with unilateral and bilateral involvement and compare to individuals without KOA. We hypothesized that some level of secondary hyperalgesia would be present in individuals with mild and moderate KOA and would be effect of unilateral or bilateral involvement.

Materials and methods

Participants

After the University Research Ethics Committee approval (No. 0012/2010) and conforms the Helsinki Declaration of 1975, the study recruitment was carried out in the Rheumatology Clinic of the university hospital and TV regional news. Four hundred-thirty individuals with KOA were contacted via telephone. Sixty individuals attended the personal evaluation to confirm their adjustment in the criteria for inclusion/exclusion.

For inclusion, individuals should be 50-years-old or more, have diagnosed KOA in the evaluation (unilateral or bilateral), and pain for at least 6 months. The diagnosis of KOA was based on the classification of the American College of Rheumatology,15 accompanied by radiological evidence of osteoarthritis affecting one or more compartments, according to the radiological criteria of Kellgren and Lawrence.16 Individuals were excluded if they had any of the following: other musculoskeletal disorders; chronic diffuse pain (fibromyalgia), chronic inflammatory conditions, such as autoimmune diseases (rheumatoid arthritis, lupus, gout); diabetes mellitus; neuromuscular disorders, such as Parkinson's disease; vertigo or other conditions that could affect the sensory capabilities and control of movement. Individuals who used central control of pain medications, such as antidepressants also were excluded, but individuals who used oral nonsteroidal anti-inflammatory drugs, it was allowed to continue its use.

After selection, 30 individuals with KOA were included. Ten individuals older than 50 years who had no history of injury, surgery, and pain in the lower extremities were selected by convenience to compose the control group. All included participants signed the informed participation consent, and were divided into three groups: bilateral KOA (n = 15), unilateral KOA (n = 15) and control (n = 10). Table 1 shows the participants’ characteristics.

Table 1 Characteristics of knee osteoarthritis (KOA) and healthy control individuals. 

Individuals Age
(mean ± SD)
Gender I/MI knee Severity KOA Medications
Control
(n = 10)
57.8 ± 6.22 Females
(n = 6)
- - -
Males
(n = 4)
- - -
KOA
Unilateral
(n = 15)
59.86 ± 7.61 Females
(n = 11)
Right knee
(n = 11)
Mild
(n = 7)
n = 8
Males
(n = 4)
Left knee
(n = 4)
Moderate
(n = 8)
Bilateral
(n = 15)
64 ± 10.06 Females
(n = 7)
Right knee
(n = 9)
Mild
(n = 4)
n = 7
Males
(n = 8)
Left knee
(n = 6)
Moderate
(n = 11)

SD, standard deviation; I, involved knee in unilateral KOA; MI, more involved knee in bilateral KOA.

Pain assessment

A digital force gauge (Force TEN™ FDX, Wagner Instruments, Greenwich, CT, USA) and with a flat ½ inch diameter head were used for mechanical quantification of hyperalgesia and allodynia resulting from peripheral or central nociceptive sensitization. The measurements were performed bilaterally in the dermatomes at levels L1, L2, L3, L4, L5, S1 and S2, using the pinch and roll maneuver described by Imamura et al.5 The same was taken for myotomes, at nine predetermined locations (vastus medialis, vastus lateralis, rectus femoris, adductor longus, tibialis anterior, peroneus longus, iliacus, quadratus lumborum, and popliteus muscles). Finally, the sclerotomes were evaluated in the L1–L2, L2–L3, L3–L4, L4–L5 supraspinous ligaments, over the L5–S1 and S1–S2 sacral areas, pes anserinus bursae, and at the patellar tendon (Fig. 1). Two experienced researchers collected all the data, using strict criteria for the location of the points. The PPT was expressed in kg/cm2, with the highest values denoting less severe symptoms.

Fig. 1 The anatomic sites used in the evaluation of the pressure pain threshold (PPT) of the muscles, patellar tendon, and pes anserinus busae in the anterior, posterior, and lateral views. (1) Vastus medialis muscle; (2) rectus femoris muscle; (3) vastus lateralis muscle; (4) adductor longus muscle; (5) anterior tibialis muscle; (6) peroneus longus muscle; (7) patellar tendon; (8) pes anserinus bursae; (9) popliteal muscle; (10) iliac muscle; (11) quadratus lumborum muscle; (12) supraspinous ligaments and sacral areas between L5-S1 and S1-S2. Figure adapted from Imamura et al.5  

Statistical analysis

In many situations it is necessary to check whether there is a significant difference in mean treatment k (k > 2). One solution would be the F test through the analysis of variance (ANOVA), which allows us to jointly test the means of k treatments. However, in some situations the model assumptions (normality and homogeneity independence of residuals) are not satisfied. Therefore we recommend the use of non-parametric tests, i.e., a non-parametric inference. In this work we applied the Kruskal–Wallis test consisting of a non-parametric ANOVA because the assumptions of parametric ANOVA were not met.17

Results

Significant difference in the mean values of the PPT was found between control and KOA unilateral and bilateral groups (p < 0.03), while no difference was found between KOA unilateral and bilateral groups. The KOA groups had a lower pain threshold in most areas of the dermatomes (Table 2), myotomes (Table 3), and sclerotomes (only the pes anserinus bursae and patellar tendon; Table 4). However, there was no difference in the mean values of the PPT (p > 0.05) in the sclerotomes of the supraspinous ligaments, over the L5-S1 and S1-S2 sacral areas (Table 4).

Table 2 Results Kruskal-Wallis test for pressure pain threshold on dermatomes. 

Dermatomal χ 2 a p-Value Groups Mean of the ranksb,c
L1 18.7044 0.0022 Control Right knee 61.55 a
Left knee 57.85 a
Unilateral Involved knee 34.97 b
Noninvolved knee 34.97 b
Bilateral More involved knee 35.00 b
Less involved knee 31.40 b
L2 13.9418 0.0159 Control Right knee 58.05 a
Left knee 55.70 a
Unilateral Involved knee 31.97 b
Noninvolved knee 34.33 b
Bilateral More involved knee 35.20 b
Less involved knee 38.67 b
L3 23.2273 0.0003 Control Right knee 61.70 a
Left knee 62.20 a
Unilateral Involved knee 33.87 b
Noninvolved knee 34.23 b
Bilateral More involved knee 35.47 b
Less involved knee 29.83 b
L4 22.0370 0.0005 Control Right knee 62.15 a
Left knee 59.8 a
Unilateral Involved knee 31.67 b
Noninvolved knee 39.20 b
Bilateral More involved knee 30.30 b
Less involved knee 33.53 b
L5 19.7702 0.0014 Control Right knee 59.60 a
Left knee 61.15 a
Unilateral Involved knee 32.10 b
Noninvolved knee 35.70 b
Bilateral More involved knee 34.83 b
Less involved knee 32.87 b
S1 22.3136 0.0005 Control Right knee 60.60 a
Left knee 61.50 a
Unilateral Involved knee 33.63 b
Noninvolved knee 35.90 b
Bilateral More involved knee 27.77 b
Less involved knee 37.30 b
S2 14.9281 0.0107 Control Right knee 58.45 a
Left knee 57.25 a
Unilateral Involved knee 33.73 b
Noninvolved knee 34.73 b
Bilateral More involved knee 34.73 b
Less involved knee 35.00 b

aχ 2 statistical value with one-tailed probability α.

bThe mean ranks derive the means of PPT collected and was represented by lowercase letters.

cDifferent lowercase letters in the column, the means of the ranks of the PPT differ by Kruskal-Wallis test at 5% significance level.

Table 3 Results Kruskal-Wallis test for pressure pain threshold on myotomes. 

Myotomal χ 2 a p-Value Groups Mean of the ranksb,c
ILIO 12.1881 0.0323 Control Right knee 55.10 a
Left knee 56.20 a
Unilateral Involved knee 38.37 b
Noninvolved knee 31.00 b
Bilateral More involved knee 35.63 b
Less involved knee 36.80 b
AL 17.8989 0.0031 Control Right knee 62.95 a
Left knee 55.10 a
Unilateral Involved knee 32.90 b
Noninvolved knee 32.47 b
Bilateral More involved knee 34.83 b
Less involved knee 37.10 b
RF 24.3074 0.0002 Control Right knee 64.00 a
Left knee 61.10 a
Unilateral Involved knee 32.83 b
Noninvolved knee 31.00 b
Bilateral More involved knee 34.53 b
Less involved knee 34.23 b
VM 21.1307 0.0008 Control Right knee 59.15 a
Left knee 62.55 a
Unilateral Involved knee 31.03 b
Noninvolved knee 34.03 b
Bilateral More involved knee 37.17 b
Less involved knee 32.63 b
VL 18.8512 0.0020 Control Right knee 62.30 a
Left knee 57.10 a
Unilateral Involved knee 35.33 b
Noninvolved knee 31.20 b
Bilateral More involved knee 33.73 b
Less involved knee 36.13 b
TA 24.7054 0.0002 Control Right knee 61.20 a
Left knee 64.20 a
Unilateral Involved knee 34.87 b
Noninvolved knee 34.37 b
Bilateral More involved knee 32.17 b
Less involved knee 31.00 b
FL 21.5347 0.0006 Control Right knee 63.10 a
Left knee 59.10 a
Unilateral Involved knee 30.30 b
Noninvolved knee 34.17 b
Bilateral More involved knee 34.87 b
Less involved knee 35.20 b
QL 24.6522 0.0002 Control Right knee 59.35 a
Left knee 65.70 a
Unilateral Involved knee 31.47 b
Noninvolved knee 33.10 b
Bilateral More involved knee 32.17 b
Less involved knee 35.90 b
POP 26.3413 <0.000 Control Right knee 62.35 a
Left knee 64.45 a
Unilateral Involved knee 31.20 b
Noninvolved knee 34.70 b
Bilateral More involved knee 30.77 b
Less involved knee 34.80 b

ILIO, iliacus muscle; AL, adductor longus muscle; RF, rectus femoris muscle; VM, vastus medialis muscle; VL, vastus lateralis muscle; TA, tibialis anterior muscle; FL, peroneus longus muscle; QL, quadratus lumborum muscle; POP, popliteus muscle.

aχ 2 statistical value with one-tailed probability α.

bThe mean ranks derive the means of PPT collected and was represented by lowercase letters.

cDifferent lowercase letters in the column, the means of the ranks of the PPT differ by Kruskal-Wallis test at 5% significance level.

Table 4 Results Kruskal-Wallis test for pressure pain threshold on sclerotomes. 

Sclerotomal χ 2 a p-Value Groups Mean of the ranksb,c
TP 24.5637 0.0002 Control Right knee 63.60 a
Left knee 61.30 a
Unilateral Involved knee 34.43 b
Noninvolved knee 33.53 b
Bilateral More involved knee 29.00 b
Less involved knee 35.77 b
PG 19.6622 0.0014 Control Right knee 59.80 a
Left knee 59.95 a
Unilateral Involved knee 33.67 b
Noninvolved knee 39.33 b
Bilateral More involved knee 31.77 b
Less involved knee 31.40 b
L1-L2 3.9834 0.1364 Control Right knee 48.00 a
Left knee 43.20 a
Unilateral Involved knee 43.27 a
Noninvolved knee 39.83 a
Bilateral More involved knee 41.63 a
Less involved knee 30.47 a
L2-L3 2.3155 0.3142 Control Right knee 37.22 a
Left knee -
Unilateral Involved knee 37.58 a
Noninvolved knee -
Bilateral More involved knee 45.60 a
Less involved knee -
L3-L4 4.4425 0.1085 Control Right knee 37.62 a
Left knee -
Unilateral Involved knee 47.48 a
Noninvolved knee -
Bilateral More involved knee 35.43 a
Less involved knee -
L4-L5 1.5373 0.4636 Control Right knee 40.30 a
Left knee -
Unilateral Involved knee 36.85 a
Noninvolved knee -
Bilateral More involved knee 44.28 a
Less involved knee -
L5-S1 3.3315 0.1890 Control Right knee 47.45 a
Left knee -
Unilateral Involved knee 41.10 a
Noninvolved knee -
Bilateral More involved knee 35.27 a
Less involved knee -
S1-S2 0.3497 0.8396 Control Right knee 39.30 a
Left knee -
Unilateral Involved knee 39.32 a
Noninvolved knee -
Bilateral More involved knee 42.48 a
Less involved knee -

PT, patella tendon; PG, pes anserinus bursae; L1-L2, L1-L2 supraspinous ligament; L2-L3, L2-L3 supraspinous ligament; L3-L4, L3-L4 supraspinous ligament; L4-L5, L4-L5 supraspinous ligament; L5-S1, L5-S1 sacral area; S1-S2, S1-S2 sacral area.

aχ2 statistical value with one-tailed probability α.

bThe mean ranks derive the means of PPT collected and was represented by lowercase letters.

cDifferent lowercase letters in the column, the means of the ranks of the PPT differ by Kruskal-Wallis test at 5% significance level.

Discussion

The aim of this study was to measure the PPT of individuals with mild and moderate KOA (with unilateral and bilateral involvement) and compare with those without KOA. The results showed that compared to controls, individuals with mild and moderate KOA had lower PPTs in most areas, while no difference occurred between unilateral or bilateral KOA involvement.

According Courtney et al.,18 primary hyperalgesia seems to be based on sensitization of peripheral C-fiber nociceptors of deep somatic tissues when a stimulus is applied at the location of the inflammation. This process progresses if the nociceptive stimulation persists. In such cases, the nerve endings of the central nervous system may be altered because of the increase in the receptive field, making them more sensitive to stimuli.5 The increase in synaptic excitability increases the response to both noxious and non-noxious stimuli, leading to allodynia and secondary hyperalgesia. In secondary hyperalgesia, a stimulus out of the lesion area causes pain in the individual.18

Although the process of degeneration in KOA is not clear, the results of this study revealed that the individuals with mild to moderate KOA had primary and secondary hyperalgesia, whereas the healthy controls did not. Comparing the data from this study with those of Imamura et al.,5 it is suggested that when KOA progresses, secondary hyperalgesia also increases. Imamura et al.5 also reported the presence of secondary hyperalgesia in distant regions of the knee, including the lumbar region, in severe KOA individuals. In contrast, in the present study, the individuals with mild to moderate KOA showed no alterations in the lumbar region. However, there were changes in the pain threshold of distant parts of the knee that exhibited secondary hyperalgesia (Tables 2 and 3). Therefore, our results suggest the secondary hyperalgesia would occur along the degeneration process and would not be a feature present only in the severe level of KOA. Similar results were showed by Rakel et al.,12 however, the PPT points were only in one point each primary and secondary hyperalgesia, and the way to determinate of the mild KOA was considered a limitation of the study by authors. The present study used the classification of the American College of Rheumatology,15 and therefore, it confirms the results of Rakel et al.,12 adding the sensitivity to mechanical stimulus in dermatomes, myotomes, and sclerotomes.

Hassan et al.3 noted that drugs could act on peripheral and/or central pain mechanisms. However, in the present study, part of the participants (n = 15; Table 1) were using, but this seems to not interfere in PPT, since most of the PPT points were more sensitive compared with control group. These results reinforce the evidence that drugs usually have limited action in chronic pain, and unsatisfactory in pain relief.19 Taylor et al.20 reported that both physicians and patients (51% of respondents) are unhappy with the inadequate control of KOA provided by traditional anti-inflammatory non-steroidal therapy. Their study included patients with mild (31%) and moderate or severe KOA (60%). In addition, these results suggest that for secondary hyperalgesia treatment and control of pain in KOA, central pain drugs could be useful, since NSAIDs act only on peripheral pain mechanisms.21

Riddle and Stratford14 found pain influence about the side of involvement (unilateral or bilateral) measured by self-report, but our results showed that pain not influenced the side of involvement and not supported the results of the Riddle and Stratford.14 Despite of important difference of size sample between these studies, we should considerate that an objective mechanism of pain mensuration (PPT) could be different of the self-report measure. Riddle and Stratford14 also suggested that difference observed in function between unilateral and bilateral pain could be a reflection of differences in pain severity. The pain measured by self-report was associated with psychological state according to Wise et al.,22 which could have influenced the results of Riddle and Stratford.14

Finally, in this study two researchers made the collection of the data and we did not assess the inter-rater reliability, what can be considered a limitation of the study, since there could be a slight difference in the locations of the anatomical points. However, they were both experienced and used strict criteria for the location of the points. As reported by Fisher,6 the individual described by the PPT is well correlated between different researchers and local analysis.

Taking all together, individuals with mild to moderate KOA had primary and secondary hyperalgesia, independent of unilateral or bilateral involvement. These results suggest that the pain have to be an assertive focus in the clinical practice, independent of the level of severity or involvement of KOA.

Acknowledgments

We appreciate the contribution of all students of the Laboratory of Physical Therapy and Neuromechanical of the Faculty of Physical Education, Universidade Federal de Uberlândia, for assistance in technical and discussions about it.

We thank the Fundação de Amparo a Pesquisa do Estado de Minas Gerais (FAPEMIG) for their support of research (Grant APQ-01110-10) and the Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq) for scholarship to this research.

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Received: October 12, 2015; Accepted: February 6, 2016

*Corresponding author. E-mail: vanessamartinsfisio@gmail.com (V.M. Pereira Silva Moreira).

Conflicts of interest

The authors declare no conflicts of interest.

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