Brain (1994), 117, 385-396
Different patterns of hyperalgesia induced by
experimental inflammation in human skin
S. Kilo,
1
M. Schmelz,
1
M. Koltzenburg
2
and H. O. Handwerker
1
department of Physiology and Biocybernetics, University
of Erlangen-Nurnberg and the
2
Department of Neurology,
University of Wiirzburg, Germany
Correspondence to: Dr Sonja Kilo, Department of
Physiology and Biocybernetics, University of Erlangen-
Nurnberg, Universitdtsstr. 17, D-91054 Erlangen, Germany
Summary
Different types of hyperalgesia were studied after experimental
induction of inflammation in small skin areas of healthy
volunteers either by topical application of capsaicin solution
(1 % in 70% ethanol) or by briefly freezing a skin area of similar
size to —28°C. Sensory tests were performed 30 min after
capsaicin application and 22 h after freeze lesions. Heat pain
thresholds were lowered after both treatments, probably due
to nociceptor sensitization. Hyperalgesia to four types of
mechanical stimulation was studied, (i) Hyperalgesia to punctate
stimuli was encountered at the skin site directly affected by the
noxious chemical or freeze stimulus (1 ° zone) and in the
surrounding skin (2 ° zone) in both models though the area of
2° hyperalgesia to punctate stimuli after freezing was smaller
than after capsaicin. (ii) Hyperalgesia to gently brushing the
skin was prominent after capsaicin in 1 ° and 2 ° zone, but almost
absent after freezing. It was concluded that both hyperalgesia
to punctate stimuli and brush-evoked pain are due to central
Key words: pain; C-fibres; A-fibres; nociception; sensitization
nervous plasticity changes rather than nociceptor sensitization.
As revealed by differential nerve blocks, brush-evoked pain is
mediated by low threshold mechanosensitive Afl-fibres, whilst
hyperalgesia to punctate stimuli can be elicited when only C-
fibres conduct. In contrast to hyperalgesia to punctate stimuli
it requires continuous background discharges in nociceptor
units. (Hi) Pressure hyperalgesia to tonic stimulation with a blunt
probe was encountered in the I ° zone of both types of
inflammation and is probably due to recruitment of sensitized
nociceptor units, (iv) Impact hyperalgesia was studied by
shooting small bullets against the skin at predetermined
velocities. It was found in the 1 ° zone after freezing and absent
in the capsaicin model. Differential nerve blocks revealed that
it is probably mediated by sensitized C-fibres. In conclusion,
different types of inflammatory changes may result in
characteristic different patterns of hyperalgesia.
Introduction
Hyperalgesia to mechanical and thermal stimuli is often found
after injury of the skin or partial lesions of peripheral nerves.
It is now known that several types of hyperalgesia can be
distinguished on the basis of topography and stimulus quality.
Insights into the nature of different types of hyperalgesia have
been derived mainly from studies of small skin traumas,
experimentally induced in healthy volunteers. Some decades
ago Lewis (1936, 1942) and Hardy et al. (1950, 1952)
characterized two zones of abnormal pain sensitivity following
focal experimental skin injuries: (i) the primary zone directly
affected by the injurious stimulus; (ii) the secondary zone
of apparently undamaged tissue surrounding the focus of
tissue injury. More recently, it became clear that different
hyperalgesias can be distinguished according to stimulus
modalities and qualities. For example, increased sensitivity to
© Oxford University Press 1994
mechanical stimulation may comprise a state in which
abnormally strong pain is evoked by punctate stimuli (LaMotte
et al., 1991), or a state in which the subject is hyperalgesic
to tonic pressure with blunt probes (Culp etai, 1989;
Koltzenburg etal, 1992). In a third form of mechanical
hyperalgesia—often referred to as allodynia —pain is elicited by
gently stroking the skin, e.g. with a soft brush or a swab of
cotton wool (Lewis, 1942; Hardy et al., 1950). These different
types of mechanical hyperalgesia are apparently based on
different neural mechanisms and may coexist after experimental
skin injury (LaMotte et al., 1991; Koltzenburg et al., 1992).
Exact description and analysis of the neural mechanisms of
experimentally induced hyperalgesias may also be of clinical
interest since similar forms of hyperalgesia have been
encountered in patients suffering from neuropathies or other