Eur J Plast Surg (1992) 15:115-119 European " ~ 1 .,jO Journalof i l - ~ l Q Q l l - l d F l b

SuFg ' © Springer-Verlag 1992

Return of thermal sensitivity in museulocutaneous flaps

A psychophysical study of flaps used for breast reconstruction after cancer

T. Waris 1, S. Kaisanlaht i 3, H. H/imfil/iinen 3, O. Kaarela 2, T. L/ihteenmfiki 1, S. Asko-Sel javaara 1 and T. J/irvilehto 4

1 Department of Plastic Surgery (National Cleft Center) Helsinki University, Central Hospital, Helsinki, Finland 2 Division of Plastic Surgery, Department of Surgery, Oulu University Central Hospital, Oulu, Finland 3 Department of Psychology, University of Helsinki, Finland 4 Department of Behavioural Sciences, University of Oulu, Finland

Summary. The recovery o f cold, w a r m and heat pain sensitivity in muscu locu taneous latissimus dorsi flaps (over silicone protheses) was studied in 17pat ien ts 8 mon ths to 5 years 8 mon ths postoperat ively. Cont ro l measurements were per formed on the contralateral side (6 patients had undergone a reduct ion plasty). Measure- ments were also made on the no rma l breasts o f 5 other heal thy patients. Cold, w a r m and heat pain thresholds were measured with a Mar s tock appara tus based on the Peltier principle under microprocessor control . The re- suits showed that bo th cold and heat pain sensitivity re turned to the reconstructed breast (even after reduc- t ion m a m m a plasty). Cold sensitivity was normal 2 to 3 years postoperat ively, and heat pain sensation 3 - 4 years postoperat ively. Sensitivity to w a r m t h remained abnormal in all but one patient. The re turn o f sensitivity was poor in reconstructed breasts which had complica- t ions dur ing healing.

Key words: Musculocu taneous flap Thermal sensitivity Nerve regenerat ion

The regenerat ion o f nerves in h u m a n skin grafts has been studied in the past by non-specific methods [3, 9, 16] and by neurohis tochemical methods [19], the latter have also been used to s tudy the regenerat ion o f nerves in skin flaps in the rat [18]. Adrenergic nerves have re- cently been shown to regenerate in free groin flaps in the rat [10], clinical studies have also demons t ra ted a return o f sensation in free skin grafts and pedicle flaps [2, 14]. N o systematic research has been carried out on the return o f sensitivity in muscu locu taneous flaps.

The latissimus dorsi muscu locu taneous flap used for reconstruct ion o f the female breast after cancer surgery offers a well s tandardized model to study this problem. A recently developed quant i ta t ive me thod for the mea- surement o f thermal sensitivity [4] has been found useful

Requests for reprints: T. Waris, Gunillankuja 2 B 16, SF-00870 Hel- sinki, Finland

in the assessment o f re turn o f sensation in free skin grafts [6, 20] and in free flaps [6, 11, 13].

The aim o f the present work was to investigate the re turn o f thermal sensitivity in muscu locu taneous latissi- mus dorsi flaps used for the reconst ruct ion o f the breast after cancer surgery. A Mars tock appara tus based on the Peltier principle and connected to a compute r [4, 8] was used for the exact measurement o f the thermal sensitivity.

Fur ther aims were to determine whether any p h a n t o m symptoms occurred after mas tec tomy, whether they dis- appeared after reconstruct ion, and to test the possible relationship between the recovery o f thermal sensation and these p h a n t o m symptoms.

Material and methods

Patients

A total of 17 patients who had undergone breast reconstruction with a latissimus dorsi musculocutaneous flap over a silicone proth- esis after mastectomy were examined for the return of thermal and thermal pain sensitivity in the flap. The age range of the pa- tients was 33-60 (mean 48.1) years.

Psychophysical measurements of thermal sensitivity were car- ried out a mean of 2 years and 10 months after reconstruction (range 11 months to 5 years and 8 months). In 6 of these patients a reduction mama plasty had been carried out on the contralateral healthy side. In addition, the thermal sensitivity and thermal pain sensitivity were compared using psychophysical measurements in both healthy breasts of 5 normal subjects.

Stimulation and testing procedure

Cold, warm and heat pain thresholds were measured with a micro- processor controlled device based on the Peltier principle [4]. The stimulation surface was 3.9 cm 2. The microprocessor controlled the continuous warming or cooling of the stimulation surface (from 0.20 ° C/s to 20 ° C/s according to the site) depending on the re- sponse of the patient. Skin temperature and stimulation tempera- ture were monitored by a thermo couple placed in the middle of the stimulation surface, measured by a microprocessor and printed on paper as soon as the patient responded.

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Fig. 1. Placement of the Marstock apparatus when carrying out thermal threshold measurements, i, in the middle of the musculo- cutaneous flap of the reconstructed breast; 2, on a healthy or reduc- tion mamma plasty breast; 3, below the reconstructed breast; 4, below a healthy or reduction mamma plasty breast

The patient was seated comfortably and the stimulation surface was linked with a symmetrical site opposite on the other breast for control measurement. The testing procedure started with a reac- tion time (RT) task in order to achieve adaptation of the stimula- tion surface to the skin temperature and to acquaint the patient with the testing procedure.

Auditory stimuli were presented through headphones and the patient was asked press a switch as fast as possible upon hearing the stimulus. RTs were measured by the microprocessor and printed on paper.

After the RT test the skin temperature was measured and the microprocessor brought the stimulation surface to a standard tem- perature of 30 ° C (maintained for 4 min). The temperature was then raised and the patient was instructed to respond as fast as possible by pressing the switch when feeling a warm sensation. Once a response occurred cooling started and the subject was again instructed to respond as fast as possible upon feeling a sensation of cold.

The temperatures recorded at the instant of response were used as warm and cold threshold estimates. Heat pain thresholds were measured in a similar manner. Five estimates were obtained for each threshold and the eventual value was calculated as an average.

Thermal threshold measurements were carried out first on the skin island of the musculocutaneous latissimus dorsi flap of the reconstructed breast, and then on the contralateral healthy side. In 6 cases in which a reduction plasty had been carried out on the contralateral healthy side, additional measurements of thermal thresholds were performed under the reconstructed breast and under the reduced healthy breast (Fig. 1).

Control subjects

In order to determine the normal variability in thermal thresholds on opposite sides of the body, additional control measurements were performed on both healthy breasts of 5 normal subjects.

Inquiry into phantom symptoms

The patients were questioned about the occurrence of any phantom symptoms, their nature, duration and frequency. They were also asked whether their phantom symptoms persisted after reconstruc- tion.

Results

Controls

The threshold values for thermal sensat ion in the right and left breasts in the cont ro l subjects differed by - 2 . 1 - + 4 . 8 0 ° C and those for the skin below bo th breast by - - 3 . 3 - + 3 . 4 0 ° C. A range of - 4 ~ + 4 ° C was chosen as normal .

The recovery of sensibili ty in the skin is land of the muscu locu taneous flap is demons t r a t ed in Fig. 2 4. It was possible to measure thermal pa in and cold sensa- t ions, which were the first to re turn , in all 17 patients.

Cold sensat ion re turned after abou t one year, al- though the threshold values were ini t ial ly higher than n o r m a l (except in 3 patients). N o r m a l cold threshold values were usual ly recorded 3-4 years after reconstruc- t ion.

A re tu rn of thermal pa in sensat ion was also not iced a bou t one year after operat ion. The thresholds were in general higher t han n o r m a l init ial ly (except in 3 pa- tients), bu t n o r m a l thresholds were recorded some 3 4 years after reconst ruct ion .

W a r m sensa t ion was the slowest to re turn , threshold v a l u e s being ob ta ined for only 8 pat ients , and with one exception these were still a b n o r m a l (higher or lower t han no rma l ) 5 years after reconst ruct ion .

Those pat ients whose breast after recons t ruc t ion showed a capsular fo rma t ion or some other physical recovery p rob lem after mas tec tomy and /o r reconstruc- t ion (pain in the operat ive scar or swelling of the a rm after rad ia t ion therapy) general ly had threshold values tha t were higher t han n o r m a l or otherwise deviant .

10 8 6 4 2

- 2 - 4

6 - 8

- 1 0

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Fig. 2. Heat pain thresholds in the musculocutaneous flaps of the breast reconstruction patients. Horizontal axis: time after recon- struction, in years. Vertical axis: difference from normal value (= mean of heat pain thresholds measured in the patients' healthy

(45.4 = )

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breasts or below the reconstructed breasts) in °C. Measured in terms of the difference between each patient's heat pain threshold in the musculocutaneous flap and the normal value (=45.4 ° C), shown by a vertical line. Normal range is --4 ° C - + 4 ° C

117

10 8 6 4

-2 - 4 - 6 - 8

-10 -12

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5 6 ( y )

Fig. 3. Warm sensation thresholds in the musculocutaneous flaps of the breast reconstruction patients. Horizontal axis: time after reconstruction, in years. Vertical axis: difference from normal value (=mean of warm sensation thresholds measured in the patients' healthy breasts or below the reconstructed breasts) in °C. Measured

(38.9 °}

in terms of the difference between each patient's warm sensation threshold in the musculocutaneous flap and the normal value (=38.9 ° C), shown by a vertical line. Normal range is --4 ° C- + 4 ° C

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1 2 3 4

Fig. 4. Cold pain thresholds in the musculocutaneous flaps of the breast reconstruction patients. Horizontal axis: time after recon- struction, in years. Vertical axis: the difference from normal value (= mean of cold pain thresholds measured in the patients' healthy

15

T (29.5 ° )

16

14 17

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breasts or below the reconstructed breasts) in °C. Measured in terms of the difference between each patient's cold pain sensation thresholds in the musculocutaneous flap and the normal value (=29.5 ° C), shown by a vertical line. Normal range --4 ° C - + 4 °

5 7 8 9 T T T T

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Fig. 5. Heat pain thresholds of 6 breast reconstruction patients who had also undergone reduction mamma plasty on their healthy breast. Horizontal axis: time after reduction mamma plasty, in years. Vertical axis: the difference from normal value (= mean of heat pain thresholds measured below the reduction mamma plasty

t (45.70)

17

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breast) in °C. Measured from the reduced breast in terms of the difference between each patient's heat pain threshold and the nor- mal value (=45.7 ° C), shown by a vertical line. Normal range --4 ° C - + 4 o C

- 2 - 4 - 6

9

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Fig. 6. Warm sensation thresholds of 6 breast reconstruction pa- tients who had also undergone reduction mamma plasty on their healthy breast. Horizontal axis: time after reduction mamma plasty, in years. Vertical axis: difference from normal value (= mean of warm sensation thresholds measured below the reduc-

I 6 (y)

tion mamma plasty breast) in °C. Measured from the reduced breast in terms of the difference between each patient's warm sensa- tion threshold and the normal value (= 35.1 ° C), shown by a verti- cal line. Normal range -4. ° C - + 4 ° C

118

10 8 6 4 2

- 6

8

1 5

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9

1 1 10

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Fig. 7. Cold pain sensation thresholds of six breast reconstruction patients who had also undergone reduction mamma plasty on their healthy breast. Horizontal axis: time after breast reconstruction, in years. Vertical axis: difference from normal value (=mean of

(27.20 )

1 17

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6 [y)

cold pain thresholds measured below the reduction plasty breast) in °C. Measured from the reduced breast in terms of the difference between each patient's cold pain threshold and the normal value (=27.2 ° C), shown by a vertical line. Normal range - 4 ° C-+4 ° C

Return of sensation after reduction mamma plasty

Both cold sensation and thermal pain sensation returned in all 6 patients who had undergone reduction mamma plasty of the breast. Warm sensation returned in 4 cases (Figs. 5-7).

Phantom symptoms in the reconstruction patients

Six patients experienced phantom symptoms after recon- struction, the onset occurred immediately after mastec- tomy. The frequency of the symptoms varied from once a day to once a month. In only one patient were the symptoms continuous. The phantom symptoms ceased after reconstruction in 2 patients (nos. 4 and 9), abated in one (no. 5) and remained the same as before in 3 (nos. 8, 11 and 14). These patients did not differ f rom the others with regard to the return of thermal sensation.

D i s c u s s i o n

The exact psychophysical measurement methods used here showed a restoration of cold, warm and thermal pain sensitivity in musculocutaneous flaps. The psycho- physical method is based on the Peltier phenomenon, which implies that a Marstock element becomes either cooler or warmer with a change in the direction of the current. Exact numerical values for the sensations are obtained by recording the patients' responses.

It has been shown in previous clinical evaluations that sensation does return to skin grafts and flaps, but the clinical methods used for measuring thermal sensitiv- ity are open to criticism since ice-cold water in a tes't tube [2, 14], for instance, does not always cause a sensa- tion of cold, and may instead - in addition to a sensation of touch - give a sensation of heat (paradoxical heat) [7]. Water at over + 4 0 ° C in a tube causes a thermal pain sensation in addition to one of touch and a thermal sensation [17].

The return of thermal sensitivity to musculocutan- eous flaps has not been studied previously. When a breast reconstruction is carried out using a musculocu- taneous latissimus dorsi flap, the cutaneous nerves in the flap are severed, and they then grow into the flap

from its edges after reconstruction, since the silicone prothesis under the flap prevents reinnervation directly from below. The nerve of the latissimus dorsi muscle is usually left intact when the breast reconstruction is performed, but it seems highly improbable that the fibres innervating the sensory muscle spindles of the latissimus dorsi muscle could transmit the thermal sensations ob- served in the skin flaps. Moreover, the penetration of a thermal gradient from the skin surface is poor [5], while the silicone prothesis under the flap guarantees that the thermal sensation is perceived by the receptors of the flap itself and not by receptors under the flap. It has been found in surveys of mechanical sensibility in microvascular flaps on the sole of the foot that me- chanical stimuli, particularly vibrations, are transmitted through the flap to the deep receptors of the sole [15].

Using Frustorfer 's method, Hermanson et al. studied the return of thermal sensitivity in free microvascular musculocutaneous flaps and found no superficial sensa- tion to thermal stimuli [6]. Recent investigations have nevertheless demonstrated beyond doubt that sensory recovery does occur in microvascular flaps if these are sutured to healthy, sensitive cutaneous edges [13].

The return of sensation after breast reconstruction with flaps has previously been studied by rather rough and ready methods, e.g. interviewing the patients [1]. Courtiss and Goldwyn [1] investigated the return of sen- sation to the breast by touching the skin and by record- ing the return of painful sensation by means of a vita- pulp device generally used to study dental pain. Owing to the rough methods used, the observations reported are only tentative. The results indicate that sensations of touch and pain returned in only 25% of women who had undergone subcutaneous mastectomy but returned much sooner and more completely after reduction mam- ma plasties. These observations tend to support the pres- ent exact measurements of the return of thermal sensa- tion after reduction mamma plasty.

The best method of preventing phantom symptoms in a stump after an amputat ion is replantation, and in our series, only 7 patients experienced phantom symp- toms after mastectomy. The symptoms ceased after re- construction of the breast in 3 cases, and abated in one patient. The material is unfortunately too small for any definite conclusions to be reached. The return of thermal sensation in the 3 patients whose phantom symptoms

119

pers is ted d id no t differ f rom tha t in the remainder , and thus, the r e tu rn o f the rmal sensa t ion does no t seem to be re la ted to the occur rence o f p h a n t o m symptoms .

The re tu rn o f t he rma l sensi t ivi ty has been d e m o n - s t ra ted by re l iable m e a s u r e m e n t m e t h o d s b o t h in free skin grafts t r a n s p l a n t e d on the muscle fascia [20], in free mic rovascu l a r f laps [11 13] and, here, in muscu lo - cu t aneous flaps. The cl inical series have been dif ferent and exact p rospec t ive m e t h o d s w o u l d be requ i red for fur ther c lar i f ica t ion. Cons ide r ing the re l iabi l i ty o f the m e t h o d s employed , it m a y never theless be s ta ted tha t the r e tu rn o f t he rma l sensa t ion to mic rovascu l a r f laps and m u s c u l o c u t a n e o u s f laps is super io r to tha t in free pa r t i a l skin grafts t r a n s p l a n t e d on to muscle fascia. A p ro tec t ive level o f t he rma l sensi t ivi ty m a y thus be ex- pec ted to re tu rn to the m u s c u l o c u t a n e o u s f lap af ter b reas t r econs t ruc t ion .

References

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2. Davis L (1934) The return of sensation to transplanted skin. Surg Gynecol Obstet 59:533

3. Folkerts JF, Sneep AJ, Meyling HA (•959) A comparative in- vestigation on the return of sensation to skin grafts, a clinical and histological study. In: Biemont A et al (eds) Recent neu- rological research. London, p 54

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5. Hensel H (1974) Thermoreceptors. Ann Rev Physiol 36:266 6. Hermanson A (•986) Sensibility and reinnervation after skin

injuries. A clinical and experimental study. MD Thesis, Stock- holm

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9. Kadanoff D, Wassilev W, Matev I (1966) fQber die regenerierte Nervenfasern und Nervenendungen in Hautnarben und Haut- transplantaten beim Menschen. Anat Anz 118 : 503 Lfihteenm/iki T (1986) The regeneration of adrenergic nerves in free microvascular groin flap in the rat. Scand J Plast Re- constr Surg 20:183

11. L/ihteenmfiki T, Waris T, Sundell B, Jfirvilehto T, Asko-Selja- vaara S (1987) Clinical and psychoplysical study of the recovery of sensation in free flaps. Transactions of the X International Congress of Plastic and Reconstructive Surgery, New Delhi, India, p 118

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14. Maris F, Jurkovic J, Kohut P, Suchanek A (1963) Reinnerva- tion of free and flap skin grafts. Acta Chir Plast 5 : 57

15. Rautio J (1990) Microsurgical free flaps reconstruction of soft- tissue defects in the foot. Is sensibility important for the soft- tissue stability of the flap? Thesis, Helsinki, Finland

16. Ridley A (1970) A biopsy study of the innervation of forearm skin grafted to the fingertip. Brain 93 : 547

17. Schlegel B (1980) Probleme der Schmerzmessung. Handwerker H (ed) Deutsche Gesellschaft fiir Innere Medizin, 86. KongreB, S 1549

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19. Waris T, Rechardt L, Ky6sola K (1983) Reinnervation of hu- man skin grafts. A histochemical study. Plast Reconstr Surg 72:439

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10.