bone grafts and chronic osteomyelitis€¦ · bone grafts and chronic osteomyelitis...

BONE GRAFTS AND CHRONIC OSTEOMYELITIS

JoS#{201}C. DE OLIvEIRA, OPORTO, PORTUGAL

From the Orihopaedic Department, Oporlo Medical School�

Chronic osteomyelitis still remains a problem despite advances in medicine. Modern

trends emphasise the ischaemia rather than the infection ofthe bone (Clawson and Dunn 1967).

Avascular bone or scar tissue acts as an impenetrable barrier to antibiotics. For antibiotics

to be effective dead bone, scar tissue and sinuses must be removed. All dead space must be

eliminated when the wound is closed, otherwise the cavity is easily reinfected (Hazlett 1954;

Valls, Brewener and Segers 1959; Clawson and Stevenson 1965).

The removal of sequestra and scar tissue is usually done without difficulty, although from

time to time the surgeon has to be less radical, lest the bone be unduly weakened (Horwitz and

Lambert 1946, Reynolds and Zaepfel 1948).

Elimination of the dead space is the more difficult procedure (Bickel, Bateman and

Johnson 1953; Rowling 1959; Rowe and Sakellarides 1961 ; Mercer and Duthie 1964). It has

long been known that osteomyelitic cavities have a poor tendency to spontaneous obliteration

by bone proliferation (Hogeman 1949). Ingenuity has resulted in a multiplicity of techniques.

At present only three deserve interest : the free skin graft, the muscle flap and the bone graft

(Hazlett 1954, Rowe and Sakellarides 1961, Mercer and Duthie 1964, Winter and Papp 1964,

Evans and Davies 1969). The first two present technical difficulties that make them

impracticable in many cases. Above all in the metaphysio-epiphysial regions difficulties are

frequent (Bickel and colleagues 1953, Martini and Essafi 1965, Evans and Davies 1969). In

these cases saucerisation is usually impracticable. On the other hand, in regions such as the

knee, ankle, wrist and shoulder it is difficult, or even impossible, to find muscle to fill the

cavity (Coleman, Bateman, Dale and Starr 1946; Bickel and colleagues 1953). That is the

reason why, when localised in one of those regions, chronic osteomyelitis continues to be a

“therapeutic challenge” (Clawson and Dunn 1967).

The use of bone grafts, not universally accepted, seems to present many advantages

(Bickel and colleagues 1953, Hazlett 1954). Their use in infected bone defects has been

condemned since the beginning of the century after early failures (Hogeman 1949, Buchman

and Blair 195 1 ). The accepted practice was to wait one or even two years after the end of

suppuration before grafts were used. With the advent of antibiotics only the period of waiting

was changed (Boyd and Lipinski 1960, Judet and Judet 1965). The general idea of the necessary

conditions of the “ground”, so that the graft takes, persisted in spite of the protection of

antibiotics (Hogeman 1949, Stringa 1958). Even with occasional good results the procedure

seemed inconsistent with the basic principles of biology, “living transplant being unable to

survive in an infected cavity” (Winter 1951).

Mowlem, of England, fighting against this opinion, and believing in protection by

antibiotics, was the first to use bone grafts in infected cavities. In his papers (1944 and 1945)

he emphasised the great resistance of cancellous bone chips to infection and the advantage of

their use in reconstructive surgery of the skeleton. In conclusion, Mowlem said : “Nobody

suggests that it is desirable to graft in the presence of infection. But it is our feeling that the

existence of a low-grade infection did not represent a barrier to the graft. If the graft can

be used before disuse atrophy of the limb, not only is much time saved, but also the possibilities

of complete recuperation are greater.” In subsequent years other authors have shown their

* Director: Professor C. Lima.

672 THE JOURNAL OF BONE AND JOINT SURGERY

interest in this subject (Knight and Wood 1945; Prigge 1946; Abbott, Schottstaedt, Saunders

and Bost 1947). However, it was only when there appeared publications based on more

extensive experience (Coleman and colleagues 1946, with fifty-two cases; Hogeman 1949, with

eleven cases; Bickel and colleagues 1953, with thirty-six cases; Hazlett 1954, with 101 cases:

Popkirow 1960, with sixty cases) that the method attracted attention.

U)

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U-0

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(I)I-zUi

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5-10 10-15 15-20 20-30 30-40 40-50 50-60

56

AGE (years)FIG. 1

Age distribution.

34

fi2 � � � � r7 I

HUMERUS RADIUS

ULNA

[s7TIBIA

121

SPINE

FEMUR METATARSAL

BONE GRAFTS AND CHRONIC OSTEOMYELITIS 673

VOL. 53 B, NO. 4, NOVEMBER 1971

FIG. 2

Bones affected.

The procedure has not achieved general acceptance. Buchman and Blair (1951), Boyd

and Lipinski (1960) and Judet and Judet (1965) considered that it was based on incorrect

principles. But the advantages of its use are evident. First, it is always possible to fill a

cavity, no matter where. Secondly, the disadvantages of the occasional wide excision are

greatly reduced once we can hope for good bone reconstruction. Finally, in cases of infected

32

24

1618

10

9 HII

0 1 2 3 4 5 6 7 8 9

OPERATIONS (before admission)FIG. 3

Number of operations undergone before admission.

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z

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2-3 3-4 4-5 5-10 10-15 15-20 >20

LENGTH OF DISEASE (yeirs)Fio. 4

Duration of disease.

mechanical resistance and of greater probability of reinfection. With a muscle pedicle the

vascularisation decreases with time (Buchman and Blair 1951), while with bone grafts the

vascularisation increases. It has been known for a long time that the only safe indication of

cure of chronic osteomyelitis is good bone reconstruction (Popkirow 1960). When the infected

defects show little tendency to spontaneous obliteration the use of bone grafts may be best.

<1 1-2

rn21 1 I

674 J. C. DE OLIVEIRA

THE JOURNAL OF BONE AND JOINT SURGERY

fracture with pseudarthrosis, the osteogenic activity of the graft is a fundamental factor

in consolidation (1-logeman 1949, Bickel and colleagues 1953, Hazlett 1954). As Hogeman

said, the main reason for its preference is that with other methods of treatment the cavity

or dead space may persist for a long time after the operation, creating a locus of lessened

FIG. 6



ClINICAL STUDY

In the last ten years 231 cases ofchronic osteomyelitis have been treated in the orthopaedic

department of Oporto Medical School. In 120 of these bone grafts were used: these cases are

Infected cavity with sinus. Figure 5-Before treatment. Figure 6-Threeyears after removal of fistula, scar tissue and sclerosed bone and filling of

cavity with cancellous chips.

reviewed in the present paper. The patients, seventy-three male and forty-seven female, were

aged between five and sixty years; most were in the first three decades of life (Fig. I). The

infection was haematogenous in 101 cases; it followed compound fracture in eighteen cases



and direct contamination from wound sepsis in one. The femur and tibia were the bones

most often affected (three-quarters of the cases), followed by the humerus and radius (Fig. 2).

Most patients had been operated on before admission: only sixteen were fresh cases. More

than half of the patients (sixty-eight) had had two to six previous operations (Fig. 3). The

duration of the disease was from six months to forty-three years. In only twelve patients

was it less than a year, while in eighty cases it was between two and fifteen years (Fig. 4).

In sixty-eight cases the infection was in the metaphysio-epiphysial region, while in forty

cases the main lesion was in the diaphysis. In ten cases both regions were involved. In sixty-

eight cases the lesion had the aspect of a cavity, without radiologically demonstrable sequestra:

in twenty-eight cases sequestra were visible in the radiograph: in fourteen cases there was a

pseudarthrosis: and in ten cases the appearance was that of Brodie’s abscess, seven with

FIG. 7 FIG. 8

Infected cavity in the humerus, with sinus. Figure 7-State onadmission, after two operations. Figure 8-Eighteen months afterremoval of sinus, scar tissue and sclerosed bone and filling of cavity

with cancellous chips.

sinuses. In 1 17 cases it was possible to identify the bacteria. The most frequent was staphy-

lococcus aureus, alone or associated with otherorganisms (108 cases) followed by pseudomonas

aeruginosa (fourteen cases). The bacteriological contaminants were more common in old

sinuses than in open fractures.

Treatment-On admission the patient had radiographs taken in two planes, and sometimes

tomography was done. If the disease affected a segment of the body with much muscle,

sinography was also done. Pus from the depth of the wound was cultured for identification

of the organism, and to determine the most suitable antibiotic. This was administered for

three to five days before operation, and for four to six weeks afterwards.

Contrary to general experience, we have had only a few cases in which plastic procedures

were needed before the bone operation was undertaken. This was because most of our cases

were of haematogenous osteomyelitis. In only twelve patients was a plastic procedure

necessary, six of them cross-leg flaps.

Operative iechnique� -A pneumatic tourniquet was employed whenever feasible. After injection

of the tract with I per cent methylene blue, an incision was made in such a way that the sinus

and bone lesions could be removed. Sometimes a different approach to the sinus was necessary.

After excision of all fibrosed or necrosed soft tissues down to the periosteum, the sequestra

(if any) and the granulation tissue were removed and the cavity was curetted. The walls of

the cavity were excised, whenever possible down to healthy bone. We never tried to saucerise

the cavities. Once all infected material had been removed the tourniquet was taken off and

the way in which the walls bled was noted. In cases of any doubt the removal of bone was

FIG.

Chronic osteomyelitis of the tibia, with sinus. Figure 9-Appear-ance on admission. Figure 10-Two years after removal of sinus,necrotic soft tissue and infected bone and filling of cavity with

cancellous chips.

BONE GRAFTS ANt) CHRONIC OSTEOMYELITIS 677


continued until the remaining bone had a healthy aspect. The aim was always to obtain a

cavity with walls of well vascularised bone. This was always feasible when the lesion was in

the metaphysio-epiphysial region. In contrast, in the diaphysis this was very difficult and

sometimes impossible. The hard, compact structure of the diaphysis does not often allow

the creation of a new cavity with walls of bone tissue of normal aspect. After the wound had

FIG. 11 FiJ. 12

Chronic osteomyelitis of the femur with sinuses. Figure 1 I-Appearance on admission.Figure 12-Two years after removal of infected soft tissues and bone, and filling the cavity

with cancellous chips.



been cleaned and washed with physiological saline, the cavity was filled with cancellous bone

grafts mixed with antibiotic and gently impacted. With pseudarthrosis without great loss of

bone substance (ten cases) the procedure was similar. Once the infected soft tissue was removed

and the bone ends curetted in such a way as to leave only tissue with a reasonable appearance,

all the dead space was filled with cancellous grafts. After suture of the wound the limb was

put in plaster. A suction drain was used for forty-eight hours.

Type ofgrqft-ln 105 cases the only graft was of autogenous bone chips (iliac grafts removed

just before the operation on the infected region started). In eleven cases the graft was of

banked homologous cancellous bone. And, in four cases of pseudarthrosis with great loss of

substance, delayed cortical autografts were associated with bone chips.

RESULTS

The duration of follow-up was between two and ten years, with an average of five years.

Out of 120 patients 1 16 showed primary healing and are now free from infection. In four

patients there has been recurrence of infection.

Clinical review was supplemented by radiographs. We sought particularly evidence of

incorporation of the graft (Figs. 5 to 8). This was more rapid and more perfect in the

metaphysio-epiphysial region in the young patients. In some ofthem we found a true restitutio

ad inlegrurn (Figs. 9 and 10). But in the diaphysis the evolution had other aspects: although

in most the graft was incorporated, some bone sclerosis was always visible (Figs. I 1 and 12).

In seven patients the radiographs suggested recurrence, four of them in the cases with



FIG. 15 FIG. 16Examples of pseudarthrosis of the tibia and response to treatment by removal of infected soft tissuesand bone, and filling ofcavity with cancellous chips. Figure l3-Pseudarthrosis after osteomyelitis.Figure 14-Three years after operation. Homograft was used. Figure 15-Infected pseudarthrosis

after fracture and internal fixation. Figure 16-One year after operation.

FIG. 17 FIG. 18

Figure 17--Pseudarthrosis after osteomyelitis. Figure 18-Two years after operation. Homograftwas used.



clinical infection. All the cases were diaphysial infections, and a review of the clinical history

showed that in six the removal of sclerosed bone had not been adequate.

Analysis of the relapsed cases shows some interesting points. In two the infecting

organism was proteus vulgaris (besides staphylococcus aureus), resistant to a large number of

antibiotics. In both cases the surgical wound had never completely healed, the suppuration

persisting. At re-operation most of the grafted material was found sequestrated. In another

patient (a child eight years old with osteomyelitis of the tibia) the recurrence appeared six

weeks later, when the limb was still in plaster. The grafted material (bone bank) was partly

sequestrated. Finally, in another case of diaphysial affection the suppuration appeared about

four months after the operation, when the patient was already walking. Grafts from the iliac

bone had been used but with much cortical material. At re-operation it was confirmed that

the cancellous parts of the graft had taken while the cortical parts were sequestrated.

In all cases of pseudarthrosis we confirmed healing of infective process and bone

consolidation (Figs. 13 to 18).

Complications-In six cases the healing ofthe wound was not normal, the discharge continuing

for some weeks. In four of these cases the wound was healed after six weeks, while in two the

discharge persisted. The only serious complication was laceration of the femoral artery while

we were dissecting a sinus in the inner part of the thigh. The artery was sutured and the

operation was completed satisfactorily, progress and recovery being normal.

DISCUSSION

We must admit that the follow-up is a little short for appraisal of the efficacy of treatment

in a lesion with the elusive characteristics of chronic osteomyelitis. Recurrence of infection

is common, so time is the only test ofcure. However, we also know that ifchronic osteomyelitis

FIG. 19 FIG. 20

Results of excision of lesion and replacement with cancellous chips. Figure 19-Tomographs showinglesion in the upper tibial metaphysis. Figure 20-Three years after operation.

I -�FIG. 21 FIG. 22

Another example of excision of the lesion and replacement with cancellouschips. Figure 21-Chronic osteomyelitis of tibia, persistent after three

operations. Figure 22-One year after operation.

BONE GRAFTS AND CHRONIC OSTEOMYLLITIS 681


call relapse many times, it is the more likely to happen if radiographic appearances are suspicious.

And this, as stated already, was so in only a few cases. In a disease so variable as chronic

osteomyelitis it becomes difficult to define exactly the indications and contra-indications of

the method. The maui object of treatment is without any doubt to fill the cavity, eliminating

dead space. It is also important to leave a good circulatory background in the affected area,

riot only because it gives a better defence but also because only thus is it possible to profit

from the antibiotic.

FIG. 23 Ii,..,.

Infected cavity in the metaphysio-epiphysial region ofthe tibia, with fistula. Figure 23-Appearance beforetreatment. Figure 24-Two years after radical operation and filling of the cavity with bone chips.

682 J. C. DE OLIVE1RA


Our experience shows that cancellous bone has the desired resistance that the cortical

graft lacks, probably from the latter’s greater resistance to vascularisation.

For vascularisation of the graft it is necessary I) that the bed should be well vascularised,

and 2) that in the critical period in which the graft is not yet penetrated by vessels it should

not be floated off by discharge. Because it is almost always possible to find an appropriate

antibiotic, the problem, from the practical point of view, is only to change one osteomyelitic

cavity into another with better circulatory conditions. The ideal case-in which a bone

graft is certainly indicated-is that in which it is possible to remove the lesion completely,

leaving a cavity surrounded by healthy bone (Figs. 19 to 22). This is more often possible in

the metaphysio-epiphysial lesions. In our experience it was in this type of lesion (in which

it is more difficult to use saucerisation or a muscle pedicle) that we obtained speedier

incorporation of the graft and more perfect reconstruction of the trabecular structure of

the bone (Figs. 9, 10, 23 and 24).

In the diaphysial lesions total removal is harder to accomplish. The indication for bone

grafting will depend on the extent of the lesion and on the bone sclerosis present. If it seems

possible to remove all the affected bone, leaving a cavity with bleeding walls, the use of bone

grafts is advisable (Figs. I 1 to 1 6). Otherwise we have to choose another technique (saucerisation,

free skin graft, muscle pedicle) because the use of bone grafts under such circumstances is

dangerous, no matter how good the antibiotic protection may be.

Summing up our experience, we believe that, while chronic osteomyelitis has different

aspects from the anatomico-pathological and clinical points of view, its treatment must also

be undertaken by different procedures. Many of those used by other authors can be justified,

but none of them can be considered a panacea. It is time, we think, to emphasise the value

of bone grafts in treatment.

SUMMARY

1. In the treatment ofchronic osteomyelitis the most troublesome factor is the infected bone

cavity. This is seldom obliterated spontaneously by bone regeneration. The number of

procedures designed to fill the cavity, since the beginning of the century, show how much it

troubles the surgeon.

2. The use of bone grafts in the treatment of chronic osteomyelitis has been studied. One

hundred and twenty cases are reviewed (the largest series in the literature), the follow-up


being between two and ten years. The most common lesion was a bone cavity, with or without

a sequestrum.

3. Treatment must include the removal of infected soft tissues as well as sclerosed bone,

and must be done under appropriate antibiotic control. The value of cancellous bone grafts

in filling infected cavities in the metaphysio-epiphysial regions is especially emphasised.

4. The results were gratifying, only four relapses occurring in 120 cases.

REFERENCES

ABBOTr, L. C., SCHOTFSTAEDT, E. R., SAUNDERS, J. B. de C. M., and BOST, F. C. (1947): The Evaluation of

Cortical and Cancellous Bone as Grafting Material. Journal ofBone andJoint Surgery, 29, 381.BICKEL, W. H., BATEMAN, J. G., and JOHNSON, W. E. (1953): Treatment ofChronic Hematogenous Osteomyelitis

by Means of Saucerization and Bone Grafting. Surgery, Gynecology and Obstetrics, 96, 265.

BOYD, H. B., and LIPIN5KI, S. W. (1960): Causes and Treatment ofNonunion ofthe Shafts of the Long Bones,with a Review of 741 Patients. Instructional Course Lectures, 17, 165.

BUCHMAN, J., and BLAIR, J. E. (1951): The Surgical Management of Chronic Osteomyelitis by Saucerization,Primary Closure, and Antibiotic Control. Journal ofBone andJoint Surgery, 33-A, 107.

CLAWSON, D. K., and DUNN, A. W. (1967): Management of Common Bacterial Infections of Bones and Joints.Journal of Bone and Joint Surgery, 49-A, 164.

CLAWSON, D. K., and STEVENSON, J. K. (1965): Treatment of Chronic Osteomyelitis. Surgery, Gynecology and

Obstetrics, 120, 59.COLEMAN, H. M., BATEMAN, J. G., DALE, G. M., and STARR, D. E. (1946): Cancellous Bone Grafts for Infected

Bone Defects. A Single Stage Procedure. Surgery, Gynecology and Obstetrics, 83, 392.EVANS, E. M., and DAVIES, D. M. (1969): The Treatment of Chronic Osteomyelitis by Saucerisation and

Secondary Skin Grafting. Journal ofBone and Joint Surgery, 51-B, 454.

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KNIGHT, M. P., and WooD, G. 0. (1945): Surgical Obliteration of Bone Cavities following Traumatic

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