Eur opean Rev iew for Med ical and Pharmacol ogical Sci ences 2016; 20: 4670-4676 Iliac crest bone graft: a 23-years hystory of infection at donor site in vertebral arthrodesis and a review of current bone substitutes

L. BABBI, G. BARBANTI-BRODANO, A. GASBARRINI, S. BORIANI

Department of Oncological and Degenerative Spine Surgery, Istituto Ortopedico Rizzoli, Bologna, Italy

Abstract. – OBJECTIVE : This is an exemplary ognized drawbacks on iliac crest bone graft, in - case report underlining a relevant morbidity which cluding increased operative time, increased blood could be associated to the use of autologous iliac loss, increased donor site morbidity, and a limita - creCsAt bSoEn Re EgPraOfRt (TI:CBG) for spine fusion. tion to the amount that can be realistically har - Starting from 1990, a 25-years- vested for multilevel fusion 1. Successful fusion old woman underwent two subsequent surgical has been demonstrated following iliac crest bone treatments for non-Hodgkin lymphoma vertebral grafting in various applications in lumbar spine localizations. In the second surgery, arthrodesis 2,3 was obtained with autograft through right poste - surgery . However, the morbidity rates associat - rior iliac crest osteotomy. During the chemother - ed with the use of ICBG remain high, with some apy treatment following the surgery, the patient studies reporting up to a 50% rate of persistent suffered from infection at posterior iliac crest donor site pain, paresthesias, hematoma and in - scar, the site ofS ptraepvhioyulosc ogcrcaufts, caauuresueds by methi - fection 4. Other authors 5-8 describe a complication cillin-resistant . She was subjected to surgical debridement and specific rate ranging from 2.4% to 5.8% for major com - antibiotic treatment with local healing and phlo - plications and from 9% to 37.9% for minor com - gosis index reduction. Chemotherapy protocol plications. Because of donor site morbidity, spine was concluded and the patient healed with de - surgeons have increasingly used synthetic and re - finitive lymphoma remission. After 22 years the combinant bone graft extenders, and a whole in - patient had a relapse of donor site infection, re - dustry has arisen from this market 9: local auto - quiring a new antibiotic therapy and a new sur - graft, allograft, demineralized bone matrix gicRaEl SdUebLTriSd: ement. The relapsed infection at donor site (DBM), synthetic bone grafts (ceramics), bone lasted for a long period, more than one year, de - morphogenetic proteins (BMPs), autogenous spite of specific care. It finally healed after an - growth factors (AGFs), bone marrow aspirate other accurate surgical debridement and post - (BMA) and collagen -based matrices are the most opCerOaNtivCeL aUnStIiObiNotSic: therapy. popular bone graft substitutes gaining popularity This case report underlines and being increasingly used in the lumbar spine. the possible consequences on the patient’s quality of life of a long-term disease affecting We report here a peculiar case of a 25 years the iliac crest bone graft donor site. Literature ICBG site infection in a patient submitted to re - concerning alternatives to autograft for spine fu - vision surgery because of a T10 non -Hodgkin sion is also reviewed. lymphoma: the intention of this exemplary case Key Words: report is to remind how the morbidity in auto - Spine fusion, Iliac crest bone graft, Bone substi - graft shouldn’t be underestimated and it also rep - tutes, Donor site, Morbidity . resents an occasion to review the synthetic alter - natives and report our experience in this field. Case Report Introduction A 49 -years -old woman presented at admission with worsening pain at right pelvis and recurrent Iliac crest bone autograft (ICBG) has long fever. Twenty-two years before, she underwent a been considered the gold standard for fusion pro - surgical debridement for an infection due to Me - cedures in spine surgery. However, there are rec - thicillin-Resistant Staphylococcus aureus (MR -

Corresponding Author: Lisa Babbi, MD; e-mail: [email protected]. 4670 Iliac crest bone graft

SA) occurring at iliac crest in the site of a previ - blood phlogosis index negativity . Currently, the ous bone autograft. Microbiological results from body scan is negative, the wound healed and the needle biopsy confirmed an active MRSA local patient is asymptomatic. infection at posterior iliac crest where a fistula appeared. Discussion The patient’s history was collected: in July 1990 the patient (aged 25 -years -old) was referred to our unit because of a T10 neoformation com - In order to achieve fusion in vertebral surgical pressing the epidural space and submitted to T10 procedures , the instrumentation can stabilize the posterior decompression and secondary T9 -T11 spine at first and then the final success depends stabilization with Hartshill hardware. Twenty on both biological and host factors, which deter - months later a T8 wedge fracture occurred and mine fusion to the adjacent bone segment. Many the patient was urgently admitted to our unit and spinal fusion procedures require the use of bone underwent hardware removal and new arthrode - grafts, and spinal fusion largely depends on the sis with T6-T12 Roy-Camille plates. Arthrodesis osteoconductive and osteoinductive properties of was obtained with autograft through right poste - bone grafts or their substitutes. rior iliac crest osteotomy. The histological exam The massive amount of cancellous bone that revealed a high -grade non -Hodgkin lymphoma can be obtained from the inner table of the pelvis and patient was addressed to the Onco-Hemato - provides all the desired properties of osteocon - logic Unit. Two months after discharge the pa - duction, osteoinduction and osteogenicity, neces - tient began chemotherapy according to the F- sary to obtain a solid arthrodesis. The large sur - MACHOP protocol consisting of 6 cycles, but face area of this bone graft has the optimal chem - soon after the first cycle a fistula appeared in the istry, structure, and porosity to serve as an excel - wound scar at the right iliac crest, the site of the lent scaffold for new bone formation. Similarly, previous graft. Phlogosis blood index increased. it contains all the necessary bone -forming growth Subsequent hospitalization was necessary and factors and it is inherently osteoinductive. Fur - microbiological diagnosis of methicillin-resistant Staphylococcus aureus (MRSA) infection at pos - terior iliac crest scar was made after swab. A sur - gical debridement of the abscess was performed , washing drains were left in place for few days and a treatment with specific antibiotic was per - formed for other 8 days with local healing and phlogosis index reduction. Chemotherapy protocol was concluded and the patient healed with definitive lymphoma remis - sion. The patient underwent regular clinical and radiological follow-up; she stayed asymptomatic, both at lumbar and iliac crest sites, for several years until Summer 2014 when symptoms and local signs of donor site infection relapsed. At this time an antibiotic specific therapy with Daptomycin, Oxacillin and Linezolid started , and a new surgical debridement was performed . Despite the specific care , the infection was still present in Autumn 2015, after 23 years from the graft, when the patient came back to our at - tention. At admission , she presented painful at the right side with a purulent fistula at the donor site (Figure 1). Surgical debridement was performed (Figure Figure 1. 2) with wide curettage of the pathological area Preoperative CT images of iliac donor site infec - and copious washings . A postoperative specific tion 23 years after grafting. A central large osteolysis is sur - antibiotic therapy started and continued until rounded by sclerotic bone.

4671 L. Babbi, G. Barbanti-Brodano, A. Gasbarrini, S. Boriani

Figure 2. (A, B) Preoperative MRI (C) shows liquid at iliac crest contest hyperintense inD ,T2 and hypointense in T1, compatible with purulent material. PET scan confirms contrast enhancement at iliac right site. Preoperative cutaneous fistula. thermore, cancellous bone is easily re-vascular - rates ranging from 4 to 49%. These complica - ized and rapidly incorporated at the host site. tions included superficial infection, minor wound There are no concerns for disease transmission problems, temporary sensory loss, and mild or and no risks of immunogenicity 10 . The use of ili - transient pain . Swan and Goodacre 17 studied the ac crest bone graft (ICBG) has been well-sup - complications of iliac bone harvesting in 72 pa - ported in the literature 2,3,11,12 with fusion rates as tients. The postoperative donor site complica - high as 93%. Nowadays , it is considered the gold tions included persistent pain at the donor site in standard in spine fusion. 7% of cases (all resolved within 6 months) and Morbidity associated with its use is also well superficial wound infections in 3% of cases (suc - reported. Donor site morbidity can be attributed cessfully treated with oral antibiotics). In all of to the harvesting procedure of the ICBG. This the studies reviewed, there were no reports of procedure is associated with longer operative long-term infective complications at the iliac times, increased estimated blood loss, and a crest donor site. longer hospital stay 13,14 . Major complications In the literature there are others example of have been reported ranging from 0.7 % to 25%, wound /donor site infection after ICBG proce - including infection, prolonged wound drainage, dures: Calori et al 18 found local infections at the large hematomas, reoperation, pain lasting more donor site in 14.28% cases of ICBG group; ac - than 6 months, sensory loss, scar, joint subluxa - cording to Pirris et al 9, one patient (4%) of his se - tion, gait disturbances, sacroiliac joint destabi - ries developed a deep wound infection that re - lization, herniation of abdominal muscles and quired operative irrigation and debridement. Ar - contents, iliac or pelvis fracture, and heterotopic maghani et al 19 report one superficial wound in - bone formation 15,16 . Minor complications are fection and a postoperative hematoma , both of more common, with a reported complications which were treated successfully with close obser -

4672 Iliac crest bone graft vation and oral antibiotics; they register no deep freeze-dried allograft bone in posterolateral lum - wound infections requiring a revision surgery or bar fusions have wide variability in the litera - a readmission to the hospital. ture 23 , probably due to its poor osteogenic or os - Similarly to our case report, De Riu et al 20 re - teoinductive properties that do not induce new port an unusual complication: a huge iliac ab - bone formation in the same manner as the auto - scess that appeared 4 years after bimaxillary genous bone graft. Moreover, they generally pro - surgery involving iliac bone grafts. Concerning vide no initial mechanical support and must be our case report, at our knowledge 25 years de - used in conjunction with a scaffold or fixa - layed abscess has never been described before as tion 24,25 . a complication in ICBG donor site morbidity. Ceramics are osteoconductive and biodegrad - For these reasons, much progress has been able bone graft scaffolds 26-30 . These agents con - β made in the field of bone graft alternatives for sist of coralline hydroxyapatite, -tricalcium spinal fusion; approximately 1,400 products are phosphate, silicate-substituted calcium phos - available on the international market for use as phate, calcium sulfate, or a combination of these bone void fillers. We briefly review the main minerals. Ceramics have several advantages; ICBG alternatives. they are nontoxic, nonimmunogenic, easy to ster - Local autograft: Park et al 21 have shown ilize, and have limitless availability. Their disad - equivalent fusion results for local laminectomy vantages are that they are brittle and have a little bone autograft (ALB) and ICBG in a single level shear strength or fracture resistance. Because posterolateral fusion . they offer minimal mechanical stability in the Allograft bone has been the most widely used immediate postoperative period, ceramics are as a substitute to avoid complications of donor usually insufficient as scaffolds in lumbar fusion site morbidity, but its use is associated with an surgery 22,30 . increased risk of infection and rejection, and it Platelet gels are osteoinductive and are used as has poor osteoinductive properties 22 . The report - bone graft enhancers in conjunction with ICBG, ed fusion rates with the use of fresh-frozen or ALB, or allograft bone. It would make logical

Figure 3. A, B, C, Intraoperative debridement with iliac crest bone milling. Postoperative CT showing bone defect after donor site debridement.

4673 L. Babbi, G. Barbanti-Brodano, A. Gasbarrini, S. Boriani sense that the addition of platelet gel to autolo - tissue similar to autologous bone in a higher gous iliac crest would enhance fusion rates due amount with respect to HDBM-MgHA. Finally, β to the presence of TGF- and PGDF. However, the bone surface to volume ratio parameter, a use - clinical study findings refute this hypothesis. Po - ful basic 3-dimensional parameter in characteriz - tential reasons for these results include rapid dis - ing the complexity of structures, showed that solving of the platelet gel and diffusion of newly formed trabecular bone around MgHA bio - growth factors 29 . material presented a greater surface than autolo - With reported fusion rates of 95% to 98%, gous bone 39 . The Authors considered the combi - bone morphogenetic proteins have revolutionized nation of osteoinductive and osteoconductive ma - the ability to achieve successful fusion in the terials such as DBM and concluded it can be a lumbar spine. BMP induces bone formation by valid alternative to the autologous/homologous influencing mesenchymal stem cells. Disadvan - bone, thus perhaps overcoming the limitation of tages include ectopic bone formation in the neur - current therapeutic strategies. al foramen and the central canal after BMP use; radiculitis, occurring just days after surgery, is al - Conclusions so a known complication of BMP use, osteolysis also a serious complication following BMP use. Wound dehiscence and infection have been re - Major and minor complications at donor site ported in multiple papers 31 . are described in the literature. An ideal bone Bone marrow aspirate (BMA) is both osteoin - graft substitute with little or no associated com - ductive and osteogenic. It is typically used with a plications and risks does not exist at this time. structural graft to give it mechanical strength. Its Currently, autograft is considered to be the gold inherent advantages are the minimal harvesting standard but it shows few limitations: this case site morbidity and the high amount of Demineral - report describes a 25 -years disabling ICBG ized Bone Matrix (DBM) which has emerged to donor site morbidity that required revision surg - enhance, and often supplant, the use of freeze- eries during years. The recent development of dried allograft. DBM retains the same properties bone graft substitutes represents a great advance as freeze-dried allograft but without the mineral in caring for these patients. Each graft alternative content. It serves as an effective osteoconductive has advantages and disadvantages, and the op - scaffold and contains type I collagen and non-col - tions must be considered on an individual, risk - lagenous proteins. Much like allograft it is rela - benefit basis to select the best option for each pa - tively inexpensive and unlimited in quantity com - tient undergoing spinal fusion. This case report pared to ICBG. Its main disadvantage is the in - also underlines the possible consequences on the herently variable osteoinductive properties. The quality of life in patients with rare , but still possi - osteoinductivity of DBMs has been well docu - ble , chronic long -term donor site disease. mented in preclinical studies 32-34 . However, few clinical studies have evaluated the efficacy of DBM as a bone graft extender in instrumented –A–c–k–n–o––w–l–e–d–g––e–m––e–n–t–s posterolateral fusion with respect to an iliac crest 35,36 The Authors thank Mr. Carlo Piovani for his helpful collab - bone autograft alone . Our experience consists oration in patients’ images storage and editing and Dr. Cris - on an in vivo study aimed to carry out an evalua - tiana Griffoni for support in the manuscript editing . tion of the osteoinductive and osteoconductive properties of two bone substitutes composed of C––o–n––f–li–c–t– –o–f– I–n––te– –r-e– s–t– MgHA granules or HDBM-MgHA dispersed in a biomimetic matrix, which has previously shown The Authors declare that there are no conflicts of interest. in vitro 37,38 biocompatibility and biological propri - eties similar to an autograft. The osteogenic abili - References ty of these compounds was evaluated and com - pared with a cortical-cancellous bone autograft in FRANCE JC, S CHUSTER JM, M ORAN K, D ETTORI JR. an ovine model of lumbar spine instrumented fu - 1) Iliac crest bone graft in lumbar fusion: the effective - sion to reproduce a model as close as possible to ness and safety compared with local bone graft, the surgical procedure performed on humans. Our and graft site morbidity comparing a single-inci - histomorphometric results showed that MgHA sion midline approach with a two-incision tradi - stimulated the deposition of newly formed bone tional approach. Global Spine J 2015; 5: 195-206.

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