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_:	Infectious spondylitis: Characteristics of geriatric patients

Takao Yasuhara, M.D.1), Yuichi Takahashi, M.D.2), Yasukazu Hijikata, M.D.2),
Tetsuya So, M.D.3), Shinji Kumamoto, M.D.2), Masayuki Nakahara, M.D.2), Takashi Tanoue, M.D.2), Akira Kusumegi, M.D.2), Takafumi Inoue, M.D.2), Koichi Ogawa, M.D.2), Hiroaki Manabe, M.D.1), Yasuyuki Miyoshi, M.D.1), Isao Date, M.D.1), Kenki Nishida, M.D.2)

Department of Neurological Surgery, Okayama University Graduate School of Medicine, Okayama, JAPAN1); Department of Spine and Spinal Surgery2), Department of Respiratory Surgery3), Shinkomonji Hospital, Fukuoka, JAPAN

Send Correspondence to:
Takao Yasuhara, M.D., Ph.D.
Department of Neurological Surgery 
Okayama University Graduate School of Medicine
Address: 2-5-1, Shikata-cho, Kita-ku, Okayama, 700-8558, JAPAN
Phone: 81-86-235-7336; Fax: 81-86-227-0191; 
Email: tyasu37@cc.okayama-u.ac.jp

Key words: delirium, discectomy, fusion surgery, geriatric patients, infectious spondylitis 
Running head: geriatric patients with infectious spondylitis

There is no conflict of interest to be declared.
ABSTRACT
Purpose: The goal of this study is to identify the characteristics and common problems of geriatric patients with infectious spondylitis and to explore possible solutions for them.
Methods: This is a retrospective study. Out of a total of 26 patients with infectious spondylitis who were treated as inpatients, the 18 geriatric patients were studied in detail and compared with non-geriatric patients with regard to systemic complications, psychological symptoms, clinical stages, pathogenic factors, surgeries and length of hospital stay. Illustrative cases are described to demonstrate our strategy for infectious spondylitis.
Results: In geriatric patients with infectious spondylitis, certain perioperative complications including cardiac complications, psychological symptoms and pseudomembranous enterocolitis were recognized to be characteristic of the patient population, although no correlations were significant because of the small number of cases. In most geriatric patients, clinical manifestations indicated a subacute or chronic stage of infection without colic pain or high fever. Eight of the 18 geriatric patients underwent surgery including discectomy, fusion surgery and removal of previous instrumentation. Subsequently, infection was controlled in all 18 patients. 
Conclusions: To improve outcomes in geriatric patients with infectious spondylitis, it is critically important to diagnose and treat any complications in their early stages in conjunction with the relevant hospital department. Additionally, early nutritional support, rehabilitation and treatment for psychological problems should be performed to prevent disuse syndrome.
Key words: delirium, discectomy, fusion surgery, geriatric patients, infectious spondylitis
INTRODUCTION
The number of geriatric patients with infectious spondylitis is increasing as Japan�s population ages. Early diagnosis and conservative therapy are the mainstays of treatment for infectious spondylitis. Conservative therapy consists of identifying the etiological agent, administering appropriate antibiotic drugs, controlling pain and fever, and improving the patient�s general condition. For patients with progressive paralysis or resistance to conservative therapy and for patients who need early aggressive treatment in order to ameliorate their general condition, surgical treatment is preferred. In geriatric patients, the possibility of complications from a treatment is also a critical issue. Steps must be taken to control any perioperative risks and to minimize disuse syndrome when surgical treatment is considered for geriatric patients with infectious spondylitis. In this manuscript, we report on the results of treatment at our institute, with special attention to the characteristics of geriatric patients with infectious spondylitis and the remedial issues to be overcome.


MATERIAL AND METHODS
Over the course of two years, from January 2010 to December 2011, we treated 26 patients with infectious spondylitis as inpatients. All patients gave full informed consent and this study was approved by our institutional ethical committee. The patients were retrospectively divided into two groups. Patients in the geriatric group were 70 years old or older and those in the non-geriatric group were under 70 years old. The characteristics, complications and length of hospital stay were compared between the two groups. 
Statistical analyses were performed using the Chi-square test, except in the case of number of days in the hospital, which was analyzed using Mann-Whitney�s U test. Statistical significance was preset at p<0.05. 


RESULTS
Characteristics of the patients
Out of the 26 patients with infectious spondylitis, 18 were in the geriatric group (male: 12, female: 6; age: 77�1.4 (70-89) years old) and 8 were in the non-geriatric group (male: 4, female: 4; age: 58�2.5 (43-64) years old). The lesions in the geriatric group were located in the cervical spine in two patients, in the thoracic spine in four, in the lumbar spine in 11 and at multiple sites in one. The lesions in the non-geriatric group were located in the cervical spine in one patient, in the thoracic spine in one and in the lumbar spine in six. Surgery was performed on eight out of the 18 geriatric patients and two out of the eight non-geriatric patients. Detailed information on the geriatric patients is shown in Table 1.

Comparison between geriatric and non-geriatric groups
In order to identify the typical characteristics of geriatric patients, data on all 26 consecutive patients including complications, clinical entities, outcomes and lengths of hospital stays are given in Table 2. There were no significant differences in any of the evaluated factors, although some tendencies were recognized. As regards systemic complications, diabetes mellitus was predominant in the non-geriatric group and cardiac complications, pseudomembranous enterocolitis and psychological symptoms as represented by delirium were more common in the geriatric group. Two patients, one in each group, developed infectious spondylitis after trigger point blocks. Many patients had been referred by other clinics after receiving conservative therapy; this fact might have made it less likely that the causative microorganism could be identified. There was no difference between the groups in the rate of cases with previous instrumentation surgeries. As regards surgery, various operative procedures were performed in geriatric patients, but fusion surgery was performed in both non-geriatric patients. There was no difference in length of hospital stay between the two groups. In non-geriatric patients, high fever in the acute stage [1] was commonly seen. 

Treatment and outcomes of geriatric patients
Ten of the 18 geriatric patients received conservative therapy only, while the other eight underwent surgery; all cases also received early rehabilitation within three days after admission. Percutaneous aspiration of fluid collected around the instrumentation was performed in one case without subsequent identification of the causative microorganisms (Case 1). For four patients with high fevers, blood culture was performed (Cases 2, 14, 16 and 17), but the causative microorganism was identified in only one case (Case 16). Of the eight surgical cases, two underwent anterior-posterior fusion with autologous bone graft, one underwent posterolateral fusion, three underwent discectomy and two underwent removal of the previous instrumentation. Among the 18 total cases (including the eight surgical cases), the causative microorganism was identified in only three cases. Nevertheless, the infection was controlled in all 18 geriatric cases. By August 2012, 11 patients were capable of independent gait, six were capable of short-range gait with subtle assistance and one could stand up with full support.

Representative cases
Case 7
A 71-year-old man with a two-month history of back pain was medically treated with antibiotics including linezolid at another institute after receiving a diagnosis of infectious spondylitis one month after onset. During treatment, he developed paraparesis and was referred to our institute. Neuroradiological investigations revealed an infected lesion at Th9/10 with fluid collection at the disc and spinal canal stenosis. CT revealed the combined features of osteosclerosis and osteolysis (Figure 1). He received laminectomy for decompression of the cord five days after admission because his paraparesis had worsened (MMT: 3/5 from 4/5). Erythromycin was effective as evidenced by decreases in leukocyte number and CRP level. Twenty-two days after admission, an anterior-posterior fusion using an iliac bone graft was performed (Figure 1). The infected lesion was controlled after surgery and the patient was transferred to a rehabilitation hospital 64 days after admission. He received follow-up care as an outpatient and wore a hard corset; eventually, his paraparesis was completely cured. By 14 months after surgery, bone fusion was achieved and the instrument was removed (Figure 1). 
Case 14
An 85-year-old man with back pain and high fever was treated medically with antibiotics for one month at another institute with a diagnosis of pneumonia. He eventually developed paraparesis and was transferred to our institute. Neuroradiological investigation revealed a lesion in the region of Th7/8 to Th9 with a paravertebral abscess expanding anterolaterally (Figure 2). We performed thoracoscopic discectomy with the aid of a respiratory surgeon (Figure 3) two days after admission because of the patient�s advanced age, wide expansion of infection, exacerbation of symptoms (MMT 2/5 from 3/5) and laboratory data reflecting persistent infection in spite of medication. Severely extended infection discouraged us from performing fusion surgery on this patient. Based on a culture from the infection focus, Serratia was unexpectedly identified as the causative microorganism. Through the use of meropenem as an appropriate antibiotic, his infection was controlled. For one month after surgery, he was bedridden; subsequently, he became able to sit up and began rehabilitation with the aid of a hard corset, although his prolonged immobility caused temporary delirium. Fifty-six days after admission he was transferred to a rehabilitation hospital; we followed up with him as an outpatient once a month. Nine months after admission, he could walk with subtle assistance and went to live at home with his family. His infection was cured with bone fusion at Th8/9 (Figure 2). 


DISCUSSION
This study is the first to identify the characteristics of infectious spondylitis in geriatric patients through representative case presentations. In geriatric patients, psychological symptoms, cardiac complications and pseudomembranous enterocolitis are more common than they are in non-geriatric patients, although there were no significant differences between the geriatric and non-geriatric groups in any of our analyses because of the small number of patients enrolled in this study. Fusion surgery with autologous bone, discectomy and removal of previous instrumentation were the means by which our patients achieved infection control. 
	
Problems and solutions pertaining to infectious spondylitis in geriatric patients 
There are no previous reports on geriatric cases of infectious spondylitis. In the study related to geriatric patients over 80 year old receiving spinal surgery, preoperative complications were recognized in 72% of cases and postoperative complications in 18% [2]. Geriatric patients are especially susceptible to postoperative delirium. In our study, psychological symptoms including delirium were found only in geriatric patients (7/18, 39%), not in non-geriatric patients (0/8). Our data does not suggest a solution to this problem, but participation in a hospital elder-life program might be helpful [3]. Hospital elder-life program consists of early rehabilitation, nutritional assistance, and therapeutic (cognitive) activities implemented by a trained nurse. With the program, geriatric patients receiving common abdominal surgical procedures experienced significantly less decline in the performance of activities of daily living and nutritional status than patients without the program did. Furthermore, the rate of delirium was significantly lower in patients enrolled in the program (0%) than in patients not enrolled (17%). With the advancement of therapeutic modalities for infectious spondylitis, the number of treatable geriatric patients is expected to increase. Therefore specialized programs for geriatric infectious spondylitis patients should be seriously considered.

Surgery for infectious spondylitis
Discectomy and drainage
Discectomy is an effective method of identifying causative microorganisms in infectious spondylitis. Additionally, the antibiotics administered systemically in discectomy might effectively reach the infection focus, with subsequent therapeutic effects due to a break in the capsule of the infection focus. Recently, the development of endoscopic and percutaneous devices has enabled us to perform discectomy more easily than before [4, 5]. In a study using endoscopic discectomy and drainage [5], the rate of identification of causative microorganisms in addition to relief of symptoms was 87% (13/15 cases). Out of a total of 15 cases, four (27%) required additional surgeries other than endoscopic surgeries, including anterior debridement and fusion. In another study, the rate of identification of causative microorganisms by endoscopic discectomy (90%) was greater than that by CT-guided biopsy (47%) [6], although CT-guided biopsy is also a good diagnostic strategy. In our 18 cases over two years, discectomy was performed in three cases, one using an anterior cervical approach, one using a thoracoscopic approach, and one using a retroperitoneal approach. The causative microorganism was identified in two of these three cases. In all three discectomy cases, control of infection was consequently achieved without further surgical procedures. The low rate of identification of causative microorganisms might be at least partially due to the fact that most of our patients were introduced from other institutes after having received some medication. Overall, however, discectomy and drainage is an effective therapeutic tool for infectious spondylitis. 

Fusion surgery
Recent studies have demonstrated that fusion surgery with autologous bone grafts is effective for infectious spondylitis at the lumbar level [7, 8], although a titanium mesh cage is also usable for infectious spondylitis in the cervical spine [9]. In our institute, early fusion surgery using autologous bone grafts was performed on some patients with infectious spondylitis, although foreign material placed directly into the infectious focus at the acme phase of infection was avoided. Early stabilization with measured instrumentation might be the most important and effective way to control infection, although patients with extensive lesions or poor systemic conditions should be excluded. In addition to autologous bone grafts, iodine-coated instrumentation might be highly effective [10]. Another study reported on 222 patients with postoperative infection or compromised status, including 82 patients who had undergone spinal surgery, who were treated using iodine-coated titanium implants. These iodine-coated implants were used in 64 cases of acute infection, and in all cases the infection was controlled without instrumentation failure. The use of instrumentation with anti-infectious properties like these iodine-coated implants might be one of the strongest therapeutic modalities for infectious spondylitis in the near future.


CONCLUSION
The present study identified several perioperative complications, including cardiac complications, psychological symptoms and pseudomembranous enterocolitis, as common characteristics of geriatric patients with infectious spondylitis. Clinical manifestations in most geriatric patients were at a subacute or chronic stage of infection without colic pain or high fever. Almost half of the geriatric patients underwent surgery of some kind, depending on the patient�s condition and lesions, with consequent favorable outcomes, indicating that surgical intervention should not be avoided simply on account of advanced patient age. To improve outcomes in geriatric patients with infectious spondylitis, it is critically important to diagnose and treat complications early in association with the relevant hospital department. Additionally, early nutritional support, rehabilitation and treatment for psychological problems should be performed to prevent disuse syndrome. 
REFERENCES 
1.	Kulowski J. (1936) Pyogenic osteomyelitis of the spine. J Bone Joint Surg 18A: 343-64.
2.	Horiuchi H, Ogata T, Morino T, Mirizane K, Yamaoka G, et al.  (2012) Complication of spine surgery in patients aged eighty years or older. J Spine Res 3: 811-4.
3.	Chen CC, Lin MT, Tien YW, Yen CJ, Huang GH, et al. (2011) Modified hospital elder life program: effects on abdominal surgery patients. J Am Coll Surg 213: 245-52.
4.	Wattamwar AS, Ortiz AO. (2010) Use of a percutaneous diskectomy device to facilitate the diagnosis of infectious spondylitis. AJNR Am J Neuroradiol 31: 1157-1158.
5.	Yang SC, Fu TS, Chen LH, Niu CC, Lai PL, et al. (2007) Percutaneous endoscopic discectomy and drainage for infectious spondylitis. Int Orthop 31: 367-373.
6.	Yang SC, Fu TS, Chen LH, Chen WJ, Tu YK. (2008) Identifying pathogens of spondylodiscitis: percutaneous endoscopy or CT-guided biopsy. Clin Orthop Relat Res 466: 3086-3092.
7.	Gonzalvo A, Abdulla I, Riazi A, Harpe DL. (2011) Single-level/single-stage debridement and posterior instrumented fusion in the treatment of spontaneous pyogenic osteomyelitis/discitis: long-term functional outcome and health-related quality of life. J Spinal Disord Tech 24: 110-115.
8.	Lee JS, Suh KT. (2006) Posterior lumbar interbody fusion with an autogenous iliac crest bone graft in the treatment of pyogenic spondylodiscitis. J Bone Joint Surg Br 88: 765-770.
9.	Heo W, Kang DH, Park KB, Hwang SH, Park IS, et al. (2011) Is titanium mesh cage safe in surgical management of pyogenic spondylitis? J Korean Neurosurg Soc 50: 357-362.
10.	Tsuchiya H, Shirai T, Nishida H, Murakami H, Kabata T, et al. (2012) Innovative antimicrobial coating of titanium implants with iodine. J Orthop Sci 17: 595-604.
TABLE AND FIGURE LEGENDS
Table 1: Data on geriatric patients with infectious spondylitis
Sex/age, Clinical stage (Kulowski), main symptoms, effective antibiotics, causative microorganism (bacteria), surgery, background/complications, and length of hospital stay of each geriatric patient are shown. ADF: anterior discectomy and fusion; Af: atrial fibrillation; ALIF: anterior lumbar interbody fusion; CHF: chronic heart failure; CRF: chronic renal failure; DM: diabetes mellitus; EM: erythromycin; FOM: fosfomycin; fx.: fracture; MEPM: meropenem; MINO: minocycline; MSSA: methicillin-sensitive Staphylococcus aureus; OP: operation; PLF: posterolateral fusion; SBT/ABPC: sulbactam/ampicillin

Table 2: Differences between geriatric and non-geriatric patients
Evaluated factors and their rates in both groups are shown. Statistical analysis was performed by means of the chi-square test for each factor. *Mann-Whitney�s U test was used for analysis of length of hospital stay. P values are shown for each factor. CM: causative microorganism; CT: conservative therapy; DM: diabetes mellitus; PE: pseudomembranous enterocolitis; PS: psychological symptoms; Pts: patients; RI: removal of instrumentation 

Figure 1: Neuroradiological investigation of case 7
a-d: Preoperative MRI (a, c) revealed a lesion at Th9/10 with fluid collection at the disc and spinal canal stenosis (a: sagittal, c: axial). CT images revealed the combined features of osteosclerosis and osteolysis (b: sagittal, d: axial). 
e: A sagittal CT image revealed laminectomy for decompression of the cord. 
f, g: CT images demonstrated anterior-posterior fusion using an iliac bone graft (f: sagittal, g: axial). 
h: A CT image showed bone fusion with removal of the instrument at 14 months after fusion surgery. 

Figure 2: Neuroradiological investigation of case 14
a-d: Preoperative MRI (a, c) revealed a lesion at Th7/8 to Th9 with a paravertebral abscess expanding anterolaterally (a: sagittal, c: axial). CT images revealed an osteolytic lesion with an expansive abscess (b: sagittal, d: axial).
e-h: Postoperative MRI (e, g) obtained nine months after surgery demonstrated the shrinkage of the abscess and the disappearance of fluid collection at the Th7/8 and 8/9 level (e: sagittal, g: axial). CT images revealed bone fusion at Th8/9 with the shrinkage of the abscess (f: sagittal, h: axial). 

Figure 3: Discectomy at Th8/9 using a thoracoscope
a: The adhesion between the visceral pleura and parietal pleura was detached.
b: The abscess was opened near the vertebral body.
c: The abscess was widely opened to the vertebral body using a monopolar electrical cautery.
d: Discectomy was performed.








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