The Intensive Care Society 2009

Original articles

The sepsis syndrome in odontogenic infection

T Handley, M Devlin, D Koppel, J McCaul
Odontogenic infection is a common cause of sepsis in the head and neck. Infection frequently spreads in a predictable pattern within the fascial spaces of the neck and can result in airway compromise. Often the condition results in significant morbidity and a prolonged hospital stay. In this study, we assessed the incidence of sepsis syndrome in patients presenting to a regional maxillofacial unit with odontogenic infection. Six months of prospective data were collected, with sixty-seven patients included. The focus of infection was mandibular in 70.1% and maxillary in 29.9%. The mean length of stay was four days and 61.2% of patients were diagnosed with sepsis syndrome on admission. This group remained in hospital significantly longer than non-sepsis syndrome patients (sepsis=4.7 days, non-sepsis=2.9 days. p=0.0145.) The site of infection was not a significant factor in the development of the systemic inflammatory response syndrome (SIRS).
Keywords: sepsis; odontogenic infection; systemic inammatory response syndrome (SIRS); dental infection

Introduction
The sepsis syndrome and related disorders have been described and the denitions used in clinical practice since 1992. These are summarised in Table 1. The systemic inammatory response syndrome (SIRS) is a progressive, pathophysiological process which may be caused by a variety of clinical precursor events including local or generalised infection, or non-infective inammatory processes such as trauma, burns or pancreatitis. The sepsis syndrome is dened as SIRS with an identiable source of infection, and is caused by the interplay of microorganism virulence factors with the host inammatory response. SIRS is the rst stage of the systemic host response to infection or injury, and is dened as occurring in any patient with any two or more of the four clinical criteria shown in Table 2. These parameters were initially agreed and published jointly by the American College of Chest Physicians and the Society of Critical Care Medicine in 1992.1 They were reafrmed in 2001 by these societies and also by the European Society of Intensive Care Medicine, the American Thoracic Society and the Surgical Infection Society.2 While there has been some controversy regarding the inclusion of further criteria for the denition of sepsis, the original concepts remain robust and have been shown to be useful denitions both for clinical research and for patient management.2 These criteria are the accepted international standard, but awareness of the specic parameters has been demonstrated to be low among both intensivists and other physicians and surgeons.3 In the Poeze et al study, only 20% of participants correctly gave respiratory rate >20/min as a parameter for SIRS. A similar level of SIRS awareness and recording was found previously in our own institution (Handley, Devlin, McCaul et al, 2003, unpublished data). The sepsis syndrome is dened as the presence of conrmed
JICS Volume 10, Number 1, January 2009

Parameter Bacteraemia

Definition The presence of viable bacteria in the blood Microbial phenomenon characterised by an inflammatory response to the presence of microorganisms or the invasion of normally sterile host tissue by those organisms The response to a variety of severe clinical insults manifested by two or more of the SIRS criteria (see Table 2) SIRS + suspected/documented infection Sepsis + sepsis-induced organ dysfunction Sepsis-induced hypotension despite adequate fluid resuscitation and perfusion abnormalities such as lactic acidosis, oliguria, altered mental status A systolic blood pressure <90 mm Hg or a reduction of 40 mm Hg from baseline in the absence of other causes of hypotension

Infection

Systemic inflammatory response syndrome

Sepsis Severe sepsis

Septic shock

Sepsis-induced hypotension

Table 1 Definition of sepsis and related disorders.

or suspected infectious agents with two or more of the SIRS criteria.2 The syndrome affects 500,000 patients per year in the USA and is associated with 35-45% mortality.4 In patients who succumb, the condition progresses to severe sepsis when organ dysfunction occurs, and then to septic shock with hypotension (see Figure 1). Mortality from sepsis-induced organ failure has been shown to be improving in some patient subgroups, even
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Criterion Temperature Pulse rate Respiratory rate White cell count (WCC)

Positive result <36C or >38C

Maxillofacial Sepsis: Admission Sheet Insert Label

>90 beats per minute >20 breaths per minute <4 or >12 x 109/L

Patient Details:

Table 2 Systemic inflammatory response syndrome criteria.

Date of Admission: ../../.. Temperature: <36 or >38

Ward: 62/HDU/ITU

Infection

Pulse Rate: >90

+
SIRS

Sepsis

Severe sepsis

Septic shock

Respiratory Rate: >20 White Cell Count: <4 or >12 Tick as appropriate

Figure 1 Pathogenesis of the sepsis syndrome.

Septic Focus:

Mandibular Dentition Dentition

without specic sepsis therapies.5 These survival enhancements have been speculated to be due to changes in denition, but importantly also due to early recognition and initiation of supportive and appropriate surgical and antimicrobial intervention.4 Infection in the head and neck is a common presentation in maxillofacial surgery, the majority being odontogenic in origin.6 This particular source of infection can rapidly spread through the anatomical spaces of the head and neck through the path of least resistance in a predictable pattern (see Figure 2). In severe cases, this can compromise the airway, necessitating surgical airway management. Signicant morbidity has also been reported by spread to other anatomical regions or tissues.7,8
Maxillary sinus

Salivary Gland Lymph Node Treatment: IV Antibiotics Surgery

Figure 3

Buccinator muscle

Deep lobe of submandibular gland Mylohyoid muscle

A recent retrospective review has identied parameters at presentation which may contribute to increased susceptibility to odontogenic infection and increased hospital stay. In a study of 22 patients, serum prealbumin was shown to be low in odontogenic infection and also to correlate with time in hospital.9 To date no study has addressed the incidence of systemic clinical features of odontogenic infection at time of presentation as identied by the presence of sepsis syndrome. The incidence of sepsis in this patient group therefore remains unknown. Furthermore, no study has addressed any impact on management or length of stay in hospital for such patients. Observing and recording the clinical criteria for SIRS at the time of admission allows rapid diagnosis. Recognition of the severity of this condition enables appropriate treatment to be provided immediately and effectively, aiming to reduce morbidity and length of stay in hospital.10 This study investigates the prevalence of sepsis in patients presenting to the Southern General regional maxillofacial unit with infection in the head and neck region.

Patients and methods

Following a data-gathering exercise assessing levels of recording of SIRS criteria in case-notes, signicant shortfalls in data collection had been found. A training event was held, emphasising the signicance of these parameters and familiarising staff with the data collection form used in this study (Figure 3). Data were collected from the regional
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Superficial lobe of submandibular gland Figure 2 Potential initial pathways of spread of odontogenic infection within the facial tissues.

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maxillofacial unit in Glasgow prospectively over a six month period. The specially designed SIRS data sheet was completed by junior medical staff on the patients admission to hospital. All patients admitted to the Southern General Hospital with a conrmed focus of odontogenic infection by clinical and radiographic criteria, were included in this study. Data collection included the recording of SIRS parameters, the patients age, sex, site of infection, length of stay in hospital, referral source, time from admission to operation and any ICU admissions. Diagnosis of the odontogenic focus of infection was made using a combination of clinical, operative and radiographic ndings. These admission sheets were then reviewed for the denable SIRS criteria as shown in Table 2, in order to establish whether a diagnosis of sepsis could be made at initial presentation. We also assessed the difference in length of stay between those presenting with SIRS and those not.

Results
Sixty-seven patients were included in the study, with a total average age of 38.7 years (range 4-91). The ratio of males to females was 1:1. The mean age of the male patients was 37.2 years (range 4-71) and the mean age of the female patients was 40.3 years (range 13-91). The referral source is shown in Figure 4. The majority of these patients were from accident and emergency departments and the local dental hospital (GDH). The mean length of stay in hospital of patients was 4.0 days (range 1-17).

with patients without systemic sepsis whose average length of stay was 2.9 days (range 1-6). This achieved statistical signicance, (p=0.0145 Mann-Whitney U test). Patients with SIRS and a mandibular focus of infection had a longer hospital stay, 5.3 days, than those patients presenting with SIRS and a maxillary focus of infection of 3.0 days. This was also statistically signicant (p=0.0146 Mann-Whitney U test). The site of the infection was not a statistically signicant factor in the likelihood of having SIRS in this series (see Figures 5a and 5b). Mandibular dental sepsis was associated with a 63.8% SIRS rate while maxillary dental sepsis was associated with a rate of 55% (p=0.46, Chi-square test), indicating no statistical difference in the likelihood of developing SIRS dependent upon the site of the infective odontogenic focus. However, the average length of stay associated with mandibular infection was 4.6 days as compared to 2.6 days in association with maxillary infection. This was statistically signicant (p=0.00089, MannWhitney U test). Twenty-two (53.7%) of the 41 patients with a diagnosis of SIRS also had positive bacterial cultures.
2.13% 6.38% 6.38% 2.13% 4.26%

Submandibular Submasseteric Subligual Submental

78.72%

Parapharyngeal Buccal

31.34%

A&E GDH

41.79% 16.42%

Dentist

5%
GP Other

7.46% 2.99%

Buccal

30%
Canine Palatal

65%
Figure 4 Pie chart illustrating the various referral sources.

The clinical focus of infection was the maxillary dentition in 29.9% (n=20) of cases and the mandibular dentition in 70.1% (n=47) of cases. Sixty-four patients (95.5%) required incision and drainage as part of the management of their head and neck infection. Fifty-six (83.5%) of these patients had their operation on the same day as admission to hospital with the remaining eight (11.9%) being operated on the day following admission. Only three patients did not require an operation and were treated with intravenous antibiotics and supportive measures. Forty-one patients (61.2%) had sepsis diagnosed on their admission to hospital. The average length of stay for patients diagnosed with sepsis was 4.7 days (range 2-17), compared
JICS Volume 10, Number 1, January 2009

Figure 5a and 5b Proportions of fascial space involvement in mandibular and maxillary odontogenic infection.

Six of the sixty-seven patients in this study were admitted postoperatively to the ICU for the management of septic complications. All admissions involved airway patency considerations; of these, two cases had septic shock and another two developed single or multiple organ failure. All six of these patients presented with sepsis on admission with a mandibular primary focus. All underwent surgical
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intervention on the day of admission. Of the parameters required for the diagnosis of SIRS, ve cases did not have the white cell count recorded and one did not have the respiratory rate documented. This did not affect the results, as none of the other parameters were positive for SIRS in these patients.

Discussion
Odontogenic infection is extremely common and may result in signicant morbidity and mortality if not recognised and treated appropriately. Abscess formation and the spread of infection within the fascial neck spaces can lead to direct pressure on the upper airway (Figure 6). This can result in signicant compromise to airway patency with immediate threat to life. Odontogenic infection has also been reported to spread into adjacent and non-adjacent structures causing signicant morbidity and also mortality, including necrotising fasciitis.6-8,11-18

The sepsis syndrome is a clinical state where the host systemic response remains compensated in the face of infective insult. This clinical phase precedes sepsis-induced organ dysfunction and thus merits careful but aggressive resuscitative management. A large proportion of our patients with cervicofacial odontogenic infection need urgent intervention to avert sepsis progression. The patients referred to the unit may represent the more severe end of the odontogenic infection spectrum, but until this study we were unsure as to the severity of systemic upset in this group. It is clear that most of these patients are signicantly systemically unwell. In managing the septic patient the rst consideration is to attempt to identify and eliminate the source of infection. When indicated, surgical drainage and debridement should be performed promptly.9 Empirical antibiotics should be commenced as early as possible, be broad enough in spectrum to cover the likely infecting organisms, and be able to penetrate to the site of infection.10,19-21 Research has shown that the commencement of intravenous antibiotic therapy within the rst hour after the recognition of sepsis is vital to reduce the likelihood of complications.22 Thus early awareness and institution of appropriate management measures should optimise clinical outcomes; this is planned to be the subject of ongoing study. We have produced a stamp detailing the SIRS criteria, which can be used for future admissions in order to accurately record the diagnosis of SIRS (Figure 7). This step aims to introduce the concepts of SIRS and sepsis to routine practice and so facilitate prompt and appropriate intervention for this patient group.

Figure 6 CT scan of cervicofacial abscess illustrating airway deviation and compromise.

It was our aim to quantify the prevalence of SIRS in our patients presenting with odontogenic infection to the regional maxillofacial unit at the Southern General Hospital, Glasgow. Development of SIRS is the common rst step in the traumatised host to many forms of insult. In the case of a suspected infective cause, if an organism is isolated then the patient has, by denition, developed sepsis syndrome. Even in the absence of a cultured organism, a diagnosis of sepsis syndrome can be made if a clinical focus of infection is diagnosed. Only 53.7% of the patients with SIRS had positive cultures. This low percentage is most likely to be due to the immediate administration of intravenous antibiotic therapy on admission, producing negative bacterial cultures. Many patients also had commenced oral antimicrobial therapy prior to presentation.
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Figure 7 Stamp produced in order to help record SIRS criteria accurately within case record clinical entries.

Conclusions
The sepsis syndrome was present in at least 61.2.% of patients presenting over the study period with odontogenic infection to a regional maxillofacial unit. Clinical recording of SIRS parameters was incomplete in the case series reported. Adoption of assessment of SIRS parameters in the initial assessment of odontogenic infection patients presenting to the maxillofacial unit should become routine and may help guide intervention.
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Original articles

References
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15.Ogiso A, Tamura M, Minemura T et al. Mediastinitis caused by odontogenic infection associated with adult respiratory distress syndrome. Oral Surg Oral Med Oral Pathol 1992;74:15-18. 16.Reed JM, Anand VK. Odontogenic cervical necrotizing fasciitis with intrathoracic extension. Otolaryngol Head Neck Surg 1992;107:596-600. 17.Rubin MM, Cozzi GM. Fatal necrotizing mediastinitis as a complication of an odontogenic infection. J Oral Maxillofac Surg 1987;45:529-33. 18.Zeitoun IM, Dhanarajani PJ. Cervical cellulitis and mediastinitis caused by odontogenic infections: report of two cases and review of literature. J Oral Maxillofac Surg 1995;53:203-08. 19.Jimenez MF Marshall JC. Source control in the management of sepsis. , Intensive Care Med 2001;27 Suppl 1:S49-S62. 20.Ibrahim EH, Sherman G, Ward S et al. The inuence of inadequate antimicrobial treatment of bloodstream infections on patient outcomes in the ICU setting. Chest 2000;118:146-55. 21.Leibovici L, Shraga I, Drucker M et al. The benet of appropriate empirical antibiotic treatment in patients with bloodstream infection. J Intern Med 1998;244:379-86. 22.Weinstein MP Murphy JR, Reller LB et al. The clinical signicance , of positive blood cultures: a comprehensive analysis of 500 episodes of bacteremia and fungemia in adults. II. Clinical observations, with special reference to factors inuencing prognosis. Rev Infect Dis 1983;5:54-70.

Thomas PB Handley Trainee Doctor, Regional Maxillofacial Unit, Southern General Hospital, Glasgow Mark F Devlin Consultant, Maxillofacial/Cleft Surgeon,
Regional Maxillofacial Unit, Southern General Hospital, Glasgow

David A Koppel Consultant, Maxillofacial/Craniofacial Surgeon, Regional Maxillofacial Unit, Southern General Hospital, Glasgow James A McCaul Consultant, Maxillofacial/Head and Neck Surgeon, Bradford Teaching Hospitals NHS Foundation Trust jim.mccaul@btinternet.com
This work was carried out at the Regional Maxillofacial Unit of the Southern General Hospital, Glasgow.

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