Oriainal Contributions Maxillary Sinusitis in the Surgical Intensive Care Unit: A Study Using Bedside Sinus Ultrasound Krista L. Kaups, MD, Stephen M. Cohn, MD, Benny Nageris, MD, and William G. Lavelle, MD Purpose: This study investigates the incidence of acute maxillary sinusitis (AMS) in the surgical intensive care unit (SICU). Methods: One hundred consecutive patients admitted to the SICU were examined in a prospective observational mode. Bedside sinus ultrasound (SUS) was performed on admission and every 48 hours. Patients with sinus fluid by SUS and unexplained sepsis underwent confirmatory sinus aspiration. Results: The development of fluid in the maxillary sinus was identified in 15 patients by SUS. Acute maxillary sinus occurred in only 1 (1%). Conclusion: This study shows SUS to be a simple, efficient method for determining the presence of maxillary sinus fluid in the SICU. Acute maxillary sinus was an unusual finding. Our policy of avoidance of nasal instrumentation may have contributed to the low incidence of AMS in this high-risk patient population. Copyright 0 1995 by W.B. Saunders Company
Paranasal sinusitis may represent as many as 5% of all infections in the surgical intensive care unit (SICU).’ The maxillary sinuses, in particular, can act as a source of occult sepsis in the SICU1-” and acute maxillary sinusitis (AMS) is a common finding in nasotracheally intubated patients (83%).6 It is often difficult to establish the diagnosis of AMS because of the absence of clinical findings in the SICU population and the inaccuracy of radiological tests.7 However, early identification of AMS is crucial if catastrophic infectious complications are to be avoided.3*6*g We postulated that AMS was not being recognized in our SICU patients and sought to verify the diagnosis using frequent bedside sinus ultrasound studies (SUS). Our goal was (1) to determine the ability of the SUS to deFrom the Departments of Surgery and Otolaryngology, University of Massachusetts Medical Center, Worcester, MA. Address reprint requests to Benny Nageris, MD, Division of Otolaryngology-Head and Neck Surgery, 55 Lake Ave N, Worcester, MA 01655. Copyright 0 1995 by W.B. Saunders Company 0196-0709/95/l 601-0004$5.00/O 24
American
Journal
of Otolaryngology,
tect AMS in the critical care setting; and (2) to ascertain the incidence of AMS in our seriously ill patients. Surprisingly, we found that maxillary sinus fluid was an unusual finding among our patients and that AMS was quite rare. MATERIALS
AND METHODS
One hundred consecutive patients admitted to the SICU at the University of Massachusetts Medical Center (UMMC) were prospectively evaluated by bedside SUS for the development of AMS during a s-month period. Each patient was assessed by SUS within 24 hours of SICU admission and every 48 hours thereafter until the patient was transferred from the SICU, completed a PI-day period of evaluation, or died. All SUS were performed by the principal investigators (Kaups and Cohn). Ultrasound equipment (Echosine 1000; American Electromedics, Hudson, NH) was factory calibrated at the onset of the study. A-mode (amplitude-mode) ultrasound was thought to provide evidence of maxillary sinus fluid if a peak was visualized 33 cm from baseline on a strip recorder. A fresh cadaver was used to confirm our ability to identify sinus fluid. The maxillary sinuses were aspirated dry; the fluid al-
Vol 16, No 1 (January-February),
1995: pp 24-28
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SINUSITIS IN THE SICU
iquots of 5, 15, and 20 mL were infused into the sinus; and the fluid wave was assessed by SUS. Reproducible SUS showed the presence of maxillary sinus fluid. The diagnosis of AMS was defined as unexplained clinical sepsis, SUS evidence of fluid in the maxillary sinus, and confirmatory antral puncture.‘-’ Drainage of the maxillary antrum was performed by a member of the Department of Otolaryngology and was considered positive if there were 225 white blood cells/high-power field and cultures grew a predominant organism. Demographic data were recorded, including age, gender, and the presence and duration of nasotracheal or orotracheal tubes and gastric tubes. Glasgow Coma Score and Acute Physiology and Chronic Health Evaluation II (APACHE II) were calculated. SICU days and ventilator days were recorded for the duration of the study. Deaths were included if they occurred during the 21 days of evaluation. The presence of skull or facial fractures after multiple trauma and corticosteroid use were noted. Orotracheal and nasotracheal tubes were most often placed before admission to the SICU, either in the emergency room or at the time of operation. Decisions regarding extubation and the site and method of tube placement were made independently by the SICU team. Computed tomography (CT) scans of the head were performed at the discretion of the SICU service. Those obtained during the SICU stay were reviewed retrospectively for evidence of maxillary sinus fluid or mucosal thickening. Statistical analysis was performed on an AST 286 computer using a software package (CSS; Statsoft, Tulsa, OK). Data were analyzed by simple t-tests (two-tailed] and the Fisher Exact test in the appropriate cases. For all statistical comparisons, the null hypothesis was rejected for P < .05.
RESULTS One hundred SICU patients were evaluated; 71 were men and 29 were women with a mean age of 45.4 years (range, 18 to 90 years). The majority of patients (N = 54) sustained multiple trauma, with associated skull fractures in 10 and facial fractures in 16. The remainder of patients were admitted to the SICU for postoperative care. Twenty-four patients received corticosteroids. Fifteen patients developed fluid within the maxillary sinus as determined by SUS (group I), whereas 85 patients did not show SUS evidence of maxillary sinus fluid accumulation (group II). The age (I, 53 -t 6; II, 45 f 2), APACHE II score (I, 17 ? 2; II, 14 + l), and Glasgow Coma Scale (GCS) (I, 10 f 1; II, 12 + 1) were not statistically different between
groups. The group that developed maxillary sinus fluid had significantly longer SICU stays (I, 13 + 2 v II, 7 + 1 days) and duration of ventilatory support (I, 11 2 2 v II, 5 + 1 days) when compared with those without sinus fluid (P = .OO2 in both instances) (Table 1). Ninety patients required mechanical ventilation, of whom 18 were nasotracheally intubated (3 in group I and 15 in group 11). The majority of these patients had nasotracheal tubes changed to orotracheal tubes. In the 3 patients nasotracheally intubated in patients with SUS evidence of sinus fluid, the length of nasotracheal intubation was no more than 2 days. In the 15 patients without sinus fluid on SUS, the length of nasotracheal intubation ranged from 1 to 14 days, with an average of 5.3 days. Only four of nasotracheal tubes remained in place longer than 3 days (14,12,10, and 7 days). There were no statistically significant differences between groups in regards to the presence of facial fractures, multiple trauma, the use of steroids, or the use of nasogastric or nasotracheal tubes. Sixty-one patients had a head CT performed during their SICU stay. Thirty-three CT studies were negative and 11 showed mucosal thickening only. Seventeen patients had CT air-fluid levels, 8 of which were visualized on the admission CT exam in patients with maxillary or orbital fractures. In the remaining 9 patients, sinus fluid was detected by head CT but not by SUS. Three of the collections were present on the admission CT, and none of the 9 patients had clinical sepsis without a clearly documented source (eg, pneumonia or intraabdominal abscess). Only 1 patient met our criteria for maxillary TABLE 1.
Demographics
Patients Age WI Apache II Glasgow coma score SICU stay (d) Days on ventilator
Group I
Group II
15 53 k 6 17 2 2 10 +- 1 l3k2 11 a2
85 45 + 2 1421 122 1 721 5*1
NS NS NS P = ,002 P = .002
Group I consists of patients with fluid on SUS. Group II consists of patients with no fluid on SUS. Data are the means 2 SE. Abbreviation: NS, not significant.
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sinusitis. This patient had sustained multiple trauma and had prolonged nasotracheal intubation. Antral puncture yielded purulent drainage that grew a Staphylococcus aureus, which was resistant to the existing antibiotic regimen.
The principal findings of our study included (1) that AMS was an unusual finding in our SICU, occurring in only 1 of the 100 patients studied; and (2) that bedside SUS was easily performed in the assessment of the presence of maxillary sinus fluid. The first description of AMS in the SICU (a complicaton of nasotracheal intubation) was reported in 1974. lo Numerous subsequent case reports support the view that the critically ill comprise a high-risk group for the development of AMS.11-16 Facial and head trauma can lead to the accumulation of blood and debris in the sinuses, can disrupt the mucosa, and can provide a favorable medium for the proliferation of bacteria.l Corticosteroids, by suppressing immune function in already compromised hosts, and broad-spectrum antibiotics, by allowing colonization of the airway with resistant bacteria, make the SICU population more susceptible to sinus infection.2 Nasotracheal tubes may contribute to the development of AMS in these patients by increasing mucosal edema or acting as a mechanical barrier to the normal drainage of the sinus ostia.1’3’5*g A review of sinusitis in steroid-treated head injured patients at Boston City Hospital by Grindlinger et al5 showed that nasotracheal intubation significantly increased the likelihood of developing paranasal sinusitis identified by air fluid levels on CT scan, with confirmatory sinus aspiration. Subsequently, Guerin et al” showed in 30 nasotracheally intubated patients mechanically ventilated for more than 6 days that 83% had CT scan evidence of sinusitis with positive antral cultures. Establishing the diagnosis of maxillary sinusitis is crucial in SICU because failure to identify this source of sepsis can lead to bacteremia,g’10 meningitis,5 subdural empyema,7 brain abscess, and osteomyelitis of the skull, or cavernous sinus thrombosis.18 The verifi-
KAUPS ET AL
cation of AMS in the critically ill is quite difficult because of limitations in the accuracy of clinical examination, radiographs, and culture data. The obtund or intubated SICU patient cannot complain of facial pain. The physical exam findings of tenderness or purulent nasal drainage, which herald the diagnosis of AMS in the ambulatory setting, are not frequently present. Furthermore, the diagnostic criteria for AMS are not well-defined. Some investigators report AMS in patients without clinical evidence of infection,lg whereas others use the presence of clinical sepsis with mucopurulent nasal discharge or radiological tests, but do not require confirmatory sinus tap.8’gg20 We rigorously defined AMS as radiological evidence of AMS (SUS demonstration of maxillary sinus fluid) and a positive antral tap in patients without other explanation for clinical sepsis. Antral trap represents the gold standard for diagnosis of AMS in the patient with clinical signs of infection. Cultures of nasal discharge correlate poorly with antral taps because the nasopharynx is contaminated, but the maxillary sinuses of both nonhuman primates21 and humans22 are sterile. Mucociliary action of the mucosa and drainage may keep the sinuses clean. Maxillary sinusitis occurring in the the outpatient setting is most commonly the result of infection with Streptococcus pneumoniae, Hemophilus influenzae, anaerobes, and viruses.23 Polymicrobial infection with Staphylococcus aureus and gramnegative organisms predominate in the SICU setting.1-6*g Most SICU patients receive broadspectrum antibiotics, which may lead to the overgrowth of resistant organisms. In the single patient meeting our criteria for AMS, a resistant S. aureus was cultured. The diagnosis of AMS by conventional multiview plain sinus radiographs, even in the ambulatory setting, is highly inaccurate.7*24*25 In the critically ill patient, the diagnostic capability of plain radiographs is further impeded by the use of portable equipment and difficulties in placing patients in the upright position. In addition, nasogastric and nasotracheal tubes, which may contribute to the development of sinusitis, also interfere with x-ray resolution. CT scan is helpful, but requires hazardous transport of septic patients
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SINUSITIS IN THE SICU
and is costly. a*‘*‘6 Furthermore, the CT scan is unable to distinguish between blood and other fluids, an important problem in the patient with facial trauma. SUS may offer a reliable, low-cost and noninvasive means of diagnosing maxillary sinus fluid in the SICU setting. SUS has been shown by other investigators to be highly accurate in large studies, confirming the diagnosis of AMS with antral tap in both ambulatory adults27-30 and children.31 This is the first study to evaluate the value of the SUS in the SICU setting. There are a number of potential criticisms of this study; the foremost is that only 1 patient had an antral puncture performed. Ideally, all patients should have undergone a sinus tap, but performing such an invasive procedure on the entire series of patients was felt to carry excessive risk. Our criteria for sinus tap included the absence of concurrent infection; therefore, AMS may have been missed in a patient with an established septic source. In addition, we may have underestimated the incidence of AMS if patients developed sinusitis beyond the study period (21 days) or after SICU discharge. The lack of correlation in our study between sinus fluid seen on SUS and CT scan is disturbing. One study showed that, after 8 days, essentially all nasotracheally intubated patients had maxillary sinus mucosal thickening on CT scan in the absence of clinical infection.” Our protocol was designed to minimize false-positive SUS findings (underdiagnose maxillary sinus fluid), because we hypothesized that abnormal findings would be quite frequently found. We chose 33 cm as criteria on A-mode SUS to maximize specificity. We feel that the head CT is probably more sensitive in identifying sinus fluid than the SUS (and definitely more expensive and timeconsuming), but may detect abnormalities that have little clinical significance. Finally, how do we explain our low rate of maxillary sinusitis? It has been the policy of our SICU to change nasotracheal tubes to orotracheal tubes within 24 to 48 hours of patient admission when safety permits. We feel that the practice of avoidance of prolonged nasal intubation is important in the low incidence of AMS in our critically ill patients. Despite reports emphasizing the prevalence
of sinusitis as a cause of sepsis in the SICU environment, we found that AMS was rare in 100 high-risk patients. Sinus ultrasound proved to be an efficient, reliable, and reproducible means of identifying maxillary sinus fluid in the SICU setting. Avoidance of the use of nasotracheal tubes and early replacement with orotracheal tubes may have contributed to the low incidence of AMS in this study. REFERENCES 1. Caplan ES, Hoyt NJ: Nosocomial sinusitis. JAMA 247:639-641, 1982 2. Bell RM, Page GV, Bynce RP, et al: Post-traumatic sinusitis. J Trauma 28:923-930, 1988 3. Michelson A, Schuster B, Kamp HD: Paranasal sinusitis associated with nasotracheal and orotracheal long-term intubation. Arch Otolaryngol Head Neck Surg 118:937-939, 1992 4. Linden BE, Anguilar EA, Allen SJ: Sinusitis in the nasotracheally intubated patient. Arch Otolaryngol Head Neck Surg 114:860-861, 1988 5. Grindlinger GA, Niehoff J, Hughes L, et al: Acute paranasal sinusitis related to nasotracheal intubation of head-injured patients. Crit Care Med 15:214-217, 1987 6. Guerin JM, Meyer P, Habib Y, et al: Purulent rhinosinusitis is also a cause of sepsis in critically ill patients. Chest 93:893-894, 1988 7. Chidekel N, Jensen G, Axelsson A, et al: Diagnosis of fluid in the maxillary sinus. Acta Radiolog Diagnosis 10: 433-440, 1970 8. Deutschman CS, Wilton PB, Sinow J, et al: Paranasal sinusitis associated with nasotracheal intubation: A frequently unrecognized and treatable source of sepsis. Crit Care Med 14:111-114, 1986 9. O’Reilly MJ, Reddick EJ, Black W, et al: Sepsis from sinusitis in nasotracheally intubated patients: A diagnostic dilemma. Am J Surg i47:601-604;1984 10. Kulber DA. Santora TA. Shabot MM. et al: Earlv diagnosis and treatment of sinusitis in critically ill trauma patient. Am Surg 57:775-779, 1991 11. Arens JF, Lejeune FE, Webre DR: Maxillary sinusitis, a complication of nasotracheal intubation. Anesthesiology 40:415-416, 1974 12. Gallagher TJ, Civetta JM: Acute maxillary sinusitis complicating nasotracheal intubation. A case report. Anesth Analg 55:885-886, 1976 13. Knodel AR, Beekman JF: Unexplained fevers in patients with nasotracheal intubation. JAMA 248:868-870, 1982 14. Pope TL, Stelling CB, Leitner YB: Maxillary sinusitis after nasotracheal intubation. South Med J 24:610612,1981 15. Aebert H, Hunefeld G, Regel G: Paranasal sinusitis and sepsis in ICU patients with nasotracheal intubation. Intensive Care Med 15:27-30, 1988 16. Willatts SM, Cochrane DF: Paranasal sinusitis: A complication of nasotracheal intubation. Br J Anaesth 57: 1026-1028,1985 17. Kaufman DM, Litman N, Miller MI-I: Sinusitis: Induced subdural empyema. Neurology 33:123-132, 1983 18. Kaplan RJ: Neurological complications of infections of the head and neck. Otolaryngol Clin North Am 9:729-749, 1976
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19. Fassoulakl A, Pamouktsoglou P: Prolonged nasotracheal intubation and its association with inflammation of paranasal sinuses. Anesth Analg 6950-52, 1989 20. Hansen M, Pouisen MR, Bendixen DK, et al: Incidence of sinusitis in patients with nasotracheal intubation. Br J Anaesth 61231-232, 1988 21. Shapiro ED, Wald ER, Doyle W, et al: Bacteriology of the maxillary sinus of Rheusus monkeys. Ann Otol Rhino Laryngol91:150-151, 1982 22. Evans FO, Sydnor JB, Moore WE, et al: Sinusitis of the maxillary antrum. N Engl J Med 293:735-739,197s 23. Hamory BH, Sande MA, Sydnor A, et al: Etiology and antimicrobial therapy of acute maxillary sinusitis. J Infect Dis 139:197-202, 1979 24. Vuorinen P, Kauppila A, Pulkkinen K: Comparison of result of roentgen examination and puncture and irrigation of the maxillary sinuses. J Laryngol 76:359-363, 1962 25. Axelsson A, Brebelius N, Chidekel N, et al: The
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correlation between the radiologica1 examination and the irrigation findings in maxillary sinusitis. Acta Otolaryngo1 (Stockh) 63:302-306,197O 26. Kronberg FG, Goodwin WJ: Sinusitis in intensive care unit patients. Laryngoscope 95:936-938, 1985 27. Mann W, Beck C, Apostolidis T: Liability of ultrasound in maxillary sinus disease. Arch Otol Rhino1 Laryngol 215:67-74, 1977 28. Landman MD: Ultrasound screening for sinus disease. Otolaryngol Head Neck Surg 94:157-169, 1986 29. Rohr AS, Spector SL, Siegel SC, et al: Correlation between A-mode ultrasound and radiography in the diagnosis of maxillary sinusitis. I Allergy Clin Immunol 78: 58-61,1986 39. Edell SL, Isaacson S: A-mode ultrasound evaluation of the maxillarv sinus. Otoiarvnnol Clin North Am 11:531-540,197s 31. Revonta M: A-mode ultrasound of maxillary sinusitis in children. Lancet 320-322, 1979 <
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