epartment of Medicine, Mahatma Gandhi Institute of Medical Sciences, Sevagram, Dist. Wardha, 442102 Maharashtra, India
r t i c l e i n f o
rticle history:eceived 5 November 2009eceived in revised form 6 June 2010ccepted 9 June 2010vailable online xxx
eywords:eningitis
hysical examinationensitivity and specificityikelihood ratios
a b s t r a c t
Objectives: To evaluate accuracy of physical signs for detecting meningitis.Patients and methods: We enrolled patients aged 12 years or more, admitted with acute encephalitissyndrome (fever, headache, altered mental status, vomiting, seizures, neurodeficit) to a rural teachinghospital. The design was a double-blind, cross-sectional analysis of consecutive patients, independentlycomparing signs of meningeal inflammation (nuchal rigidity, head jolt accentuation of headache, Kernig’ssign and Brudzinski’s sign) elicited by internal medicine residents against an established reference stan-dard (cerebrospinal fluid white cell count >5 white cells/�L). Diagnostic accuracy was measured bycomputing sensitivity, specificity and likelihood ratios (LRs) and their 95% confidence interval (CI) values.Results: Of 190 patients (119 men, 71 women; ages 13–81 years; mean 38(SD 18) years) CSF analysisidentified meningitis in 99 (52%; 95% CI 44, 59%) patients. No physical sign of meningeal irritation could
accurately distinguish those with and without meningitis: nuchal rigidity (LR+ 1.33 (0.89, 1.98) and LR−0.86 (0.70, 1.06)), head jolt accentuation of headache (LR+ 5.52 (0.67, 44.9) and LR− 0.95(0.89, 1.00)),Kernig’s sign (LR+ 1.84 (0.77, 4.35) and LR− 0.93(0.84, 1.03)) and Brudzinski’s sign (LR+ 1.69 (0.65, 4.37)and LR− 0.95 (0.87, 1.04)).Conclusion: Physical signs of meningeal inflammation do not help clinicians rule in or rule out meningitisaccurately. Patients suspected to have meningitis should undergo a lumbar puncture regardless of the
ysica
presence or absence of ph
. Introduction
Meningitis is an important cause of morbidity and mortality,orldwide. Bacterial meningitis is among the 10 most common
nfectious causes of death and kills estimated 135,000 peoplehroughout the world each year [1]. It is estimated that about auarter of adults with bacterial meningitis [2,3], and a third of allatients with tuberculous meningitis die [4]. Another one-fourthf survivors develop transient or permanent neurologic morbidity2,3]. Early recognition of this serious infection in primary care set-ings is important; so as to initiate timely life saving treatmentsnd appropriate referrals. This in turn can reduce mortality andorbidity in meningitis.For over 100 years, clinicians have used three physical signs –
uchal rigidity, Kernig’s and Brudzinski’s signs – to help diagnose
Please cite this article in press as: Waghdhare S, et al. Accuracy of physicalstudy. Clin Neurol Neurosurg (2010), doi:10.1016/j.clineuro.2010.06.003
eningitis at bedside and to decide need for lumbar puncture,r more intensive care. Although Verghese and Gallemore [5]rgued that “the physical signs of meningeal irritation may aidn early diagnosis and treatment of meningitis and are excellent
demonstrations for medical students and house staff of the art ofthe bedside examination”, there is limited information about theaccuracy of these signs for detection of meningitis. A prospectivecross-sectional study [6] has concluded that physical signs do notaccurately discriminate between patients with and without menin-gitis (Kernig’s sign (sensitivity, 5%; likelihood ratio for a positive testresult (LR+), 0.97)), Brudzinski’s sign (sensitivity, 5%; LR+, 0.97), andnuchal rigidity (sensitivity, 30%; LR+, 0.94). Another study [7] thatevaluated 54 patients with fever and new headaches reported thatjolt accentuation of headache may be the best sign for meningitis(sensitivity, 97%; LR+, 2.4).
Despite poor accuracy, the physical signs of meningeal irrita-tion continue to be part of bedside clinical teaching and practice.In resource limited settings, cerebral malaria, tuberculous menin-gitis and bacterial meningitis are close differential diagnoses inpatients with fever and impaired mental status. In these settingsclinicians cannot always perform a lumbar puncture or lack accessto cerebrospinal fluid (CSF) microscopy. They, therefore, use clin-
signs for detecting meningitis: A hospital-based diagnostic accuracy
ical signs to distinguish meningitis from encephalopathy such ascerebral malaria. It is important for the clinicians to know if thesigns of meningeal irritation are accurate enough to obviate theneed for CSF examination. We carried out this study to find outthe diagnostic accuracy of four physical signs – nuchal rigidity, jolt
ccentuation of headache (hereafter called head jolt sign), Kernig’sign and Brudzinski’s sign – to detect meningitis among hospital-zed patients, 12 years of age or older, suspected to have meningitis
ith cerebrospinal fluid cell count as the reference standard.
. Subjects and methods
.1. Patients, setting and data collection
This study was performed at a 620 bed teaching hospital with00,000 patient visits and about 10,000 patient admissions to the
nternal medicine wards, each year. Typically about 200 patientsith fever, headache and altered mental status (clinically classified
s acute encephalitis syndrome or AES) seek care at this hospi-al every year [8]. These patients typically are usually tested for
alaria (microscopy and rapid diagnostic tests) and evaluated formetabolic encephalopathy (glucose, electrolytes and renal panel
ests). Patients testing negative for malaria and not found to havemetabolic encephalopathy undergo a lumbar puncture and CSFicroscopy to determine cause of AES. Treating physicians use on
dmission Glasgow coma score (GCS) to grade severity of disease,nd make a final diagnosis based on clinical profile, results of CSFased tests, clinical biochemistry, and neuro-imaging.
For a period of 1-year, beginning May 2008, we prospectivelynrolled all consecutive patients with AES (fever, headache, andltered mental status, with or without seizures or focal neurologicaleficit) in whom treating physicians had ordered CSF examination.lind to the diagnosis, physical findings and laboratory data, the
CU residents, who were aware of the study, used standardizedxamination techniques [1] to elicit the following physical signsn each patient before they underwent a lumbar puncture.
Physical sign Method ofelicitation
Positive test
Nuchal rigidity With the patient inthe supine position,the resident gentlyflexed the neck,asking the patientsto touch their chinto sternum
Resistance toflexion
Jolt accentuation ofthe patient’sheadache
The resident askedthe patients to turntheir headshorizontally at afrequency of 2–3rotations persecond
Worsening of thebase line headache
Kernig’s sign With the patient inthe supine position,the resident liftedthe knee in flexedposition untilmaximal hipflexion wasobtained. The legwas extended atthe knee andresistance waschecked
Resistance toextension at theknee to >135◦ orpain in the lowerback or posteriorthigh
Brudzinski’s sign With the patient inthe supineposition, theresident flexed theneck, and lookedfor flexion of boththe lower limbs
Flexion of theknees and hips
Please cite this article in press as: Waghdhare S, et al. Accuracy of physicalstudy. Clin Neurol Neurosurg (2010), doi:10.1016/j.clineuro.2010.06.003
ICU resident recorded the results of these tests on a speciallyesigned sheet. This sheet was folded, and sealed to ensure that
ndex tests were interpreted blinded to and independent of theeference standard. Before performing lumbar puncture the sealed
PRESSd Neurosurgery xxx (2010) xxx–xxx
recording-sheet was deposited in a box placed in the intensive careunit of the hospital.
Since lumbar punctures are often done in the middle of nightand cells in the CSF need to be counted within 30 min of a lum-bar puncture, a medicine resident (SW) underwent training to doCSF cell counting using a haemocytometer (Neubauer’s chamber).The methodology was pilot tested and cell counts performed bythe medical resident and an experienced microscopist were com-pared and shown to be reproducible in a set of 25 patients. It wasensured that time-interval between recording of physical signs,lumbar puncture, and CSF cell counting does not exceed 60 and30 min, respectively. The resident (SW) was blind to the historyand results of the physical examination until after the CSF countswere entered in data collection forms.
Meningitis was defined as >5 white blood cells/�L of CSF.Patients were excluded from the study if lumbar puncture was trau-matic (defined as either grossly bloody CSF, or if red blood cell countin CSF was >400 cells/�L). A differential count was also obtainedfrom the wet smear. Additional tests (CSF sugars, proteins, and bac-terial cultures) were performed in all samples as a standard of care.Further CSF tests (e.g. mycobacterial cultures, specific viral diag-nostics) were ordered based on discretion of the treating physician,cost, and availability.
The study protocol was approved by the institutional ethicscommittee, and consent was obtained from patients or their rela-tions to elicit physical signs and to do lumbar punctures.
2.2. Statistical analysis
We assessed the accuracy of physical signs in diagnosing menin-gitis by calculating sensitivity, specificity, positive and negativepredictive values and positive and negative likelihood ratios. Ina post hoc analysis we estimated diagnostic accuracy of physicalsigns by sub-classifying individuals with meningitis by [1] severityof meningeal inflammation: mild (CSF cells 6–100/�L), moderate(101–1000 cells/�L) and severe (>1000 cells/�L); [2] predominantcells in CSF: lymphocytes, neutrophils, and mixed, using 75% cellsas a cutpoint; [3] tertiles of Glasgow coma score and [4] dischargediagnosis of type of meningitis (aseptic, tuberculous or bacterial).We used diagti command in STATA (version 10, Stata Corp. CollegeRoad, TX, USA) to calculate point estimates of accuracy and their95% confidence intervals.
3. Results
We have used STARD (Standards for Reporting Diagnostic Accu-racy Study) guidelines to report this study. Figure shows the studyprofile. Between May 2008 and July 2009, we enrolled 204 patients.We could not use data from 14 patients because the lumbar punc-ture was traumatic. Thus, our final sample consisted of 190 patients(119 men, 71 women); ages 13–81 years [mean 38 (SD 18) years].CSF analysis identified meningitis in 99 of 190 (52%) patients. Thediagnosis based on clinical profile, cerebrospinal fluid findings, andneuro-imaging for these 99 patients was aseptic meningitis (n = 62(63%)), tuberculous meningitis (n = 30 (31%)) and bacterial menin-gitis (n = 7 (7%)). There were only seven patients with confirmedbacterial meningitis, and 13 with a predominantly neutrophilicleucocytosis. The final discharge diagnosis of those classified innon-meningitis group (n = 91) consisted of acute encephalitis ofundermined etiology, acute hepatic encephalopathy, metabolic
signs for detecting meningitis: A hospital-based diagnostic accuracy
Because of rounding, the sum of percentage may not be 100.Meningitis: defined as >5 WBCs/�L of cerebrospinal fluid.S sgowFM �L an
tctowpptwc
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rhadl
m((mwhh(w11o(csantat
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D, standard deviation; IQR, inter-quartile range; CSF, cerebrospinal fluid; GCS, Glaigures in parenthesis denote %, unless specified otherwise.eningeal inflammation: mild = 5–100 WBC/�L of CSF, moderate = 101–1000 WBC/
able is age, distribution of symptoms, physical signs and CSFhemistry in patients with meningitis, categorized according tohe severity of meningeal inflammation. All patients were febrilen admission. Compared to patients without meningitis, patientsith meningitis were more likely to report seizures (24% vs.16%;= 0.24) but were as likely to have altered sensorium (68% vs. 70%;= 0.80). Only 17 (17%) patients with meningitis had the classic
riad of fever, nuchal rigidity, and a change in mental status. Patientsith meningitis tended to have lower glucose and higher protein
ompared to those without.
.1. Accuracy of physical signs
All the four physical signs had a poor accuracy. While nuchaligidity was most sensitive (sensitivity of 39.4; 95% CI 29.7, 49.7%),ead jolt sign had highest specificity (98.9; 95% CI 94, 100%). Theccuracy estimates of Kernig’s and Brudzinski’s signs were interme-iate between these two extremes. None of the positive or negative
ikelihood ratios were statistically significant (Fig. 1).Of the 190 study patients, 33 (17.3%) had evidence of
ild meningeal inflammation (5–100 WBC/�L of CSF), 5026.3%) had evidence of moderate meningeal inflammation101–1000 WBC/�L) and 16 (8.4%) had evidence of severe
eningeal inflammation (>1000 WBC/�L). In a subset of patientsith severe meningeal inflammation, no patient had a positiveead jolt sign, Kernig’s sign or Brudzinski’s sign. Nuchal rigidityad a poor sensitivity (12.5%) and low positive likelihood ratio0.42) for diagnosis of severe inflammation. The +LRs for thoseith moderate meningeal inflammation ranged between 0 and
.69 while −LRs for severe inflammation ranged between 0.71 and
.42. The degree of meningeal inflammation did not influence theperating characteristics of the physical signs to detect meningitis.Table 2). We also stratified the test results according to types ofells in CSF and three tertiles of Glasgow coma scale (data nothown). In no subgroup did LRs swing significantly farther from 1nd provided little change in probability that a patient has or doesot have meningitis. Among patients classified according to theype of meningitis, except Kernig’s sign (LR+ 5.57, 95% CI, 1.83, 17)ll physical signs were associated with unhelpful likelihood ratioshat also lacked statistical significance (Table 3).
Please cite this article in press as: Waghdhare S, et al. Accuracy of physicalstudy. Clin Neurol Neurosurg (2010), doi:10.1016/j.clineuro.2010.06.003
. Discussion
The main finding of our study is that none of the physical signssed to assess meningeal inflammation are accurate enough toonfidently rule in or rule out meningitis in adult inpatients sus-
coma scale.
d severe = >1000 WBC/�L.
pected to have meningitis. These physical signs also perform poorlyregardless of the severity of meningeal inflammation, type of cellsin CSF, severity of disease, and type of meningitis.
Textbooks of medicine describe, and students routinely learnand elicit, physical signs to detect meningitis. Of these signs, nuchalrigidity and Kernig’s signs are almost universally elicited in allpatients suspected to have meningitis; Brudzinski’s sign and thejolt accentuation of headache sign have not become as popu-lar. In Brudzinski’s original description of 42 cases of meningitis(including 21 cases of tuberculous meningitis), Kernig’s sign hada sensitivity of 57%, while Brudzinski nape of the neck sign had asensitivity of 97% and the contralateral reflex sign had a sensitivityof 66% [5]. Interestingly, although Vladimir Kernig described thephysical sign in a German journal in 1884 that epitomizes him andJosef Brudzinski described the physical sign in a Polish journal in1909 that bears his name [5], clinicians accepted these signs on theirface value and made little attempt to evaluate their diagnostic accu-racy in well-designed cross-sectional studies. Thus generations ofmedical students have learnt these physical signs and hundreds ofthousands of patients had these signs performed on them, withoutfirm evidence on their accuracy.
Studies that have evaluated the accuracy of these signs areretrospective [3,9–16], have a small sample size [9–14,17], haveevaluated people aged 60 and older [9,10,17], have included onlypatients with bacterial meningitis [3,10–12,14,16] or very smallnumber of patients with tuberculous meningitis [7,17] or asep-tic meningitis [7,9,13] or have not stated the method of elicitationof physical signs [3,10–14,16]. Moreover, except two studies [6,7]no study has enrolled patients with and without meningitis, andtherefore specificity of the physical signs in other studies can-not be calculated. The pooled sensitivity of nuchal rigidity in ameta-analysis of 10 studies [18] (nine studies of retrospectivechart review) of 824 patients (845 episodes) was 70% (95% con-fidence interval, 58, 82%). By contrast, Thomas et al. [6] in theirwell-designed prospective diagnostic accuracy study reported thatnuchal rigidity (LR+ 0.94 and LR− 0.92) was too poor a physicalsign to rule in or rule out meningitis. Our estimates of diagnosticaccuracy of nuchal rigidity (LR+ 1.33 [0.89, 1.98] and LR− 0.86 [0.7,1.06]) are consistent with these observations. The prior probabil-ity of meningitis in our study was 52%; nuchal rigidity, if present,raised the probability of meningitis to 59%; a supple neck reduced
signs for detecting meningitis: A hospital-based diagnostic accuracy
the probability to 48%. Thus the presence or absence of nuchalrigidity did not result in clinically meaningful changes in post-testprobability of meningitis. Older people frequently suffer from cer-vical spondylosis which could result in nuchal rigidity despite theabsence of meningitis – 35% of the geriatric patients on acute-care
4 S. Waghdhare et al. / Clinical Neurology and Neurosurgery xxx (2010) xxx–xxx
cy of
aono
s–f
TD
Tm
Fig. 1. Study flow and diagnostic accura
nd rehabilitation wards had nuchal rigidity in one series [19]. Inur study only 25 (13%) patients were aged 60 and above; the diag-ostic accuracy of nuchal rigidity might have been much lower hadur study population been older.
Please cite this article in press as: Waghdhare S, et al. Accuracy of physicalstudy. Clin Neurol Neurosurg (2010), doi:10.1016/j.clineuro.2010.06.003
Previous studies have shown that Kernig’s sign and Brudzinski’signs occur infrequently among patients with suspected meningitisonly 5% each in 297 patients in a prospective cross-sectional study
rom America [6] and 9% of 54 patients in a study from Japan [7].
able 2iagnostic accuracy of physical signs in different categories of meningeal inflammation.
P, true positive; FN, false negative; FP, false positive; TN, true negative; LR+, posild = 5–100 WBC/�L of CSF, moderate = 101–1000 WBC/�L and severe = >1000 WBC/�L.
physical signs for detecting meningitis.
Our observations are almost similar: Kerning’s sign was positive in12% of 190 patients. The low sensitivity of Kernig’s sign indicatesthat most patients with meningitis could be missed if cliniciansuse it as a screening test to order a lumbar puncture. In line with
signs for detecting meningitis: A hospital-based diagnostic accuracy
a previous study [6], the specificity of these signs was close to 95%in our study. If very few patients test positive for a physical sign,despite high specificity, the positive predictive value of the signremains low – as shown by our study.
P, true positive; FN, false negative; FP, false positive; TN, true negative; LR +ild = 5–100 WBC/�L of CSF, moderate = 101–1000 WBC/�L and severe = > 1000 WB
Only one study [7] has tested the accuracy of accentuation ofeadaches by head jolt. In 1993 Uchihara and Tsukagoshi prospec-ively examined the clinical signs of 54 febrile patients with neweadaches. Jolt accentuation of headaches, a novel sign, had aensitivity of 97%, a specificity of 60%, a LR+ of 2.4 and LR− of. The authors argued that all febrile patients with recent-onseteadaches and jolt accentuation should undergo a lumbar punc-ure even in the absence of nuchal rigidity or Kernig’s sign and lackf accentuation of headache on physical examination may essen-ially exclude meningitis (LR−, 0). Noteworthy, this study samplednly 54 relatively young patients (mean age, 39 years) at a timenteroviral meningitis was prevalent in Japan. The low frequencyf this sign in our study (7 of 190 patients) and poor likelihoodatios that the sign yielded indicate that clinicians cannot rely onhis sign to confirm or exclude meningitis.
We also wondered if severity of meningeal inflammation couldnfluence the frequency of positive physical signs. We used CSFell count to categorize meningeal inflammation – mild, moderatend severe. Contrary to our assumption that patients with severelynflamed meninges would have a higher frequency of the physicaligns, our study data did not support our assumption. The diag-ostic accuracy of all physical signs was poor regardless of theeverity of meningeal inflammation. In fact, no patient with severeeningeal inflammation had a positive head jolt sign, Kernig’s sign
r Brudzinski’s sign. Our results are in line with those reportedy Thomas et al. [6] who also found that the diagnostic accuracyf Kernig’s sign and Brudzinski’s sign was poor for patients withoderate and severe meningeal inflammation. We also found that
mong subgroups classified by type of cellular response, severity ofisease, and type of meningitis, the diagnostic accuracy of physicaligns was too low to make large and clinically meaningfully shiftsetween pretest and post-test probability.
When clinicians suspect meningitis, they use physical signs ofeningeal inflammation not to rule in but to rule out menin-
itis. These signs generate likelihood ratios which can be usedo refine clinical diagnosis. A physical sign with LR− close to 0ould almost rule out meningitis and assure clinicians that theyould not be missing meningitis by not ordering a lumbar punc-
ure. By contrast, physical signs with LR− close to unity wouldardly reduce the probability of meningitis. In our study, among a
Please cite this article in press as: Waghdhare S, et al. Accuracy of physicalstudy. Clin Neurol Neurosurg (2010), doi:10.1016/j.clineuro.2010.06.003
ubgroup of patients with meningitis and mild meningeal inflam-ation (Table 2), 21 of 33 patients with meningitis (64%) did not
ave nuchal rigidity, as did 64 of 91 patients without meningi-is (70%). The LR− for nuchal rigidity (64%/70% = 0.90) suggestshat absence of nuchal rigidity among patients suspected to have
meningitis cannot exclude meningitis because it is almost as likelyin someone who has meningitis than in a patient without menin-gitis. Other signs of meningeal inflammation also yielded LRs notsmall enough to rule out meningitis with confidence.
Our study has several strengths. We did a prospectivecross-sectional study in which the results of physical signs onconsecutively recruited groups of patients were cross-classifiedagainst meningitis status determined by the reference standard(CSF microscopy). Both the index tests and the reference standardwere performed in a blind and independent manner on the samegroup of patients. Our spectrum of patients includes patients withmild, moderate and severe meningeal inflammation and disorderswith which meningitis is usually confused at bedside. Because ourstudy was prospective, our test results were not influenced by theknowledge of laboratory tests. We standardized the elicitation andinterpretation of physical signs. Also, we excluded patients withtraumatic lumbar punctures.
We acknowledge that our study has several limitations. Weenrolled hospitalized patients aged 12 and older, and thereforeour study results cannot be generalized to community settings andto children. Second, the prevalence of bacterial meningitis in ourstudy was only 3.6%, thus our results may not be generalizable tothose settings with a higher prevalence of bacterial or tuberculousmeningitis. Third, although we enrolled 190 patients in the study,95% confidence intervals around the point estimates are not tight,indicating that the sample size was small. Finally, this study doesnot address the issue of reproducibility.
In conclusion, none of the physical signs used to assessmeningeal inflammation are accurate enough to confidently rulein or rule out meningitis in adult inpatients suspected to havemeningitis. These physical signs also perform poorly regardless ofthe severity of meningeal inflammation. Their presence or absencedoes not lead to large and conclusive change from pretest topost-test probability of meningitis. Clinicians should not trustphysical signs to assess the need for performance of lumbar punc-ture. Patients with suspected meningitis must undergo a lumbarpuncture regardless of presence or absence of physical signs ofmeningeal irritation.
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