AJR InPractice
HOME HELP FEEDBACK SUBSCRIPTIONS ARCHIVE SEARCH TABLE OF CONTENTS
 QUICK SEARCH:   [advanced]


     


This Article
Right arrow Abstract Freely available
Right arrow Figures Only
Right arrow Full Text (PDF)
Right arrow Alert me when this article is cited
Right arrow Alert me if a correction is posted
Right arrow Citation Map
Services
Right arrow Email this article to a friend
Right arrow Similar articles in this journal
Right arrow Similar articles in PubMed
Right arrow Alert me to new issues of the journal
Right arrow Download to citation manager
Right arrow reprints & permissions
Citing Articles
Right arrow Citing Articles via HighWire
Right arrow Citing Articles via Google Scholar
Google Scholar
Right arrow Articles by Johnson, P. T.
Right arrow Articles by Fishman, E. K.
Right arrow Search for Related Content
PubMed
Right arrow PubMed Citation
Right arrow Articles by Johnson, P. T.
Right arrow Articles by Fishman, E. K.
Social Bookmarking
 Add to CiteULike   Add to Complore   Add to Connotea   Add to Del.icio.us   Add to Digg   Add to Reddit   Add to Technorati  
What's this?
Hotlight (NEW!)
Right arrow
What's Hotlight?
DOI:10.2214/AJR.07.2620
AJR 2008; 190:743-747
© American Roentgen Ray Society


Original Research

64-MDCT Angiography of the Coronary Arteries: Nationwide Survey of Patient Preparation Practice

Pamela T. Johnson1, John Eng, Harpreet K. Pannu and Elliot K. Fishman

1 All authors: The Russell H. Morgan Department of Radiology and Radiological Science, Johns Hopkins School of Medicine, 601 N Caroline St., Rm. 3251, Baltimore, MD 21287.

Received May 24, 2007; accepted after revision September 24, 2007.

 
Address correspondence to E. K. Fishman (efishman{at}jhmi.edu).


Abstract
Top
Abstract
Introduction
Materials and Methods
Results
Discussion
References
 
OBJECTIVE. The purpose of this study was to evaluate the current practice of patient preparation for 64-MDCT angiography (CTA) of the coronary arteries.

MATERIALS AND METHODS. Sites in the United States that perform 64-MDCT coronary angiography were surveyed by mail in 2006. Information requested included physician specialty; experience level; details about patient preparation, including the use, dose, route, and timing of premedication; and acceptable heart rate and rhythm. A total of 142 surveys were analyzed, with comparison of parameters across specialties (radiology, cardiology, or shared) and experience levels.

RESULTS. All facets of the study (premedication, data acquisition, cardiac interpretation) are performed exclusively by radiologists in 49% of sites and by cardiologists in 14%. All sites administer β-blockers. Target heart rate was reported as ≤ 65 beats per minute (bpm) by 89% of responders. Despite most centers aiming for a heart rate of ≤ 65 bpm, the maximum allowable heart rate is > 65 bpm in 80% of centers. Patients with arrhythmia are scanned in at least 25% of sites. Most sites (84%) administer nitroglycerin. Significant differences between specialties were noted for experience levels, timing and route of β-blocker administration, and for target heart rate. The likelihood of scanning in the setting of arrhythmia and β-blocker timing correlated with experience levels.

CONCLUSION. These 64-MDCT coronary artery data from 2006 reveal consensus for a range of patient preparation parameters. Use of β-blockers and nitroglycerin is routine, and the target heart rate is usually ≤ 65 bpm. However, differences were noted for β-blocker protocols and acceptable heart rate and rhythm, and some differences in practice are associated with experience level and specialty.

Keywords: coronary artery • CT • CT angiography • practice • questionnaire


Introduction
Top
Abstract
Introduction
Materials and Methods
Results
Discussion
References
 
Earlier generation MDCT scanners provided the foundation for coronary artery MDCT angiography (CTA), but implementation of 64-MDCT technology has bolstered its usefulness as a reliable diagnostic tool. The improved temporal and spatial resolutions are instrumental in producing high-quality data sets during peak arterial perfusion and enhancement. Early investigations confirm high diagnostic efficacy for coronary artery disease. Reported sensitivities range from 85% to 99%, specificities between 94% and 95% [19], and per-lesion positive and negative predictive values between 78–89% and 94–99%, respectively [24, 6, 7].

Unlike other new CT angiography applications made possible by advances in technology during the past decade, coronary artery imaging with MDCT is far more complicated than simply modifying the acquisition parameters and IV contrast infusion protocols for a new anatomic region. Compounding variables include the requirement for a controlled heart rate, a regular heart rhythm, and carefully timed arterial enhancement during maximal arterial perfusion and minimal cardiac motion. After data acquisition, multiple reconstructions may be necessary to optimize the evaluation of each coronary region for interpretation using a range of display and rendering techniques. Because of the numerous factors playing a role in these challenging studies, we sought to assess current practice characteristics for each component of the examination through a nationwide survey.


Materials and Methods
Top
Abstract
Introduction
Materials and Methods
Results
Discussion
References
 
This investigation was deemed exempt by the institutional review board of our institution. A two-page survey was designed to anonymously collect data about all facets of 64-MDCT of the coronary arteries from centers conducting the examination. This article presents the information collected with respect to patient preparation, physician specialty, and departmental experience levels (Fig. 1). The remainder of the data will be reported in a separate article. Sites potentially performing these exam inations were identified through the companies distributing 64-MDCT scanners in May 2006. Two of the three companies agreed to participate; the third declined. The survey and cover letter were mailed by the U.S. Postal Service to 563 sites in June and July of 2006, with a second mailing between August and October of 2006. To increase parti cipation, each respondent was offered a $25 gift card.


Figure 1
View larger version (23K):
[in this window]
[in a new window]
[as a PowerPoint slide]
 
Fig. 1 Diagram of survey mailed nationwide to centers potentially performing 64-MDCT of coronary arteries, highlighting portions of questionnaire analyzed in this study. Illustration by Frank Corl.

 
The survey included a section on experience level according to total number of studies performed, number of studies conducted per week, and length of time that the site has been performing 64-MDCT of the coronary arteries (Fig. 1). Experience level was defined as low (< 100 studies to date), moderate (100–500 studies total), or high (> 500 studies total or 25–50 studies per week and at least 6 months of experience). The protocol for β-blocker administration (route, dose, and timing); use of nitroglycerin, calcium channel blockers, or other medications; target heart rate sought with medication administration; and the maximum allowable heart rate were queried, in addition to the department's policy on scanning patients with arrhythmias. Multiple variables were analyzed with respect to physician specialty (cardiology, radiology, or shared) and site experience level.

Potential relationships between survey variables were evaluated using the Fisher's exact test from two-way cross-tabulations of the data. A p value of less than 0.05 was considered statistically significant.


Results
Top
Abstract
Introduction
Materials and Methods
Results
Discussion
References
 
Seven departments responded indicating that they were not currently performing coronary MDCT, and 36 surveys were returned because of insufficient address. A total of 149 surveys were submitted; however, five were determined to be second submissions from the same center and two pertained to 40-MDCT, leaving 142 surveys available for evaluation. Accordingly, the response rate was 27% (142/520). For each of the following, the denominator represents the number of respondents who completed the section.

Of the sites responding, all roles (premedication, data acquisition, and study interpretation) are performed exclusively by radiologists in 49% (66/134) and cardiologists in 14% (19/134) of sites. The remainder of the centers apportioned facets of the study as shown in Table 1. Medications are administered exclusively by radiologists in 56% (79/140), exclusively by cardiologists in 24% (33/140), and medication administration is shared by both specialties in 19% (27/140) of sites. One center has the referring physician perform premedication.


View this table:
[in this window]
[in a new window]

 
TABLE 1: Apportioning Roles in 64-MDCT Coronary Angiography in 134 Sites Reporting This Information

 

Most sites had low (44%, 59/135) or moderate (41%, 55/135) levels of experience, with a high experience level reported by 16% (21/135). Of the 20 high-experience sites indicating specialty, 55% (11/20) are cardiology sites and 30% (6/20) are radiology sites. The relationship between site specialty and experience level was statistically significant (p < 0.001) (Table 2).


View this table:
[in this window]
[in a new window]

 
TABLE 2: Experience Level by Site Specialty in 128 Sites Providing This Information

 

Beta-blockers are used by all sites for heart rate control. Respondents provided varying degrees of detail in describing the dose and timing. Among the 119 oral β-blocker protocols described, most sites simply reported dose and timing. However, a number detailed some degree of dependence on heart rate (13%, 15/119), weight (2%, 2/119), or both (1%, 1/119). Additional evidence that patient variables affect dose include the incremental administration of subsequent doses over time performed by 4% (5/119) and a range of doses provided by 20% (24/119) of sites. The route of administration, reported by 139 sites, is most commonly oral supplemented by IV (53%, 73/139). Again, respondents provided a range of detail. Slightly more than half (53%, 39/73) specifically described that IV β-blocker use after oral medication was heart rate–dependent, and the remainder either listed the dose (+/– timing of administration) (23/73) or provided no IV dose or timing details (11/73). Oral β-blockers only are used by 36% (50/139); and the least common practice is to administer IV only (12%, 16/139), with five of these sites reporting that the medication was administered only as needed.

Analysis according to specialty revealed that cardiologists are more likely than radiologists to supplement oral β-blockers with IV. Of the centers using oral β-blockers, IV β-blockers are potentially administered by 87% (27/31) of cardiologists, 41% (28/69) of radiologists, and 85% (17/20) of sites where medication administration is shared. However, no participating site where cardiologists exclusively administer medication uses IV β-blockers only. A statistically significant difference (p < 0.001) was identified for route of β-blocker administration when correlated with specialty (radiology, cardiology, or shared). Significant differences across experience levels were not identified (p = 0.07).

Of the 115 sites that indicated timing for oral β-blocker administration, 68% (78/115) give the first dose on the day of the examination, most commonly 1 hour before CT (77%, 60/78). The initial dose is administered either the day or the evening before the examination by 32% (37/115). Cardiologists and sites with high experience levels were more likely to begin premedication on the day before CT. Differences were statistically significant across specialty (p < 0.001) and experience levels (p = 0.006).

Table 3 shows the range of target heart rates using best-fit categories; 89% of sites (126/141) aim for a heart rate ≤ 65 bpm, with a median value of 60 bpm (n = 53). Of note, cardiologists consistently (32/32) use a target heart rate of ≤ 65 bpm, whereas 18% (14/79) of radiologists set a higher target. Using categories of ≤ 65 and > 65 bpm, differences in target heart rate across specialty were statistically significant (p = 0.007), but no significant differences were seen across experience levels (p = 0.7).


View this table:
[in this window]
[in a new window]

 
TABLE 3: Target Heart Rate Before 64-MDCT Coronary Angiography in 141 Sites

 

Despite the target heart rate commonly being ≤ 65 bpm, the maximum allowable heart rate, reported by 141 centers, ranged from 59 bpm to any heart rate (Table 4). A cutoff higher than 65 bpm is used by 80% (113/141) of sites. The most commonly reported values were 65 (n = 15), 70 (n = 36), 75 (n = 16), and 80 (n = 15) bpm. Using categories of < 75, 75–80, and > 80 bpm, no significant difference was seen in experience level or specialty that dictated the maximum allowable heart rate (p = 0.4–0.7).


View this table:
[in this window]
[in a new window]

 
TABLE 4: Maximum Allowable Heart Rate Reported by 141 Sites

 

When asked if they scan patients with arrhythmias, 25% (35/138) of sites simply answered yes, 6% (8/138) supplemented the answer by writing that they scan only with ectopic beats (n = 7) or bradycardia (n = 1), and 38% (53/138) answered no. The remaining 30% (42/138) wrote in a conditional response. Although the difference in practice was significant across experience levels (p = 0.006), data analysis did not reveal a practice pattern evolving from increasing level of experience (Table 5).


View this table:
[in this window]
[in a new window]

 
TABLE 5: Policy for Scanning Patients with Arrhythmias Based on Experience Level, as Reported by 132 Sites

 

With respect to other medications, 84% (119/142) of centers administer nitroglycerin. Of the 131 centers who responded to the question about whether they use calcium channel blockers, 27% (35/131) reported they do, and 26% of these (9/35) wrote that this was only in the setting of a β-blocker contraindication. Other medications, reported by 14 centers, include benzodiazepines (n = 6), lidocaine (n = 5), Mucomyst [acetylcysteine, Bristol-Myers Squibb] (n = 2), atropine (n = 2), and digoxin (n = 1).


Discussion
Top
Abstract
Introduction
Materials and Methods
Results
Discussion
References
 
The improvements in both temporal and spatial resolutions resulting from 64-MDCT affect different facets of coronary artery MDCT. When acquisition parameters for isotropic resolution are optimized, smaller vessels are better visualized with less motion artifact [10]. The improved temporal resolution facilitates acquisition timing during peak arterial perfusion and the coupling of contrast infusion with data acquisition. Temporal resolution is 165–185 milliseconds for single-segment reconstruction with gantry rotation speeds of 330–370 milliseconds on a 64-MDCT scanner but ranged from 84 to 157 milliseconds using dual-segment reconstruction and a gantry rotation speed of 330 milliseconds in one cardiac study [11]. Despite these advances in MDCT technology that have improved data set quality, proper patient preparation remains imperative to maximize the window of optimal data acquisition.

The increased speed of 16-MDCT over earlier generation MDCT scanners did not obviate the requirement for heart rate control [1215], and neither has 64-MDCT technology, according to published studies [11, 16]. With 16-MDCT, a heart rate < 80 bpm minimizes motion artifact, but highest image quality was seen in patients with a mean heart rate of 60 bpm [12]. Cademartiri et al. [13] have also shown that increasing heart rate decreases diagnostic accuracy. In patients who have not received β-blockers and have a heart rate > 64–68.5 bpm, reconstruction of data during end-systole or early diastole improves image quality [14]. Using 64-MDCT, a heart rate of ≤ 65 bpm results in significantly improved image quality for the left anterior descending, left circumflex, and right coronary arteries [11]. Control of heart rate and rhythm with β-blockers has been shown to increase the percentage of coronary segments with acceptable 16-MDCT image quality from 58–96% to 87–100%, depending on the arterial territory [15]. Using 64-MDCT, patients receiving β-blockers as part of their baseline medications had significantly decreased heart rate variability, resulting in improved image quality for all vessels [16].

Accordingly, it is not surprising that all centers administer β-blockers. Among the centers surveyed, a greater percentage of examinations are performed by radiologists (Table 1), accounting for the higher percentage of radiologists administering premedication. The route varies across specialty, and cardiologists more commonly supplement oral β-blockers with IV. Theoretic explanations for more frequent supplementation with IV β-blockers by cardiologists include a higher comfort level in administering the medication IV and that the target heart rate was uniformly lower among cardiologists. Future analysis of the remaining data from the survey will be used to determine whether the scanner site (inpatient vs outpatient) has an impact on the premedication regimen. The practice of initiating oral β-blockers the day before the study is facilitated by cardiologists' knowledge of the patient's medical history and current medications, and their access to the patient before the study.

At the time of this survey, when experience levels were lower, cardiology sites comprised the majority of those with high experience levels. Several explanations are possible. Before implementing 64-MDCT, a cardiology practice likely determines that they have adequate volume to support utilization. Furthermore, their scanners are probably dedicated to cardiac CT, whereas a radiology department's CT volume includes other regions of the body.

A notable discrepancy was identified when comparing target heart rate with maximum allowable heart rate. Despite the usual goal of ≤ 65 bpm, both radiologists and cardiologists, and sites with all experience levels, will scan across a range of heart rates. Nearly one third of centers scan patients with arrhythmias; however, we did not inquire about the specific rhythm irregularities that were deemed acceptable in each center. Correlation of results with experience level revealed significant differences; however, this analysis did not reflect a pattern evolving from increasing experience level. A lack of consensus among experts with respect to scanning in the setting of an arrhythmia persists even a year after this survey was conducted. It would be useful to determine more detailed information from highly experienced sites with respect to specific rhythm irregularities that are more or less amenable to 64-MDCT angiography.

Nitroglycerin is routinely administered (84% of sites) and has been recommended because it significantly increases the diameter of the proximal coronary artery at MDCT [17]. A small percentage of sites (27%) reported that they administer calcium channel blockers. Although some listed their division's indications for this medication, the survey did not inquire in detail about whether this was a routinely administered medication or limited to patients with contraindications to β-blockers (the latter probably because β-blockers are more effective). Few centers listed other medications, most commonly anxiolytics or lidocaine to suppress ectopy.

This study has several limitations. Administration of the survey by a radiology department may have enhanced the percentage of radiologists responding; however, participating cardiologists expressed enthusiasm for the study. Analysis of the data elucidated details that were lacking from the questionnaire, including the heart rate threshold that dictates β-blocker administration in each division, whether additional β-blockers are administered to those who routinely take these medications, whether calcium channel blockers were administered on an as-needed basis or routinely, and who dictates the maximum allowable heart rate and acceptable heart rhythm (physician administering β-blocker or physician acquiring CT data set). The response rate might have been higher; however, our rate of 27% is similar to that of a recent nationwide survey on CT pulmonary angiography [18] and is within the range of other CT practice surveys [1922]. The response rate was per-letter rather than per-institution, and because the questionnaires were designed to be anonymous, we are unable to determine the response rate per institution. At least four participating institutions that received multiple surveys contacted us and were instructed to submit only one survey, despite the fact that they had multiple 64-MDCT scanners performing coronary CTA. Also, additional sites that were sent letters may have implemented 64-MDCT but were not yet using it to perform coronary angiography. We believe that our method of querying sites that have installed the technology was sufficient to survey the maximum number of sites performing MDCT coronary angiography at this time.

In conclusion, our data suggest that radiologists constituted a larger percentage of sites performing MDCT coronary angiography in 2006. However, a greater percentage of the cardiology centers that participated in this study had high experience levels at the time of the survey. Routine practice includes administration of β-blockers and nitroglycerin before scanning. Cardiologists frequently administer the first oral β-blocker dose the day or night before the study and are more likely to supplement an oral β-blocker with an IV β-blocker. The target heart rate before performance of 64-MDCT is usually ≤ 65 bpm, particularly among cardiologists. Results revealed considerable variation in acceptable heart rate and rhythm for scanning. Despite the fact that coronary artery MDCT is a new procedure, the consensus for many key parameters suggests that the basics of the study are becoming well defined. These findings should facilitate implementation by new sites beginning this practice because they can build on the experience of others.


References
Top
Abstract
Introduction
Materials and Methods
Results
Discussion
References
 

  1. Fine JJ, Hopkins CB, Ruff N, Newton FC. Comparison of accuracy of 64-slice cardiovascular computed tomography with coronary angiography in patients with suspected coronary artery disease. Am J Cardiol 2006; 97:173 –174[CrossRef][Medline]
  2. Pugliese F, Mollet NRA, Runza G, et al. Diagnostic accuracy of non-invasive 64-slice CT coronary angiography in patients with stable angina pectoris. Eur Radiol 2006;16 : 575–582[CrossRef][Medline]
  3. Ehara M, Surmely J-F, Kawai M, et al. Diagnostic accuracy of 64-slice computed tomography for detecting angiographically significant coronary artery stenosis in an unselected consecutive patient population: comparison with conventional invasive angiography. Circ J 2006; 70:564 –571[CrossRef][Medline]
  4. Leschka S, Alkadhi H, Plass A, et al. Accuracy of MSCT coronary angiography with 64-slice technology: first experience. Eur Heart J 2005; 26:1482 –1487. Epub ahead of print 2005Apr 19[Abstract/Free Full Text]
  5. Mollet NR, Cademartiri F, van Mieghem CAG, et al. High-resolution spiral computed tomography coronary angiography in patients referred for diagnostic conventional coronary angiography. Circulation 2005;112 :2318 –2323[Abstract/Free Full Text]
  6. Nikolaou K, Knez A, Rist C, et al. Accuracy of 64-MDCT in the diagnosis of ischemic heart disease. AJR2006; 187:111 –117[Abstract/Free Full Text]
  7. Ong TK, Chin SP, Liew CK, et al. Accuracy of 64-row multidetector computed tomography in detecting coronary artery disease in 134 symptomatic patients: influence of calcification. Am Heart J2006; 151:1323.e1 –e6
  8. Ropers D, Rixe J, Anders K, et al. Usefulness of multidetector row spiral computed tomography with 64- x 0.6-mm collimation and 330-ms rotation for the noninvasive detection of significant coronary artery stenoses. Am J Cardiol 2006;97 : 343–348[CrossRef][Medline]
  9. Schuijf JD, Pundziute G, Jukema W, et al. Diagnostic accuracy of 64-slice multislice computed tomography in the noninvasive evaluation of significant coronary artery disease. Am J Cardiol2006; 98:145 –148[CrossRef][Medline]
  10. Pannu HK, Jacobs JE, Lai S, Fishman EK. Coronary CT angiography with 64-MDCT: assessment of vessel visibility. AJR2006; 187:119 –126[Abstract/Free Full Text]
  11. Wintersperger BJ, Nikolaou K, von Ziegler F, et al. Image quality, motion artifacts, and reconstruction timing of 64-slice coronary computed tomography angiography with 0.33-second rotation speed. Invest Radiol 2006; 41:436 –442[CrossRef][Medline]
  12. Hoffmann MHK, Shi H, Manzke R, et al. Noninvasive coronary angiography with 16-detector row CT: effect of heart rate. Radiology 2005;234 : 86–97[Abstract/Free Full Text]
  13. Cademartiri F, Mollet NR, Runz G, et al. Diagnostic accuracy of multislice computed tomography angiography is improved at low heart rates. Int J Cardiov Imaging 2006;22 : 101–105; Epub ahead of print 2005 Aug 3[CrossRef]
  14. Herzog C, Arning-Erb M, Zangos S, et al. Multi-detector row CT coronary angiography: influence of reconstruction technique and heart rate on image quality. Radiology 2006;238 : 75–86[Abstract/Free Full Text]
  15. Shim SS, Kim Y, Lim SM. Improvement of image quality with β-blocker premedication on ECG-gated 16-MDCT coronary angiography. AJR 2005; 184:649 –654[Abstract/Free Full Text]
  16. Leschka S, Wildermuth S, Boehm T, et al. Noninvasive coronary angiography with 64-section CT: effect of average heart rate and heart rate variability on image quality. Radiology2006; 241:378 –385[Abstract/Free Full Text]
  17. Dewey M, Hoffmann H, Hamm B. Multislice CT coronary angiography: effect of sublingual nitroglycerine on the diameter of the coronary arteries. Rofo Fortschr Geb Rontgenstr Neuen Bildgeb Verfahr2006; 178:600 –604[Medline]
  18. Weiss CR, Scatarige JC, Diette BG, Haponik EF, Merriman B, Fishman EK. CT pulmonary angiography is the first-line imaging test for acute pulmonary embolism: a survey of US clinicians. Acad Radiol 2006; 13:434 –446[CrossRef][Medline]
  19. Kaste S, Laningham F, Stazzone M, et al. Safety in pediatric MR and cardiac CT: results of a membership survey of the Society for Pediatric Radiology–2006. Pediatr Radiol2007; 37:409 –412; Epub ahead of print 2007Feb 27[CrossRef][Medline]
  20. Barish MA, Soto JA, Ferrucci JT. Consensus on current clinical practice of virtual colonoscopy. AJR2005; 184:786 –792[Abstract/Free Full Text]
  21. Schuster ME, Fishman JE, Copeland JF, Hatabu H, Boiselle PM. Pulmonary embolism in pregnant patients: a survey of practices and policies for CT pulmonary angiography. AJR 2003;181 :1495 –1498[Abstract/Free Full Text]
  22. O'Malley ME, Halpern E, Mueller PR, Gazelle GS. Helical CT protocols for the abdomen and pelvis: a survey. AJR2000; 175:109 –113[Abstract/Free Full Text]

Add to CiteULike CiteULike   Add to Complore Complore   Add to Connotea Connotea   Add to Del.icio.us Del.icio.us   Add to Digg Digg   Add to Reddit Reddit   Add to Technorati Technorati    What's this?


This article has been cited by other articles:


Home page
Am. J. Roentgenol.Home page
P. T. Johnson, H. K. Pannu, and E. K. Fishman
IV Contrast Infusion for Coronary Artery CT Angiography: Literature Review and Results of a Nationwide Survey
Am. J. Roentgenol., May 1, 2009; 192(5): W214 - W221.
[Abstract] [Full Text] [PDF]


Home page
Am. J. Roentgenol.Home page
R. J. Stanley
Reflections on This Month's Wealth of Content
Am. J. Roentgenol., March 1, 2008; 190(3): 555 - 555.
[Full Text] [PDF]


This Article
Right arrow Abstract Freely available
Right arrow Figures Only
Right arrow Full Text (PDF)
Right arrow Alert me when this article is cited
Right arrow Alert me if a correction is posted
Right arrow Citation Map
Services
Right arrow Email this article to a friend
Right arrow Similar articles in this journal
Right arrow Similar articles in PubMed
Right arrow Alert me to new issues of the journal
Right arrow Download to citation manager
Right arrow reprints & permissions
Citing Articles
Right arrow Citing Articles via HighWire
Right arrow Citing Articles via Google Scholar
Google Scholar
Right arrow Articles by Johnson, P. T.
Right arrow Articles by Fishman, E. K.
Right arrow Search for Related Content
PubMed
Right arrow PubMed Citation
Right arrow Articles by Johnson, P. T.
Right arrow Articles by Fishman, E. K.
Social Bookmarking
 Add to CiteULike   Add to Complore   Add to Connotea   Add to Del.icio.us   Add to Digg   Add to Reddit   Add to Technorati  
What's this?
Hotlight (NEW!)
Right arrow
What's Hotlight?


HOME HELP FEEDBACK SUBSCRIPTIONS ARCHIVE SEARCH TABLE OF CONTENTS